Thèse MAZEL Diversité Des Mamifères Et Biogéographie

Comprendre et protéger la diversité des mammifères :
une approche de biogéographie évolutive et fonctionnelle

à l’échelle du globe.
Florent Mazel
To cite this version:

Florent Mazel. Comprendre et protéger la diversité des mammifères : une approche de biogéographie
évolutive et fonctionnelle à l’échelle du globe.. Ecologie, Environnement. Université Grenoble Alpes,
2015. Français. �NNT : 2015GREAV063�. �tel-01684747�
HAL Id: tel-01684747

https://tel.archives-ouvertes.fr/tel-01684747
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THÈSE
Pour obtenir le grade de
DOCTEUR DE L’UNIVERSITÉ GRENOBLE ALPES

Spécialité : Biodiversité Écologie Environnement
Arrêté ministériel : 7 août 2006
Présentée par
Florent MAZEL
Thèse dirigée par Wilfried Thuiller

codirigée par Sébastien Lavergne
préparée au sein du Laboratoire d’Écologie Alpine

dans l'École Doctorale de Chimie et des Sciences du Vivant
Comprendre et protéger la diversité

des mammifères : une approche de
biogéographie évolutive et
fonctionnelle à l’échelle du globe.
Thèse soutenue publiquement le 14 décembre 2015,

devant le jury composé de :
M. Miguel ARAÚJO
Professeur à l’Université de Madrid, Rapporteur et président du jury.
M. Olivier HARDY
Maïtre de Recherches à l’Université de Bruxelles, Rapporteur
M. Fabien LEPRIEUR
Maître de conférence à l’Université de Montpellier, Examinateur
M. Frédéric DELSUC
Chargé de Recherche à l’Université de Montpellier, Examinateur
M. Francesco FICETOLA
Chargé de Recherche à l’Université Grenoble Alpes,Examinateur
M. Sébastien LAVERGNE
Chargé de Recherche à l’Université Grenoble Alpes, Co-directeur de
thèse, Invité
M. Wilfried THUILLER
Directeur de Recherche à l’Université Grenoble Alpes, Directeur de thèse
!
!
!
À!mon!père!
!
!
!
Sommaire!
SOMMAIRE(GÉNÉRAL(
(
LISTE(DES(ARTICLES( ( ( ( ( ( ( ( ( 5(
LISTE(DES(ANNEXES( ( ( ( ( ( ( ( ( 6(
!
INTRODUCTION(GÉNÉRALE( ( ( ( ( ( ( ( 8(
(
PARTIE(I.(Classer(la(diversité(des(diversités((
phylogénétiques(et(fonctionnelles( ( ( ( ( ( ( 48(
(
Chapitre!I.!Tentative!de!synthèse!exhaustive! ! ! ! ! ! 58!
Chapitre!II.!L’importance!de!l’échelle!évolutive! ! ! ! ! ! 90!
!
PARTIE(II.(Utiliser(les(diversités(phylogénétiques(et(fonctionnelles((
en(conservation( ( ( ( ( ( ( ( ( ( 118(
!
Chapitre!III.!Quantification!de!l’érosion!de!la!diversité!phylogénétique! ! 128!
Chapitre!IV.!Les!points!chauds!de!diversité!fonctionnelle!et!phylogénétique! ! 140!
!
PARTIE(III.(Utiliser(les(diversités(phylogénétiques(et(fonctionnelles(pour(
comprendre(certains(patrons(biogéographiques( ( ( ( ( 170(
(
SOUS$PARTIE$III.1(
Chapitre!V.!L’environnement!et!l’espace!modulent!la!répartition!mondiale!!
des!oiseaux!et!mammifères!à!différentes!échelles!phylogénétiques! ! ! 184!
!
Chapitre!VI.!Le!régime!alimentaire!et!la!phylogénie!de!l’hôte!modulent!!
la!composition!des!microbiotes!à!différentes!échelles!phylogénétiques! ! 198!
!
SOUS$PARTIE$III.2$
Chapitre!VII.!La!convergence!évolutive!des!assemblages!de!mammifères! ! 222!
!
CONCLUSION(GÉNÉRALE(( ( ( ( ( ( ( ( 254(
GLOSSAIRE( ( ( ( ( ( ( ( ( ( ( 258(
ANNEXES( ( ( ( ( ( ( ( ( ( ( 262(
!
)!4!)!
Contributions!
LISTE(DES(ARTICLES(
(
PARTIE(I.((
(
Article(1.!C.!M.!Tucker,!M.!W.!Cadotte,!S.!B.!Carvalho,!!J.!T.!Davies,!S.!Ferrier,!S.!A.!Fritz,!R.!
Grenyer,!M.!R.!Helmus,!L.!S.!Jin,!A.!O.!Mooers,!S.!Pavoine,!O.!Purschke,!D.!W.!Redding,!D.!F.!
Rosauer,! ! M.! Winter,! F.( Mazel.! A$ unification$ of$ phylogenetic$ metrics$ for$ conservation,$
community$ecology$and$macroecology.$En!révision!dans!Biological$Reviews!
Article( 2.! F.( Mazel,! Davies,! T.J,! Gallien! L.,! Groussin,! M.,! Münkemüller! T.! &! Thuiller,! W.!
Influence$ of$ tree$ shape$ and$ evolutionary$ timeDscale$ on$ phylogenetic$ diversity$ metrics.$
Accepté!dans!Ecography(
Article(3.!D.W.!Redding,!F.!Mazel,!and.!A.O.!Mooers.!Measuring$evolutionary$isolation$for$
conservation.$PloS$one,!9(12),!e113490.(
!
PARTIE(II.((
!
Article( 4.! F.( Mazel,! J.! Renaud,! F.! Guilhaumon,! D.! Mouillot,! D.! Gravel! &! W.! Thuiller.!
Mammalian$ phylogenetic$ diversity$ area$ relationships$ at$ a$ continental$ scale$ (2015).$
Ecology,$96$(10),$2814D2822!
Article( 5.!F.!Mazel,!F.!Guilhaumon,!N.!Mouquet,!V.!Devictor,!D.!Gravel,!J.!Renaud,!M.!V.!
Cianciaruso,! R.D.! Loyola,! J.A.F.! Diniz)Filho,! D.! Mouillot! and! W.! Thuiller! (2014)!
Multifaceted$ diversityDarea$ relationships$ reveal$ global$ hotspots$ of$ mammalian$ species,$
trait$and$lineage$diversity.$GEB,!23,!836–847(
Article(6.!W.!Thuiller,!L.!Maiorano,!L.,!F.!Mazel,!F.!Guilhaumon,!G.F.!Ficetola,!S.!Lavergne,!
S.,! J.! Renaud,! J.,! C.! Roquet! and! D.! Mouillot! (2015).! Conserving! the! functional! and!
phylogenetic! trees! of! life! of! European! tetrapods.! Phil.$ Trans.$ of$ the$ Royal$ Society$ of$
London$B:$Biological$Sciences,!370(1662),!2014.!
! !
!
)!5!)!
Contributions!
PARTIE(III.((
(
Article( 7.!F.( Mazel,!R.!Wüest,!J.!Renaud,!S.!Lavergne!and!W.!Thuiller.!Decomposing!the!
global! beta! diversity! of! mammals! and! birds! along! evolutionary! scale! reveal! the!
differential!effects!of!space!and!contemporary!climate.!En!préparation.!
Article( 8.!M.!Groussin*,!F.( Mazel*,!J.!Sanders,!C.!Smillie,!S.!Lavergne,!W.!Thuiller!and!E.!
Alm.!Selecting!the!bacterial!lineages!living!in!guts!of!mammals.!En!préparation(
Article(9.!F.(Mazel,!T.!J.!Davies,!D.!Georges,!S.!Lavergne,!W.!Thuiller!and!P.!R.!Peres)Neto.!!
Improving$ phylogenetic$ regression$ under$ complex$ evolutionary$ models.$ Accepté! dans!
Ecology!
Article( 10.! F.( Mazel,! R.! Wüest,! J.! Renaud,! S.! Lavergne! and! W.! Thuiller.! The$ global$
biogeography$of$nonDneutral$trait$evolution$in$mammals.$En!préparation!
!
LISTE(DES(ANNEXES(
PARTIE(I.((
(
Annexe!1.1.!Matériel!supplémentaire!de!l’article!1!
Annexe!1.3.!Article!3!
Annexe!1.4.!Résumé!d’un!article!additionnel!
!
PARTIE(II.((
!
Annexe!2.3.!Article!6!
!
PARTIE(III.((
(
Annexe!3.1.1.!Matériel!supplémentaire!de!l’article!7!
Annexe!3.2.1.!Article!9!
!
)!6!)!
!
!
)!7!)!
Introduction!générale!
INTRODUCTION(GÉNÉRALE(
!
!
!
!
«!…!that!grand!subject,!
that!almost!keystone!of!the!laws!of!creation!
)!Geographical!Distribution.!»!
C.!Darwin!
Dans!une!lettre!à!J.D.!Hooker,!1845
!
)!8!)!
!
! !
Figure'1.''Phytogéographie'du'Mont'Chimborazo'(Equateur)."La"figure"présente"un"
dessin"de"Humboldt""(1805)"décrivant"la"répar>>on"des"plantes"sur"les"flancs"du"mont"
Chimborazo.""""""
!
)!9!)!
1.(Les(origines(du(questionnement(biogéographique(
!
«$On$ne$connaît$pas$complètement$une$science$tant$qu’on$n’en$sait$pas$l’histoire$»$
Auguste!Comte!
Cours!de!philosophie!positive!(1830)1842)!
!
Pourquoi! des! régions! géographiques! différentes! abritent)elles! des! espèces!
différentes?! Pourquoi! certaines! en! possèdent! davantage?! Ces! questions! reflètent! les!
principales! problématiques! des! biogéographes! et! ont! constitué! le! fil! directeur! de! mon!
travail!de!thèse.!
La! biogéographie! décrit! et! tente! de! comprendre! «!la! géographie! de! la! nature!»!
(Lomolino!et!al.!2010),!c’est)à)dire!la!distribution!)!dans!l’espace!et!dans!le!temps!)!des!
êtres! vivant! sur! terre.! Ce! vaste! objectif! n’est! pas! nouveau.! En! effet,! les! populations! de!
chasseurs)cueilleurs! du! Paléolithique! savaient! déjà! très! probablement! localiser! leur!
nourriture!et!leurs!prédateurs!(Ladle!and!Whittaker!2011).!Au!delà!de!cette!origine!très!
lointaine,! de! nombreux! auteurs! ont,! au! cours! de! l’histoire,! décrit! la! répartition!
géographique! des! êtres! vivants!:! c’est! par! exemple! le! cas! du! philosophe! grec!
Théophraste! (371! à! 228! av.! JC)! ou! encore! de! celui! de! l’écrivain! et! naturaliste! romain!
Pline! l’Ancien! (23! à! 79! ap.! JC).! De! telles! descriptions! étaient! cependant! difficilement!
comparables! puisqu’elles! ne! reposaient! pas! sur! le! même! système! de! classification! des!
êtres! vivants.! Il! faudra! attendre! le! XVIIIème! siècle! et! la! classification! binomiale! de! Carl!
von!Linné!(1707)1778)!pour!disposer!d’une!nomenclature!solide!permettant!de!mener!
des!études!biogéographiques.!Un!nom!d’espèce!devra!alors!se!composer!de!deux!mots!
en!latin,!le!premier!donnant!le!nom!de!genre!auquel!l’espèce!appartient!et!le!deuxième!le!
nom!de!l’espèce!à!l’intérieur!du!genre!(par!exemple,!les!humains!appartiennent!au!genre!
Homo$ et! à! l’intérieur! de! ce! genre! à! l’espèce$ Homo$ sapiens).! C’est! finalement! sous!
l’impulsion!de!grandes!campagnes!d’exploration!biologique!à!travers!le!monde!(voir!les!
flèches! orange! de! l’encadré! 1,! page! 13)! que! la! biogéographie! a! connu! un! essor!
spectaculaire! au! XIXème! siècle.! Alexander! von! Humboldt! (1769)1859)! a! par! exemple!
méticuleusement!décrit!la!répartition!des!plantes!sur!les!flancs!du!volcan!Teide!sur!l’île!
de!Tenerife!ou!du!Chimborazo!en!Equateur!(Humbolt!and!Bonpland!1805).!Ses!études!
de! l’étagement! de! la! végétation! ont! d’ailleurs! fourni! des! représentations!
cartographiques!emblématiques!(voir!Figure!1).!
!
)!10!)!
! !
1.#By#Wallace#(1876)#
2.#By#Holt#et#al.#(2009)#
Figure(2.(Régions!Zoo0géographiques!du!monde.$La!figure!présente!deux!versions!des!
grandes!provinces!biogéographiques!du!monde!basées!sur!les!distributions!de!certains!
vertébrés!terrestres.!
!
)!11!)!
Ses! travaux! et! voyages! ont! alors! inspiré! une! génération! de! naturalistes! du! milieu! du!
XIXème! siècle,! notamment! Charles! Darwin! (1809)1882),! Alfred! Russel! Wallace! (1823)
1913)!ou!encore!Joseph!Dalton!Hooker!(1817)1911).!Au!cours!de!nouvelles!expéditions!
scientifiques!de!plusieurs!années,!ces!derniers!ont!amassé!une!quantité!considérable!de!
nouvelles! données! et! ont! jeté! les! bases! de! la! biogéographie! moderne! (Sclater! 1858,!
Darwin! 1859,! Wallace! 1876).! Ces! découvertes! et! leurs! intégrations! à! large! échelle!
spatiale!ont!permis!à!Alfred!Russel!Wallace!(1876)!de!décrire!deux!des!plus!frappants!
patrons!de!la!biogéographie!mondiale:!!
!
«!Animal$life$is,$on$the$whole,$far$more$abundant$and$more$varied$in$the$tropics$than$in$any$
other$part$of$the$globe$»!!
Wallace,!1876!
!
Le!gradient!latitudinal!de!diversité!décrit!ici!par!Wallace!atteste!du!fait!qu’il!y!a!
davantage! d’espèces! dans! les! tropiques! que! dans! les! régions! tempérées.! Ce! patron,!
documenté! à! l’époque! pour! les! animaux,! est! en! fait! généralisable! à! un! grand! nombre!
d’êtres!vivants!(Hillebrand!2004).!!
$
«$Zoological$regions$[…]$are$the$most$recent$natural$primary$divisions$of$the$earth$as$
regards$to$its$forms$of$animal$life$»$
Wallace,!1876!
$
Wallace! décrit! ici! un! provincialisme! à! large! échelle! spatiale,! c’est! à! dire! «!la!
présence!simultanée!d’un!grand!nombre!de!formes!endémiques!bien!différenciées!dans!
une! région!»! (Lomolino! et! al.! 2010).! Il! découpera! ainsi! le! monde! en! six! régions!
biogéographiques!distinctes!(Wallace!1876,!figure!2.1),!en!se!basant!notamment!sur!les!
travaux!de!Sclater!(1858).!Ce!découpage!du!monde!a!été!utilisé!pendant!très!longtemps!
et!ce!n’est!que!relativement!récemment!qu’il!a!été!réactualisé!(Kreft!&!Jetz!2007;!Holt!et$
al.!2013,!figure!2.2).!On!se!rend!alors!compte!à!quel!point!Wallace!et!ses!prédécesseurs!
avaient! déjà! atteint! une! précision! exceptionnelle! pour! l’époque! (comparez! les! deux!
régionalisations!de!la!figure!2).!
! !
!
)!12!)!
Encadré(1.(Un(bref(aperçu(de(l’histoire(de(la(biogéographie(
!
C.#Elton#
A.#R.##Wallace#
E.#O.#Wilson#&#R.#MacArthur##
C.#Lyell# J.#Grinnell# G.#Nelson#&#N.#Platnick#
1800$ 1850$ 1900$ 1950$ 2000$
Actualisme# Dérive#conKnentale#
EvoluKonisme# Synthèse#moderne#
Vicariance#biogeography#
Biogéographie#de#la#dispersion# Biogéographie#phylogénéKque##
Biogéographie#vicariante#
!
A.#von#Humboldt# E.#Mayr#
)!13!)!
C.#Darwin# G.#G.#Simpson#
A.#De#Candolle# L.#Croizat#
L.#Brundin#
Légende(
Date$d’une$publica5on$ Ecologie$$
$clef$de$l’auteur$ A.#von#Humboldt# Evolu5on$
Expédi5on$clef$de$l’auteur$ Géologie$
EvoluKonisme# Concepts$ Pères$fondateurs$
Vie$de$l’auteur*$
Biogéographie$historique$
Ce$document$n’a$pas$pour$objec5f$de$retracer$toute$l’histoire$de$la$biogéographie$(voir$Lomolino$et#al.$2010),$mais$simplement$d’en$
souligner$les$grandes$lignes.$*$Lorsque$deux$auteurs$sont$notés,$la$durée$de$vie$correspond$à$celle$du$premier.$
Cette! description! de! la! répartition! des! espèces! est! une! étape! fondamentale! de!
l’enquête!biogéographique.!Elle!ne!constitue!cependant!que!le!premier!pas!vers!ses!deux!
objectifs! majeurs.! Le! premier! –!fondamental!–! réside! dans! la! compréhension! des!
processus! sous)tendant! ces! distributions! (Diamond! 1975,! Lomolino! et! al.! 2010).! Le!
second! –!appliqué!–! est! d’informer! la! société! sur! les! conséquences! biologiques! des!
changements! globaux! provoqués! par! l’homme! et,! éventuellement,! de! proposer! des!
solutions!pour!conserver!les!espèces!(Whittaker!et!al.!2005).!!
!
!
Dans! cette! introduction,! je! propose! d’abord! de! brefs! rappels! sur! les! processus!
fondamentaux! contrôlant! la! distribution! des! espèces! et! les! bases! conceptuelles! de! la!
conservation! de! la! biodiversité! (points! 2! et! 3).! Je! présente! ensuite! les! questions!
générales!de!ma!thèse!et!l’approche!qui!m’a!permis!d’y!répondre!(point!4).!Puis!je!décris!
les! données! utilisées! (point! 5)! et! la! logique! de! l’organisation! générale! de! mon! travail!
(point!6).!
!
! !
!
)!14!)!
2.(Comprendre(la(distribution(des(espèces(:(les(forçages(fondamentaux(
(
La!répartition!des!espèces!repose!traditionnellement!sur!deux!types!de!facteurs!:!
les!facteurs!écologiques!(biogéographie!écologique,!reportée!en!vert!dans!l’encadré!1)!et!
les!facteurs!historiques!(biogéographie!historique,!reportée!en!rouge!dans!l’encadré!1)!
(Morrone!and!Crisci!1995,!Lomolino!et!al.!2010).!
(
(
2.1.(La(niche(écologique(et(la(biogéographie(écologique(
(
Von! Humboldt! (1805)! avait! remarqué! que! les! plantes! s’étageaient! le! long! des!
gradients!altitudinaux!(figure!1).!La!formalisation!de!la!relation!entre!la!distribution!des!
espèces!et!les!conditions!environnementales!n’est!pourtant!établie!qu’au!début!du!XXème!
siècle.!C’est!en!effet!Grinnell!(1917)!qui!pour!la!première!fois!a!défini!la!niche!écologique!
d’une!espèce!comme!l’ensemble!des!conditions!environnementales!dans!lesquelles!elle!
peut! survivre! et! se! reproduire.! En! effet,! des! contraintes! physiologiques! peuvent!
empêcher!le!maintien!d’une!population!dans!un!environnement!donné,!par!exemple!le!
froid!pour!certains!oiseaux!nord)américains!(Root!1988a,!b)!ou!le!taux!de!dessiccation!
pour! certains! crustacés! vivant! sur! les! rochers! de! l’estran! (i.e.! la! zone! littorale! située!
entre!les!limites!extrêmes!des!plus!hautes!et!des!plus!basses!marées,!Connell!1961).!!
Une!autre!vision!de!la!niche!a!été!proposée!par!Elton!(1927)!:!la!niche!d’une!espèce!est!
considérée! comme! l’ensemble! des! fonctions! assurées! par! celle–ci! au! sein! d’un!
écosystème,!c’est!en!d’autres!termes!«!son!statut!dans!la!communauté!»!(Elton!1927).!La!
niche!«!Grinnellienne!»!se!concentre!donc!sur!les!effets!de!l’environnement!sur!l’espèce!
alors! que! la! niche! «!Eltoniennne!»! se! concentre! sur! les! effets! de! l’espèce! ! sur!
l’environnement.!!
! Hutchinson! (1957)! propose! de! relier! le! concept! de! niche! écologique! aux!
ressources! nécessaires! à! la! survie! et! à! la! reproduction! de! l’espèce.! En! incorporant! les!
travaux! de! Gause! (1934)! sur! la! compétition! entre! espèces! pour! l’utilisation! des!
ressources! du! milieu,! il! définit! ainsi! deux! types! de! niche.! L’ensemble! des! conditions!
abiotiques!permettant!la!survie!de!l’espèce!sans!interactions!biotiques!et!sans!limitation!
de! la! dispersion! correspond! à! la( niche( fondamentale! de! l’espèce.! La! niche( réalisée(
représente,! quant! à! elle,! les! conditions! environnementales! dans! lesquelles! on! observe!
!
)!15!)!
l’espèce!dans!la!nature.!La!niche!réalisée!n’est!donc!dans!certains!cas!qu’une!sous)partie!
de! la! niche! fondamentale.! En! effet,! les! capacités! de! dispersion! des! espèces! n’étant! pas!
infinies,! l’absence! d’une! espèce! dans! une! région! donnée! ne! signifie! pas! forcément! que!
les!conditions!environnementales!ne!s’y!prêtent!pas,!mais!peut!simplement!être!due!au!
fait!que!l’espèce!n’a!pas!encore!atteint!la!région.!Il!est!aussi!admis!que!les!interactions!
biotiques! (prédation,! compétition,! facilitation)! peuvent! restreindre! ou! élargir! la! niche!
réalisée.! Par! exemple,! les! expériences! de! transplantation! de! Connell! (1961)! montrent!
qu’une! espèce! de! balane! (Balanus! balanoides)! présente! naturellement! dans! la! zone!
haute!de!l’estran!(la!niche!réalisée!de!l’espèce)!peut!survivre!dans!des!zones!plus!basses!
en! l’absence! de! compétiteurs! (i.e.! cette! zone! est! incluse! dans! la! niche! fondamentale).!
Cependant! elle! se! trouve! exclue! par! la! chthamale! (Chthalamus$ stellatus),! plus!
compétitrice,!naturellement!présente!dans!cette!zone!basse.!Il!est!aussi!possible!que!la!
niche! réalisée! d’une! espèce! soit! plus! étendue! que! sa! niche! fondamentale! si! des!
interactions! positives! ou! des! processus! de! type! source)puits! le! lui! permettent.! Par!
exemple,! la! présence! de! certaines! plantes! en! coussin! permet! l’installation! d’autres!
espèces!dans!des!conditions!abiotiques!qu’elles!n’occupent!normalement!pas!(processus!
de!facilitation).!!
!
La!nature!de!la!niche!écologique!des!espèces!repose!souvent!sur!des!adaptations!
morphologiques,! physiologiques! ou! phénologiques.! Par! exemple,! les! espèces! de!
crustacés!vivant!dans!le!haut!de!l’estran!possèdent!des!adaptations!physiologiques!leur!
permettant! de! résister! à! la! dessiccation.! Ces! adaptations! leur! permettent! donc! d’être!
présentes!dans!un!espace!environnemental!particulier.!Ainsi!les!traits!fonctionnels!vont!
permettre!de!caractériser!la!niche!écologique!des!espèces.!Un!trait!fonctionnel!est!une!
caractéristique! morphologique,! physiologique! ou! phénologique! d’un! individu! qui! a! un!
impact! indirect! sur! sa! performance! (ou! «!fitness!»,! voir! Violle! et$ al.! 2007).! Ces! traits!
permettent!donc!de!faire!le!lien!entre!les!caractéristiques!des!individus!(ou!des!espèces)!
et!leur!niches!écologiques.!
!
En!définitive,!il!est!possible!de!passer!de!l’espace!environnemental!occupé!(i.e.!la!
niche! écologique! sensu! Grinell)! à! l’espace! géographique! en! connaissant! la! distribution!
dans!l’espace!des!facteurs!environnementaux.!Cette!approche!ne!permet!cependant!pas!
de!rendre!compte!de!toutes!les!observations.!
!
)!16!)!
2.2.(La(diversification(et(la(dispersion(des(organismes(:(la(biogéographie(
historique(
(
(
«$Dans$les$eaux,$nous$ne$trouvons$ni$le$castor$ni$le$rat$musqué,$
$mais$le$coypou$et$le$capybara,$rongeurs$ayant$le$type$sudDaméricain.$[…]$$
Ces$faits$dénotent$l’existence$de$quelque$lien$organique$intime$et$profond$$
qui$prévaut$dans$le$temps$et$l’espace,$[…]$indépendamment$des$conditions$physiques.$$
Il$faudrait$qu’un$naturaliste$fût$bien$indifférent$pour$n’être$pas$tenté$de$rechercher$quel$
peutDêtre$ce$lien.$»$
$
Darwin!(1859)$
!
Dans! cette! citation! tirée! de! L’origine$de$Espèces! (1859)! Darwin! constate! que! les!
facteurs! physiques! ne! permettent! pas! de! rendre! compte! de! certaines! distributions!
disjointes!(i.e.!séparées)!de!certains!taxons.!En!l’occurrence,!la!famille!des!Castoridés!se!
répartit!en!Eurasie!et!en!Amérique!du!Nord!alors!que!celle!des!Cavidés!(dont!font!partie!
les! capybaras)! est! restreinte! à! l’Amérique! du! Sud! (les! deux! familles! appartiennent! à!
l’ordre!des!rongeurs).! Il! existe! en! effet!de!nombreux!groupes!de!mammifères!typiques!
du! continent! sud)américain! qui,! selon! Darwin,! entretiennent! un! «!lien! organique!
intime!»,! c’est)à)dire! une! évolution! et! une! histoire! communes.! La! biogéographie! des!
mammifères! du! continent! sud)américain! en! général! illustre! effectivement! très! bien!
comment! les! explications! de! nature! historique! permettent! de! mieux! comprendre! la!
distribution!des!espèces!et!notamment!d’expliquer!le!provincialisme!de!ce!continent.!Sa!
faune! est! aujourd’hui! composée! par! une! mosaïque! étonnante! de! lignées! propres! à!
l’Amérique! du! Sud! et! de! lignées! beaucoup! plus! cosmopolites! (Encadré! 2).! Cette!
structure!est!le!reflet!d’une!histoire!complexe,!qui!peut!être!en!partie!révélée!grâce!au!
registre! fossile! (Encadré! 3).! On! s’aperçoit! alors! que! le! continent,! splendidement! isolé!
depuis!le!démembrement!de!la!Pangée!permienne!(Simpson!1980),!a!connu!des!vagues!
successives! de! colonisations! et! de! diversifications! qui! ont! contribué! à! former! sa! faune!
actuelle,! indépendamment! des! facteurs! physiques! (Encadrés! 2! &! 3).! Cependant,! dans!
certain!cas,!le!registre!fossile!est!trop!pauvre!pour!retracer!et!comprendre!l’histoire!de!
ces! distributions.! La! phylogénie! représente! alors! un! outil! complémentaire! permettant!
!
)!17!)!
de! retracer! conjointement! l’histoire! des! lignées! et! de! leur! distribution! (Brundin! 1972,!
voir!Encadré!1).!En!étudiant!les!relations!de!parenté!entre!êtres!vivants,!elle!permet!en!
effet!de!reconstruire!un!arbre!phylogénétique!qui!retrace!l’histoire!de!la!formation!des!
lignées!(figure!3.1,!Lecointre!&!Le!Guyader!2001).!Le!rapprochement!entre!la!théorie!de!
l’évolution! et! les! méthodes! biogéographiques! constitue! le! socle! fondamental! de! toutes!
les! méthodes! biogéographiques! actuelles! (Ronquist! and! Sanmartín! 2011).! L’utilisation!
d’une! multitude! de! lignées! biologiques! indépendantes! –!et! non! pas! d’une! seule!–! pour!
parvenir! à! une! histoire! commune! des! aires! de! distributions! représente! une! autre!
avancée! méthodologique! majeure.! Cette! approche,! introduite! par! Leon! Croizat! (1894)
1982,!voir!Encadré!1)!dans!les!années!50)60!(Croizat!1952,!1964)!est!plus!connue!sous!
le!nom!de!panbiogéographie.!!
! !
!
)!18!)!
!
! !
Encadré(2.(Un(bref(aperçu(de(l’originalité(des(mammifères(sud;américains.!
!!
La!diversité!et!la!singularité!des!mammifères!sud3américains!est!fascinante!(Darwin!1859;!Simpson!
1980).!En!effet!les!mammifères!actuels!peuplant!le!conEnent!représentent!une!mosaïque!étonnante!
de! lignées! propres! à! l’Amérique! du! Sud! et! de! lignées! beaucoup! plus! cosmopolites.! Ces! lignées!
propres! (endémiques)! ont! la! parEcularité! de! se! distribuer! sur! tout! le! gradient! de! la! classificaEon!
taxonomique.!
!!
Par!exemple,!on!y!retrouve!quelques!clades!proches!du!niveau!de!l’ordre!:!
3!les!xénarthres!dont!font!parEe!les!tatous,!fourmiliers!et!paresseux.!
3!les!caviomorphes!(les!Histricognathes!d’Amérique!du!Sud,!voir!la!carte!de!richesse)!dont!font!parEe!
le!capybara!ou!l’agouE!(voir!cliché)!.!
3!les!singes!du!nouveau!monde!(ou!Platyrhiniens)!dont!font!parEe!le!singe!hurleur!ou!les!ouisEEs.!
!!
Et! à! l’autre! bout! du! spectre! de! l‘échelle! taxonomique,! on! retrouve! certains! genres! très!
majoritairement! confinés! à! l’Amérique! du! sud! (et! éventuellement! centrale)! n’appartenant! pas! au!
clades!ci3dessus!mais!bien!à!des!clades!plus!largement!répandus!:!
3le! genre! Leopardus! (voir! la! carte! de! richesse)! qui! conEent! notamment! l’ocelot! (voir! cliché)! et! qui!
apparEent!à!la!famille!(presque)!cosmopolite!des!félidés.!
3le!genre!Mazama!qui!conEent!des!espèces!de!peEts!cerfs!et!qui!apparEent!à!la!famille!largement!
répandue!des!cervidés!(mais!néanmoins!absente!en!Afrique!et!en!Australie).!
!
!Leopardus! !Caviomorphes!
Richesse! Richesse!
6
10
5
8
4
6
3
©!Victor!O.!Vendramini!
2 4
©!Julia!Gonzalo!
1 2
0 0
Leopardus!pardalis! Dasyprocta!leporina!
!
)!19!)!
Encadré(3.(Un(bref(résumé(de(la(paléontologie(des(mammifères(sud9américains.!
!!
!En!schéma*sant,!on!dis*ngue!trois!phases!(ou!«!strates!»)!majeures!dans!le!registre!fossile!des!
mammifères!sud=américains!(Simpson!1980;!Flynn!1998).!Les!groupes!appartenant!à!ces!trois!phases!
n’ont! pas! nécessairement! de! représentants! aujourd’hui! et! c’est! pour! cela! que! le! registre! fossile! est!
d’une!importance!capitale.!!
! La! première! phase! con*ent! des! faunes! dites! «! archaïques! »! qui! peuplaient! le! con*nent! au!
début! de! son! isola*on! :! elle! comprend! des! lignées! de! xénarthres,! de! marsupiaux! ! et! d’ongulés!
aujourd’hui! disparus.! La! deuxième! phase! con*ent! des! éléments! «! modernisés! »! de! la! phase! 1! ainsi!
qu’une! lignée! de! rongeurs! et! une! lignée! de! primates,! dont! les! représentants! actuels! sont! les!
caviomorphes!et!les!singes!du!Nouveau!Monde!(voir!Encadré!2).!Ces!deux!évènements!de!colonisa*on!
apparaissent!être!le!fruit!d’une!migra*on!transocéanique,!probablement!depuis!l’Afrique!(Poux!et#al.!
2006).! !La!troisième!et!dernière!phase!con*ent!les!faunes!dites!modernes!et!correspond!à!la!dernière!
vague! de! colonisa*on.! Le! GABI! («! Great! American! Bio*c! Interchange! »)! représente! l’arrivée! de!
nombreux! nouveaux! ordres! (cetar*odactlyles,! carnivores,! lagomorphes! et! périssodactyles)!
consécu*vement!à!la!forma*on!!de!l’isthme!de!Panama!entre!13!et!3.5!Ma!(Haug!&!Tiedemann!1998;!
Coates!&!Stallard!2013;!Bacon!et#al.!2015).!!
! En! résumé,! l’Amérique! du! Sud! a! donc! été! le! théâtre! d’un! «! splendide! isolement! »! (Simpson!
1980)! et! s’est! vue! colonisée! par! trois! vagues! successives.! Ces! colons! se! sont! alors! diversifiés! pour!
former!les!groupes!d’espèces!que!l’on!connaît!aujourd’hui,!ou!se!sont!éteints.!!
!
Reproduced!from!Flynn!(1998)!
!
! !
!
)!20!)!
!
Traditionnellement,! deux! processus! évolutifs! sont! proposés! pour! expliquer! les!
distributions!disjointes!des!taxons!(figure!3.2)!:!la!dispersion!et!la!vicariance!(Lomolino!
et! al.! 2010).! La! vicariance! postule! que! les! régions! A! et! B! ne! formaient! qu’une! seule! et!
même!entité!lorsque!le!clade!est!apparu!et!que!c’est!son!morcellement!postérieur!qui!a!
conduit!à!la!séparation!des!deux!sous)clades!(figure!3.3.1).!La!dispersion!postule!que!le!
clade! est! apparu! dans! une! des! régions! et! a! ensuite! dispersé! dans! l’autre! en! donnant!
naissance!à!une!nouvelle!lignée!(figure!3.3.2).!!La!séparation!des!sous)clades!est!dans!les!
deux!cas!le!fruit!d’une!spéciation!allopatrique.!
!
L’analyse! de! l’histoire! de! la! biogéographie! nous! montre! combien! l’importance!
paradigmatique! accordée! aux! deux! processus! a! varié! au! cours! du! temps,! souvent! sous!
forme!de!révolutions!scientifiques!(Kuhn!1962)!et!notamment!en!fonction!de!l’état!des!
connaissances! dans! d’autres! disciplines.! Linné! postulait! ainsi! que! les! organismes!
provenaient! tous! de! l’arche! de! Noé! qui! s’était! échouée! sur! le! Mont! Ararat! (dans! la!
Turquie! actuelle)! et! avaient! ensuite! dispersé! sur! l’ensemble! du! globe.! Darwin! et! sa!
théorie!de!l’évolution!vinrent!balayer!ces!explications!et!il!devint!alors!plus!commun!de!
penser! que! des! lignées! pouvaient! apparaître! indépendamment! sur! les! continents! et!
disperser! via! des! ponts! transocéaniques! éphémères.! Cette! vision! fut! soutenue! par! de!
très!nombreux!naturalistes!à!différentes!époques,!notamment!par!le!paléontologue!G.!G.!
Simpson!(voir!Encadré!1)!ou!le!zoogéographe!P!.!Darlington!(1957).!C’est!l’acceptation!
tardive!(dans!les!années!60)!de!la!théorie!de!la!dérive!des!continents!proposée!par! un!
géographe,! Alfred! Wegener! (1912,! voir! Encadré! 1)! qui! redonnera! une! plus! grande!
importance!au!processus!de!vicariance.!La!dispersion!sera!alors!considérée!comme!un!
bruit!de!fond!parasite!et!sans!véritable!intérêt!(Nelson!1974,!Platnick!and!Nelson!1978,!
Lomolino!et!al.!2010).!En!fait,!le!débat!ne!portait!pas!tant!sur!l’importance!relative!de!la!
dispersion!et!de!la!vicariance,!mais!plutôt!sur!le!fait!que!la!dispersion!étant!un!processus!
hautement! stochastique! (contingent),! il! n’avait! pas! sa! place! dans! une! démarche!
hypothético)déductive! classique! sensu! Popper! (1968).! Finalement,! une! synthèse!
combinant!vicariance!et!dispersion!semble!émerger!depuis!quelques!années!(Sanmartin!
et! al.! 2001,! Ronquist! and! Sanmartín! 2011),! notamment! car! les! évènements! de!
dispersion! peuvent! en! fait! être! prédictibles! (par! exemple,! voir! Sanmartín! &! Ronquist!
2004).!
!
)!21!)!
1.'Arbre'phylogéné6que''' 2.'Distribu6ons'géographiques'
Espèce''A' Région''3'
Espèce''B' Région''2'
Espèce''C' Région''1'
3.'Hypothèses'biogéographiques'
3.1.$Vicariance$ 3.2.$Dispersion$
1+2+3' 2
1
3
ou'
1 2+3'
2
1
3
2
1
3
!
Figure(3.(Les(processus(fondamentaux(en(biogéographie(historique.!
La! figure! présente! les! données! de! base! utilisées! en! biogéographie!:! les! relations!
historiques!(1)!et!la!distribution!actuelle!(2)!de!trois!espèces.!Elle!décrit!ensuite!les!deux!
processus!fondamentaux!(3)!permettant!d’expliquer!ces!données!:!la!vicariance!(3.1)!et!
la! dispersion! (3.2).!
!
)!22!)!
Synthèse$
La! diversification! et! la! dispersion! des! organismes,! c’est! à! dire! les! dynamiques!
évolutives!de!leurs!aires!de!distribution,!jouent!un!rôle!majeur!dans!l’établissement!des!
patrons! de! répartition! actuels! et! passés! (Simpson! 1944,! 1980,! Gould! 2002,! Sanmartín!
and! Ronquist! 2004,! Lomolino! et! al.! 2010,! Hoorn! et! al.! 2010,! Belmaker! and! Jetz! 2015).!
Cependant,! les! facteurs! de! nature! historique! et! les! facteurs! de! nature! écologique!
expliquent! conjointement! la! répartition! des! êtres! vivant! et! leurs! influences! semblent!
varier!selon!l’échelle!d’étude!considérée!(Levin!1992,!Chave!2013).!
!
!
2.3.(L’importance(de(l’échelle(d’étude(
(
«$The$very$foundation$of$geography$is$scaling.$»$
J.A.!Wiens!(1989)!
!
La! biogéographie! étudie! un! système! biologique! donné! dans! un! espace! et! un!
temps!particuliers.!La!description!d’un!patron!biogéographique!et!la!compréhension!des!
phénomènes! sous)jacents! nécessitent! donc! un! positionnement! sur! trois! échelles! )
spatiale,! taxonomique! et! temporelle! )! distinctes.! Traditionnellement,! une! échelle! se!
décompose!en!un!grain!et!une!étendue.!Chacune!de!ces!deux!composantes!peut!affecter!
les! patrons! observés! mais! aussi! l’importance! respective! des! différents! processus! sous)
jacents.!!
!
!
L’échelle$spatiale$
En! écologie,! l’échelle! spatiale! revêt! une! importance! fondamentale! (MacArthur!
and!Wilson!1967,!Wiens!1989,!Levin!1992,!Chave!2013).!Le!grain!est!l’aire!du!site!dans!
laquelle! les! espèces! sont! répertoriées! alors! que! l’étendue! est! l’aire! recouvrant!
l’ensemble! des! sites.! ! Premièrement,! le! patron! biogéographique! lui)même! dépend! très!
largement! du! grain! de! l’étude.! Wiens! (1989)! en! donne! un! exemple! d’une! saisissante!
simplicité!:!deux!espèces!d’oiseaux!sont!globalement!présentes!dans!la!même!partie!du!
monde! (i.e.! en! Amérique! du! Nord)Est,! association! positive)! mais! ne! coexistent! pas! à!
l’échelle!locale!de!quelques!hectares!(association!négative).!La!description!des!patrons!
est! donc! fondamentalement! reliée! à! l’échelle! considérée.! Deuxièmement,! l’importance!
!
)!23!)!
relative!de!la!niche!écologique!et!de!l’histoire!est!aussi!contrainte!par!l’échelle!spatiale!
de! l’étude! (Rosenzweig! 1995,! Lomolino! et! al.! 2010,! Chase! and! Myers! 2011).! Par!
exemple,! les! patrons! à! large! échelle! semblent! influencés! par! la! géographie! de! la!
spéciation! et! les! contraintes! de! dispersion! historiques! (la! présence! des! océans! dans! le!
cas!des!régions!zoogéographiques!du!monde,!figure!2).!A!l’intérieur!de!ces!régions,!c’est)
à)dire!à!une!échelle!inférieure,!l’environnement!(et!donc!la!niche!écologique!des!espèces!
sensu!Grinell)!a!un!effet!important,!par!exemple!via!la!répartition!des!biomes.!Au!niveau!
du! paysage! et! de! la! communauté,! les! effets! relatifs! de! la! stochasticité,! des! interactions!
biotiques!et!des!perturbations!sont!encore!beaucoup!discutés!(Ricklefs!2008).!Dans!tous!
les! cas,! il! apparaît! que! les! processus! à! l’œuvre! à! différentes! échelles! sont!
interdépendants.!Ainsi,!les!patrons!à!l’échelle!locale,!par!exemple!la!richesse!spécifique!
d’une!communauté,!sont!en!partie!déterminés!par!les!processus!agissant!à!cette!échelle,!
comme!par!exemple!l’influence!de!l’environnement!ou!de!la!dispersion!(Hubbell!2001,!
Chase! and! Myers! 2011).! Cependant! ils! sont! aussi! forcément! contraints! par! la! richesse!
régionale,!qui!peut!être!façonnée!par!des!processus!macro)évolutifs!(e.g.!Ricklefs!1987).!
La! dépendance! est! cependant! réciproque!:! les! patrons! à! larges! échelles! spatiales! se!
construisent! à! partir! de! patrons! locaux! et! sont! donc! nécessairement!sous!contrôle!des!
processus!agissant!à!l’échelle!locale.!!
(
(
L’échelle$biologique$et$taxonomique$
L’ensemble!des!entités!biologiques!présentes!en!un!endroit!donné!à!un!moment!
donné!et!qui!composent!le!système!étudié!peut!lui!aussi!être!défini!à!plusieurs!niveaux.!
La! hiérarchie! phylogénétique! fournit! ici! un! cadre! conceptuel! robuste! pour! ce!
changement!d’échelle.!Cette!échelle!décrit!un!continuum!depuis!l’individu!jusqu’au!clade!
entier!(par!exemple!l’ensemble!des!mammifères).!Nous!pouvons!donc!progressivement!
ranger! les! individus! en! boîtes! concentriques! qui! sont! représentées! par! les! rangs!
taxonomiques.!On!peut!alors!étudier!un!système!biologique!aux!niveaux!des!individus,!
des!espèces,!des!genres,!des!familles!ou!mêmes!des!ordres.!Un!tel!changement!d’échelle!
a! aussi! démontré! son! intérêt! en! biogéographie! étant! donné! que! différents! processus!
peuvent!jouer!à!différentes!échelles!biologiques!(e.g.!Qian!2009;!Thuiller!et$al.!2010).!!
(
!
!
)!24!)!
L’échelle$temporelle$
L’échelle! temporelle! de! l’observation! correspond! au! temps! pendant! lequel!
l’observation! est! menée.! L’abondance! d’une! espèce! va! ainsi! pouvoir! varier! de! façon!
drastique!sur!une!courte!échelle!de!temps!mais!être!relativement!stable!à!moyen!et!long!
terme.! Dans! cette! thèse,! je! me! suis! cependant! focalisé! sur! de! longues! échelles!
temporelles!uniquement.!!
(
2.4.(Synthèse(
(
Ces!brefs!rappels!montrent!que!la!biogéographie!est!un!exercice!à!la!confluence!
d’une! multitude! de! disciplines.! L’approche! historique! se! focalise! sur! l’évolution! de! la!
distribution! des! espèces! et! par! conséquent,! s’appuie! largement! sur! l’évolution! des!
espèces! (reportée! en! violet! dans! l’encadré! 1)! et! la! géologie! (reportée! en! marron! dans!
l’encadré!1).!La!biogéographie!écologique!est!quant!à!elle!influencée!par!la!physiologie,!
la!dynamique!des!populations!ou!encore!l’écologie!des!communautés.!Pour!comprendre!
l’importance! relative! des! processus! historiques! et! écologiques,! une! approche!
biogéographique! intégrative!se!doit!d’effectuer!des!changements!d’échelles.!Dans!cette!
thèse,! j’ai! eu! à! cœur! de! travailler! le! long! de! ces! échelles! d’étude,! par! exemple! l’échelle!
taxonomique! (I.2! et! III.1)! mais! aussi! l’échelle! spatiale! (II).! La! compréhension! des!
mécanismes!régissant!la!distribution!des!espèces!nous!offre!alors!des!outils!pertinents!
pour!prédire!le!devenir!des!espèces!dans!un!monde!changeant.!!!
!
)!25!)!
3.(Protéger(les(espèces(:(la(biogéographie(de(la(conservation(
(
$«The$cowman$who$cleans$his$range$of$wolves$does$not$realize$that$he$is$taking$over$the$
wolf's$job$of$trimming$the$herd$to$fit$the$range.$He$has$not$learned$to$think$like$a$
mountain.$Hence$we$have$dustbowls,$and$rivers$washing$the$future$into$the$sea.$»$
Aldo!Leopold!(1949)!!
!
Comme! le! fait! remarquer! Aldo! Leopold! dans! cet! extrait! de! «!Thinking! like! a!
mountain!»! (1949),! les! conséquences! des! activités! humaines! sur! les! écosystèmes!
peuvent!parfois!être!aussi!!imprévisibles!que!désastreuses.!En!l’occurrence,!l’éradication!
du!loup!dans!certaines!zones!de!l’Amérique!du!Nord!a!des!conséquences!en!cascade!sur!
l’ensemble!du!milieu!montagnard.!Plus!généralement,!les!changements!globaux!induits!
par! l’homme! semblent! avoir! profondément! modifié! la! distribution! du! vivant.! Ces!
forçages! sont! de! nature! ! extrêmement! variable!:! changements! climatiques,!
déforestation,! changements! d’utilisation! des! terres! ou! propagation! des! espèces!
invasives!(e.g.!Barnosky!et$al.!2012).!Face!à!ces!menaces,!les!biogéographes!ont!un!rôle!
de!premier!plan!:!ils!se!doivent!de!proposer!des!prédictions!sur!les!conséquences!de!ces!
menaces! et! éventuellement! des! solutions! viables! pour! les! atténuer.! Ainsi! la!
biogéographie! de! la! conservation! (Whittaker! et! al.! 2005)! peut! être! définie! comme! la!
discipline! qui! s’attache! à! «!appliquer! les! principes,! théories! et! analyses!
biogéographiques! aux! problèmes! concernant! la! biologie! de! la! conservation!».! Il! s’agit!
donc!de!définir!les!unités!de!bases!sur!lesquelles!travailler,!de!prédire!leur!devenir!dans!
un!monde!changeant!et!éventuellement!de!fournir!des!conseils!pour!les!protéger.!!
!
3.1.(Définir(les(unités(de(base(de(la(biodiversité(:(de(quoi(parle]t]on(?((
!
La!variabilité!du!vivant!est!exubérante!et!se!trouve!souvent!qualifiée!par!le!terme!
un! peu! fourre)tout! de! «!biodiversité!»! (contraction! de! «!diversité! biologique!»! en!
anglais).! Le! mot! lui)même! est! davantage! une! construction! sociale! et! politique! que!
scientifique.!Il!est!apparu!dans!les!années!80!dans!le!but!de!sensibiliser!la!société!à!son!
érosion.!Sa!définition!est!extrêmement!large!puisqu’elle!englobe,!selon!la!Convention!sur!
la!diversité!biologique!(www.cbd.int,!introduite!au!Sommet!de!la!Terre!à!Rio!en!1992)!la!
«!variabilité! des! organismes! vivants! de! toute! origine! y! compris,! entre! autres,! les!
!
)!26!)!
écosystèmes! terrestres,! marins! et! autres! écosystèmes! aquatiques! et! les! complexes!
écologiques!dont!ils!font!partie;!cela!comprend!la!diversité!au!sein!des!espèces!et!entre!
espèces! ainsi! que! celle! des! écosystèmes!».! Cette! définition! étant! peu! opérationnelle,! il!
faut!s’attacher!à!en!préciser!la!nature.!!
En! conservation,! deux! approches! sont! généralement! entreprises! pour! définir! ce!
que! l’on! veut! préserver!:! l’approche! peut)être! fonctionnelle! ou! compositionnelle!
(Callicott! et! al.! 1999).! L’approche! fonctionnelle! privilégie! plutôt! les! processus! des!
écosystèmes! comme! les! flux! de! matières! (azote,! phosphore,! etc.! )! alors! que! l’approche!
compositionnelle! se! concentre! d’avantage! sur! les! entités! biologiques! comme! les!
individus!ou!les!espèces.!En!ce!sens,!cette!dernière!approche!se!rapproche!davantage!de!
la! biogéographie! écologique! et! historique.! Nous! focaliserons! donc! sur! celle)ci! dans! un!
premier! temps! pour! l’élargir! par! la! suite! dans! le! développement! et! la! discussion!
générale.!!
!
3.2.(Prédire(l’érosion(de(la(biodiversité(
!
Dans! le! cadre! d’une! approche! compositionnelle,! l’érosion! de! la! biodiversité! se!
traduit! notamment! par! l’extinction! des! populations! ou! des! espèces.! Pour! les!
biogéographes,!il!s’agit!donc!de!pouvoir!prédire!ces!extinctions!en!fonction!de!différents!
scénarii! futurs.! Il! existe! de! nombreuses! méthodes! de! prédiction! mais! deux! sont!
particulièrement! utilisées.! Premièrement,! l’utilisation! des! «!modèles! de! distribution!»!
permet!de!projeter!les!distributions!d’espèces!dans!le!futur!en!fonction!des!scénarii!de!
changement! climatique! fournis! par! exemple! par! le! groupe! d’experts!
intergouvernemental! sur! l’évolution! du! climat! (e.g.! Thuiller! et$al.! 2005).! On! peut! alors!
évaluer! la! part! d’espèces! susceptibles! de! voir! son! aire! de! distribution! réduire!
significativement!et!donc!être!potentiellement!en!danger!d’extinction.!C’est!notamment!
le! cas! pour! les! espèces! vivant! à! haute! latitude! et! haute! altitude! (Thuiller! et$al.! 2005).!
Dans!un!deuxième!temps,!l’utilisation!de!la!relation!aire)espèce!(c’est)à)dire!la!relation!
statistique! entre! l’aire! d’échantillonnage! et! le! nombre! d’espèces,! voir! Chapitre! III)IV)!
permet!de!prédire!les!taux!d’extinction!en!fonction!de!la!perte!ou!de!la!fragmentation!de!
l’habitat!(e.g.!Thomas!et$al.!2004;!Hanski!&!Zurita!2013),!une!des!menaces!majeures!qui!
pèse!sur!la!biodiversité.!
!
!
)!27!)!
3.3.(Protéger(la(biodiversité(?(
!
La!biogéographie!de!la!conservation!s’attache!aussi!à!élaborer!des!solutions!pour!
protéger! la! biodiversité.! Le! constat! fondamental! est! le! suivant!:! la! protection! de!
l’ensemble! des! entités! biologiques! peuplant! la! terre! n’est! pas! possible,! il! faut! donc!
choisir! et! protéger! des! aires! restreintes.! La! biologie! de! la! conservation! vise! donc! à!
définir!ou!à!complémenter!des!aires!de!protection.!Ce!plan!de!conservation!repose!sur!
quatre! critères! complémentaires!:! la! représentativité,! la! persistance,! l’efficacité! et! la!
flexibilité.! Il! s’agit! d’élaborer! un! projet! flexible! socialement! et! viable! économiquement!
pour!protéger!un!échantillon!représentatif!de!l’ensemble!biologique!qui!sera!capable!de!
se!maintenir!à!plus!ou!moins!long!terme.!!
!
3.4.(Synthèse(
!
De! la! même! façon! que! la! biogéographie! fondamentale,! la! biogéographie! de! la!
conservation! travaille! le! long! de! différentes! échelles! d’étude!:! échelle! de! l’entité!
biologique! (populations,! espèces,! écosystèmes)! et! échelles! spatiales! d’intervention!
(régions,!pays,!globe).!En!définitive!les!deux!disciplines!manipulent!donc!des!systèmes!
complexes!qu’il!s’agit!de!comprendre!et!de!protéger.!Dans!les!deux!cas,!il!faut!dans!un!
premier! temps! tenter! de! les! décrire! de! façon! synthétique,! ce! à! quoi! je! vais! m’attacher!
dans!le!prochain!point.!
( (
!
)!28!)!
4.(Considérer(la(biodiversité(sous(toutes(ces(facettes(pour(mieux(la(comprendre(et(
la(protéger(
En!général,!on!synthétise!la!structure!(ou!la!diversité)!d’un!assemblage!d’espèce!
par! un! ou! plusieurs! indices! quantitatifs.! Par! exemple,! le! plus! simple! est! le! nombre!
d’espèces! contenues! dans! l’assemblage! (=la! richesse).! De! façon! générale,! ces! mesures!
représentent! différentes! façon! de! synthétiser! les! données! faunistiques! de! base,! par!
exemple! plusieurs! milliers! de! polygones! de! distribution.! Dans! le! cas! de! la! richesse,! la!
diversité!est!entrevue!par!le!prisme!de!l’espèce.!Bien!qu’étant!informative!et!importante,!
elle! ignore! cependant! les! différences! fonctionnelles! et/ou! phylogénétiques! entre!
espèces!et!en!ce!sens!ne!représente!qu’une!vue!partielle!de!la!biodiversité.!La!démarche!
générale! de! ma! thèse! propose! de! (1)! décrire! les! facettes! évolutives! et! les! facettes!
fonctionnelles! de! la! biodiversité! pour! (2)! distinguer! entre! plusieurs! hypothèses!
concernant!l’importance!des!processus!explicatifs!sous)jacents!(par!exemple!historiques!
ou!écologiques)!et!(3)!mieux!protéger!l’histoire!et!le!fonctionnement!des!écosystèmes.!
La!description!de!ces!facettes!via!l’utilisation!des!indices!de!diversité!phylogénétique!et!
fonctionnelle! a! déjà! été! entreprise! en! biogéographie! fondamentale! (Webb! et! al.! 2002,!
Petchey!and!Gaston!2006)!et!de!la!conservation!(Forest!et!al.!2007).!Je!commence!donc!
par! décrire! les! avancées! récentes! et! les! intérêts! de! la! démarche! (4.1)! puis! je! pose! les!
questions!spécifiques!de!ma!thèse!qui!utiliseront!cette!démarche!(4.2).!
4.1.(Etat(de(l’art((
$
4.1.1.!Principe!et!intérêts!de!la!démarche!en!biogéographie!fondamentale!
(
Contexte$
Dans!cette!thèse!je!me!suis!intéressé!à!la!description!et!à!la!compréhension!des!
patrons! biogéographiques! à! large! échelle! spatiale! et! je! me! suis! attaché! à! étudier! les!
propriétés!émergentes!de!ces!systèmes,!une!approche!que!l’on!nomme!parfois!la!macro)
écologie! (Brown! and! Maurer! 1989,! Brown! 1999,! Keith! et! al.! 2012).! La! macro)écologie!
s’intéresse!ainsi!à!certains!grands!patrons!de!la!diversité!biologique!comme!le!nombre!
d’espèces!(Hillebrand!2004,!Belmaker!and!Jetz!2015),!la!taille!des!aires!de!distribution!
(Gaston!and!Blackburn!2008),!la!taille!des!organismes!(Olson!et!al.!2009)!ou!encore!les!
!
)!29!)!
différences!de!composition!faunistique!entre!grandes!régions!du!monde!(Kreft!and!Jetz!
2010,! Holt! et! al.! 2013).! Les! règles! générales! en! écologie! correspondent! à! des!
corrélations! saisissantes! entre! ces! variables! faunistiques! et! des! paramètres!
géographiques!ou!climatiques!(Lawton!1999).!On!pourra!citer!les!plus!incontournables!:!!
!
!
)! le! nombre! d’espèce! et! l’aire! d’échantillonnage,! i.e.! la! relation! aire)espèces!
(MacArthur!&!Wilson!1967;!Storch!et$al.!2012,!voir!Chapitre!III)IV).!
)!le!nombre!d’espèce!et!la!latitude,!i.e.!le!gradient!latitudinal!de!diversité!(Wallace!
1876,!Hillebrand!2004,!Belmaker!and!Jetz!2015).!
)!la!taille!des!aires!de!répartition!et!la!latitude,!i.e.!la!loi!de!Rapoport!(Lomolino!et!
al.!2010).!
)!la!dissimilarité!faunistique!et!la!distance!géographique,!i.e.!«!the!distance)decay!
relationship!»!(Rosenzweig!1995;!Qian!&!Ricklefs!2012,!voir!chapitre!VII).!!
)!la!masse/taille!d’une!espèce!et!la!latitude,!i.e.!la!règle!de!Bergman!(Lomolino!et$
al.!2010,!voir!Annexe!3).!
!
!
Ces! règles! écologiques! représentent! le! terrain! d’investigation! de! la! plupart! des!
biogéographes.! Après! les! avoir! confirmées,! il! s’agit! de! proposer! et! de! tester! différents!
types! d’hypothèses! explicatives.! Ici,! le! propos! n’est! pas! de! détailler! ces! règles,! mais!
d’introduire!l’approche!suivie!dans!cette!thèse.!Pour!comprendre!ces!grands!patrons!de!
la!biogéographie,!il!faut!dans!un!premier!temps!élaborer!des!hypothèses!explicatives!qui!
produisent!des!prédictions!claires!et!précises!que!l’on!peut!confirmer!ou!infirmer!en!les!
comparant! aux! observations.! Nous! avons! vu! que! la! biogéographie! écologique! reposait!
entre!autre!sur!l’utilisation!des!traits!fonctionnels!alors!que!la!biogéographie!historique!
était! fondamentalement! reliée! aux! arbres! phylogénétiques.! Peut)on! utiliser!
conjointement! les! traits! fonctionnels! et! les! phylogénies! pour! tester! des! hypothèses!
précises! expliquant! les! patrons! biogéographiques!?! En! utilisant! l’exemple! du! gradient!
latitudinal! de! diversité,! je! montre! dans! cette! introduction! comment! une! approche!
utilisant! conjointement! les! indices! de! diversité! fonctionnelle! et! phylogénétique! est!
prometteuse.!!
!
!
)!30!)!
L’apport$des$données$phylogénétiques$
Pour! expliquer! le! gradient! latitudinal! de! diversité,! l’hypothèse! du! «!time! for!
speciation!»! (TFS)! couplée! à! celle! du! «!tropical! niche! conservatism!»! (TNC,! Wiens! &!
Donoghue! 2004)! postule! que! (1)! la! plupart! des! clades! sont! d’origine! tropicale! car! ce!
biome! occupait! une! large! partie! du! globe! au! cénozoïque,! que! (2)! les! adaptations! aux!
conditions! tempérées! sont! rares! (hypothèse! TNC)! et! qu’en! conséquence! les! tropiques!
ont!accumulé!davantage!d’espèces!au!cours!de!l’évolution!(hypothèse!TFS).!Ce!postulat!
prédit! que! les! espèces! tempérées! doivent! être! relativement! «!jeunes!»! et! que! les!
tropiques!contiennent!des!espèces!«!jeunes!»!et!«!vieilles!»,!c’est!à!dire!qu’ils!constituent!
un!musée!et!un!berceau!de!diversité.!Il!est!donc!nécessaire!de!décrire!plus!finement!la!
structure!phylogénétique!des!assemblages!d’espèces!tropicales!et!tempérées!pour!tester!
si!les!hypothèses!proposées!sont!valides.!La!description!de!la!diversité!phylogénétique*!
des! assemblages! permet! alors! de! tester! une! telle! prédiction,! puisqu’elle! résume! la!
structure! des! relations! phylogénétiques! entre! espèces! dans! un! endroit! donné.! Dans! ce!
cas,!elle!permet!de!tester!des!hypothèses!de!type!historique.!!
!
L’apport$des$données$fonctionnelles$
Une! seconde! hypothèse! postule! que! les! régions! possédant! une! plus! grande!
disponibilité!en!niches!écologiques!permettront!la!coexistence!d’un!plus!grand!nombre!
d’espèces! (Belmaker! and! Jetz! 2015).! En! effet,! la! théorie! de! la! coexistence! prédit! que!
deux!espèces!possédant!des!niches!écologiques!identiques!ne!peuvent!pas!coexister!et!
vont! s’exclure! mutuellement! (Chesson! 2000).! Il! s’agit! donc! de! tester! si! les! zones!
tropicales!possèdent!relativement!plus!de!niches!disponibles!que!les!zones!tempérées.!
Les!traits!fonctionnels!vont!permettre!de!caractériser!la!niche!écologique!des!espèces!et!
ainsi! de! tester! cette! prédiction.! En! construisant! une! mesure! de! diversité! fonctionnelle!
(Petchey!and!Gaston!2006)!au!niveau!des!assemblages!d’espèces,!il!va!dont!être!possible!
de! tester! si! les! régions! riches! en! espèces! possèdent! aussi! davantage! de! niches!
écologiques!(Belmaker!and!Jetz!2015).!
!
4.1.2.!Principe!et!intérêts!de!la!démarche!en!biogéographie!de!la!conservation!
!
L’utilisation!de!la!diversité!phylogénétique!et!de!la!diversité!fonctionnelle!dans!le!
cadre!de!la!biogéographie!de!la!conservation!revêt!plusieurs!intérêts.!!
!
)!31!)!
Tout! d’abord,! la! dualité! traditionnelle! entre! approche! fonctionnelle! et!

compositionnelle! peut! être! unifiée! en! utilisant! simultanément! des! mesures!
taxonomiques!et!des!mesures!fonctionnelles!de!la!biodiversité.!En!effet,!les!mesures!de!
diversités!fonctionnelles!permettent!de!décrire!de!façon!plus!réaliste!certains!aspects!du!
fonctionnement! des! écosystèmes! (Dı́az& && Cabido& 2001),! par! exemple! leur! productivité!
(Cadotte! et! al.! 2011).! Les! services! que! rendent! les! écosystèmes! aux! sociétés! humaines!
pourraient!eux!aussi!être!représentés!par!des!indices!de!diversité!fonctionnelle!(Díaz!et$
al.! 2007).! En! conséquence,! la! préservation! de! la! diversité! fonctionnelle! pourrait!
permettre!de!mieux!protéger!le!fonctionnement!des!écosystèmes!(Mouillot!et!al.!2013).!
La! préservation! de! la! diversité! phylogénétique! (Faith! 1992),! c’est)à)dire! de!
l’histoire!évolutive!des!espèces,!apparaît!être!une!considération!davantage!éthique.!Est)
il!également!important!de!protéger!une!espèce!qui!est!le!seul!représentant!de!son!ordre!
(par! exemple! Orycteropus$ afer,! l’oryctérope! du! Cap)! ou! une! espèce! appartenant! à! un!
ordre!contenant!plusieurs!milliers!d’espèces!(par!exemple!une!espèce!de!rongeur)!?!En!
fait,!Vane)Wright!et$al.!(1991)!montrent!que!dans!un!monde!où!la!préservation!de!toutes!
les!lignées!est!impossible!(la!fameuse!«!agonie!du!choix!»),!il!est!important!de!considérer!
l’originalité!(=!la!rareté)!évolutive!des!espèces,!c’est)à)dire!leur!position!dans!l’arbre!de!
la!vie.!En!effet,!la!perte!de!lignées!évolutives!uniques!engendrera!la!perte!définitive!d’un!
grand!nombre!de!caractéristiques!uniques!alors!que!la!perte!de!lignées!«!redondantes!»!
n’aura! qu’un! effet! mineur! sur! la! perte! de! caractéristiques! uniques.! Certains! auteurs!
considèrent! aussi! qu’une! forte! diversité! phylogénétique! représente! un! réservoir! de!
potentiel! adaptatif! dans! un! futur! instable! (Forest! et! al.! 2007)! et,! potentiellement,! un!
réservoir!de!diversité!fonctionnelle.!!
!
En! définitive,! il! s’agit,! selon! Lecointre! (2011),! de! préserver! les! espèces! pour! ce!
qu’elles! font! (=! approche! fonctionnelle)! et! pour! ce! qu’elle! sont! (=! approche!
phylogénétique).!Certaines!analyses!commencent!à!montrer!que!les!différentes!facettes!
de!la!biodiversité!ne!sont!pas!interchangeables!ou!«!congruentes!»,!c’est!à!dire!qu’en!en!
préservant! une,! on! ne! garantit! pas! forcément! la! protection! des! autres! (Devictor! et$ al.!
2010).! En! conséquence,! il! apparait! important! de! considérer! les! trois! facettes! de! la!
biodiversité!dans!les!plans!de!conservation.!A!large!échelle,!cette!démarche!a!d’ailleurs!
été! intégrée! aux! objectifs! de! la! plateforme! intergouvernementale! sur! la! biodiversité! et!
les!services!des!écosystèmes!(IPBES,!Díaz!et$al.!2015).( !
!
)!32!)!
Nombre de Publications 600
Indice
400
FD
PD
200
0
1990 1995 2000 2005 2010 2015
Années
Diversité)Phylogéné1que) Diversité)Fonc1onelle)
Research.Areas ENVIRONMENTAL SCIENCES ECOLOGY

AGRICULTURE
MARINE FRESHWATER BIOLOGY
BIOCHEMISTRY MOLECULAR BIOLOGY
MICROBIOLOGY
BIOTECHNOLOGY APPLIED MICROBIOLOGY
PLANT SCIENCES
CELL BIOLOGY
SCIENCE TECHNOLOGY OTHER TOPICS
ENVIRONMENTAL SCIENCES ECOLOGY
!
Figure(4.(Utilisation(des(indices(de(diversité(phylogénétique(et(fonctionnelle!dans!
la! littérature! (d’après! ISI! web! of! knowledge,! le! 01/09/2015).! La! figure! A! présente! le!
nombre! d’articles! qui! utilisent! les! expressions! «!diversité! phylogénétique!»! ou!
«!diversité!fonctionnelle!»!dans!leurs!mots!clefs,!au!cours!du!temps.!La!figure!B!présente!
la! répartition! de! l’ensemble! de! ces! articles! dans! différentes! disciplines! (seules! les! cinq!
premières!disciplines!pour!chaque!expression!sont!conservées).( !
!
)!33!)!
4.2.(Questions(abordées(dans(cette(thèse(
!
Il!apparaît!ainsi!que!l’utilisation!des!diversités!fonctionnelles!et!phylogénétiques!
en! biologie! soit! prometteuse.! On! observe! d’ailleurs! depuis! le! début! des! années! 90! une!
forte!augmentation!de!leur!utilisation,!notamment!en!écologie!(figure!4)!et!de!nouveaux!
champs!entiers!de!recherche!leur!sont!maintenant!dédiés,!par!exemple!la!biogéographie!
fonctionnelle! (Violle! et$ al.! 2014)! ou! encore! «!l’écophylogénétique!»! (Mouquet! et! al.!
2012).!!
!
Dans!cette!thèse,!nous!proposons!d’étudier!les!grands!patrons!biogéographiques!
via! la! description! des! différentes! facettes! de! la! diversité! biologique! (taxonomique,!
fonctionnelle!et!phylogénétique).!En!particulier!:!
!
(1)! Les! différentes! facettes! de! diversité! des! mammifères! sont0elles! congruentes! à!
l’échelle! du! globe!?! En! d’autres! termes,! protéger! le! nombre! d’espèces! suffit0il! à!
protéger!la!diversité!fonctionnelle!et!évolutive!?!
!
(2)! Ces! différentes! facettes! sont0elles! également! vulnérables! aux! changements!
globaux!et!en!particulier!à!la!perte!d’habitat!?!
!
(3)! Ces! différentes! facettes! sont0elles! également! couvertes! par! les! zones! de!
protection!?!
!
(4)! Que! peuvent! nous! apporter! ces! différentes! facettes! dans! la! compréhension! des!
grands!patrons!de!répartition!du!vivant!?!
En! particulier,! peut0on! décomposer! la! distribution! des! lignées! sur! une! échelle!
phylogénétique!pour!mieux!comprendre!les!effets!relatifs!de!l’histoire!et!de!la!niche!
écologique!?!
( (
!
)!34!)!
5.(Le(système(biologique(et(l’échelle(spatiale(de(l’étude(
!
Les! seuls! groupes! de! taille! importante! dont! on! connaît! la! répartition! mondiale,!
les! relations! de! parenté! ainsi! qu’un! certain! nombre! de! traits! fonctionnels! sont! les!
mammifères! et! les! oiseaux.! Il! est! d’abord! utile! de! se! demander! pourquoi! ces! groupes!
sont!si!bien!connus,!puisqu’ils!vont!constituer!le!matériel!de!base!de!mon!travail.!!
!
5.1.(Les(origines(du(biais(de(connaissance((
(
Les!mammifères!et!les!oiseaux!sont!relativement!mieux!connus!que!la!plupart!des!
autres! groupes! pour! trois! raisons! majeures.! Premièrement,! les! mammifères! et! les!
oiseaux! contiennent! relativement! peu! d’espèces! (environ! 5000! et! 10! 000!
respectivement)!contrairement! aux! plantes! (environ! 300.000,!
http://www.theplantlist.org/)! ou! aux! arthropodes! (5)10.000.000!;! Ødegaard,! 2000).!
Deuxièmement,!!ils!sont!relativement!gros,!ce!qui!facilite!évidemment!leur!découverte!et!
leur!description.!Dans!le!cas!des!mammifères,!une!troisième!raison!majeure!apparaît!:!ils!
nous!ressemblent.!!
!
!
«$Ce$sont$les$mammifères$qui$doivent$occuper$le$premier$rang$dans$le$règne$animal,$sous$le$
rapport$du$perfectionnement$de$l’organisation$et$du$plus$grand$nombre$de$facultés.$»$
$
Jean!Baptiste!de!Lamarck!(1809)!
!
!
Cette!citation!de!Lamarck!(1744)1829)!peut!aujourd’hui!paraître!dépassée!mais!
elle!est!pourtant!le!reflet!d’un!véritable!impact!de!l’anthropocentrisme!en!biogéographie!
et!en!évolution.!Pourtant,!Darwin!initia!bien!un!radical!changement!de!paradigme!chez!
les! naturalistes! il! y! a! déjà! plus! de! 150! ans.! Il! replaça! en! effet! l’homme! au! sein! des!
primates!et!des!êtres!vivants!en!général,!et!non!plus!aux!côtés!de!Dieu,!ce!qui!lui!valut!
d’ailleurs!de!nombreuses!critiques!et!moqueries!(figure!5).!Malgré!les!preuves!avancées!
par! Darwin,! l’impact! de! l’anthropocentrisme! en! évolution! a! continué! à! être! fort.! Les!
planches!de!Ernst!Haeckel!(1834)1919),!notamment!celles!sur!les!animaux,!en!sont!une!
!
)!35!)!
illustration!remarquable!(figure!6).!En!effet,!on!y!voit!une!représentation!en!arbre!où!les!
mammifères! occupent! le! sommet! du! houppier,! véhiculant! ainsi! l’idée! qu’ils! sont! de!
nature!«!supérieure!».!Cet!anthropocentrisme!chronique!explique!en!partie!pourquoi!les!
mammifères! sont! aujourd’hui! mieux! connus! que! les! autres! groupes! et! pourquoi! ils!
représentent!donc!un!groupe!de!choix!dans!l’étude!des!patrons!biogéographique!à!large!
échelle!spatiale.! !
!
)!36!)!
Figure(5.(Caricature(de(Charles(Darwin.!Cette!caricature!a!été!dessinée!par!André!Gill!
en!1878!pour!La$petite$lune.$Elle!dépeint!Darwin!en!singe!(une!hérésie!!)!accroché!à!
l’arbre!de!la!science.( (
!
)!37!)!
(
Figure( 6.( Planche( de( Ernst( Haeckel( (1874)! représentant! le! pedigree! de! l’homme!
(«!pedigree! of! man!»).! L’homme! y! est! représenté! au! sommet! de! la! plus! haute! branche!
d’un! arbre! des! animaux! dont! le! tronc! est! découpé! en! quatre! stades! majeurs!:! des!
«!animaux! primitifs!»! à! la! base! suivis! d’invertébrés,! des! vertébrés! et! finalement! des!
mammifères.!On!notera!deux!points!intéressants!:!(1)!les!mammifères!ne!sont!pas!placés!
au! seins! des! vertébrés,! mais! bien! au! dessus!;! (2)! certaines! branches! paraissent!
redescendre,!comme!celle!de!la!myxine!ou!celle!des!éponges.!
!
!
!
)!38!)!
5.2.(Les(données(de(distribution(utilisées(
!
Les!données!de!distribution!de!ces!groupes!sont!donc!relativement!anciennes!et!
parmi!les!meilleures!à!large!échelle!spatiale.!Elles!sont!aujourd’hui!mises!à!disposition!
par!l’IUCN!pour!les!mammifères!(http://www.iucnredlist.org/)!et!par!BirdLife!pour!les!
oiseaux!(http://www.birdlife.org/).!!
!
L’étendue!de!mon!échelle!d’étude!est!le!globe!terrestre!et!le!grain!va!dépendre!de!
la! qualité! des! données! de! distribution.! Les! données! brutes! disponibles! sont! des!
polygones! d’étendue! d’occurrence! («!extent! of! occurrence!»,! EOO;! cf.! figure! 7! pour! le!
loup,!Canis$lupus).!En!fait,!elles!ont!été!compilées!sur!la!base!de!dire!d’experts!nationaux!
réunis! en! comités! plus! larges.! Concrètement! elles! ont! été! produites! en! traçant! un!
«!contour!»!!autour!des!localités!où!l’espèce!a!été!effectivement!observée.!Ceci!implique!
que!l’espèce!ne!sera!pas!forcément!présente!à!l’intérieur!de!l’ensemble!du!polygone!(à!la!
différence!des!distributions!basées!sur!les!aires!d’occupations!–!«!area!of!occupancy!»!–).!
A!priori!il!existe!aussi!de!grands!écarts!de!précisions!entre!espèces!et!entre!régions.!La!
carte! de! distribution! du! loup! en! montre! un! exemple! frappant!:! la! répartition! est!
extrêmement! détaillée! en! Europe! de! l’ouest,! où! l’on! reconnaît! même! les! massifs!
montagneux.! Au! contraire,! le! loup! apparait! réparti! sur! l’ensemble! de! la! péninsule!
arabique,!ce!qui!n’est!a!priori!pas!le!cas!(F.!Ficetola,!communication!personnelle).!!
Pour! définir! des! assemblages! d’espèces,! il! faut! définir! des! aires! )souvent! des!
«!pixels!»! )! dans! lesquelles! on! note! si! l’espèce! est! absente! ou! présente.! Peut)on! alors!
réellement! utiliser! les! données! de! l’IUCN! et! de! BirdLife! sans! risquer! de! surestimer! le!
nombre! de! pixels! dans! lesquels! l’espèce! est! présente! (étant! donné! que! son! EOO! ne!
représente! qu’un! contour)?! Une! solution! conservative! est! d’utiliser! un! grain! d’étude!
«!assez!large!»,!ce!qui!permettra!de!minimiser!les!faux!positifs.!Ce!grain!adéquat!n’est!en!
fait!pas!défini!et!différents!auteurs!utilisent!différents!grains!:!par!exemple!Jenkins!et$al.!
(2013)! utilise! un! grain! de! 10km*10km! alors! que! certaines! études! montrent! qu’on! ne!
peut!pas!descendre!en!dessous!de!100km*100km!sans!risquer!de!faire!de!graves!erreurs!
(Hurlbert!and!Jetz!2007).!Dans!cette!thèse,!j’adopte!donc!une!démarche!conservative!en!
utilisant!un!grain!grossier!(>!100*100km)!dans!la!plupart!des!cas.!
! !
!
)!39!)!
( (
Figure(7.(L’aire(de(distribution(du(loup((Canis!lupus)(dans(le(monde,(selon(l’IUCN.(
Les! zones! en! orange! montrent! la! répartition! actuelle! de! l’espèce! alors! que! la! zone! en!
rouge!montre!la!zone!où!l’espèce!a!disparu.!
!
)!40!)!
6.(Stratégie(de(travail(et(plan(de(la(thèse.((
(
6.1.(Principe(
L’utilisation! des! indices! de! diversité! fonctionnelle! et! phylogénétique! en!
biogéographie! se! heurte! à! une! première! difficulté! majeure.! La! discipline! est!
littéralement!parasitée!par!la!multiplication!des!indices,!empêchant!ainsi!toute!tentative!
de!synthèse!cohérente.!En!effet,!le!grand!nombre!d’indices!de!diversité!proposés!a!créé!
une! véritable! «!jungle!»! dans! laquelle! il! est! compliqué! –!si! ce! n’est! impossible!–! de! se!
retrouver! (Winter! et! al.! 2012).! A! titre! d’exemple,! la! discipline! comprend! plus! de! 60!
indices! de! diversité! phylogénétique! (voir! le! matériel! supplémentaire! de! l’article! 1).!
Puisque! différentes! études! utilisent! différents! indices! et! qu’il! n’existe! pas! de! synthèse!
permettant!de!relier!les!indices!les!uns!aux!autres!(mais!voir!Pavoine!&!Bonsall!2011),!
toute!tentative!de!généralisation!est!compliquée.!
!
La! première! partie! de! ma! thèse! s’attache! donc! à! résoudre! ce! problème! en!
répondant! à! une! triple! nécessité!:! répertorier,! classer! et! comparer! les! indices! de!
diversité.!Les!articles!1!&!3!(Chapitre!I!et!Annexe!1.3,!respectivement)!listent,!classent!et!
comparent!les!indices!de!diversité.!L’article!2!(Chapitre!II)!va!plus!loin!en!explorant!la!
sensibilité!des!principaux!indices!à!l’échelle!taxonomique/phylogénétique.!
La! deuxième! partie! de! ma! thèse! explore! la! sensibilité! des! approches! de!
conservation!classique,!c’est)à)dire!basées!sur!la!diversité!taxonomique!uniquement,!à!la!
prise!en!compte!des!diversités!fonctionnelles!et!phylogénétiques.!En!particulier,!j’évalue!
la!perte!de!la!diversité!phylogénétique!consécutive!à!la!destruction!d’habitat!(Article!4,!
Chapitre! III),! la! nature! des! points! chauds! de! diversité! («!biodiversity$ hotspots!»)! à!
plusieurs! facettes! («!multifaceted! biodiversity$ hotspots!»,! Article! 5,! Chapitre! IV),! ! et! la!
capacité!des!aires!de!protection!européenne!à!préserver!les!diversités!fonctionnelles!et!
phylogénétiques!(Article!6,!Annexe!2.3).!
La! troisième! partie! de! ma! thèse! s’attache! à! mieux! comprendre! quelques!
problématiques! de! la! biogéographie! fondamentale! en! utilisant! les! indices! de! diversité!
phylogénétique! et! fonctionnelle.! Notamment,! je! montre! dans! un! premier! temps!
comment! les! changements! d’échelles! le! long! d’un! gradient! phylogénétique! permettent!
de! séparer! les! effets! de! différents! processus! (sous)partie! 1),! notamment! en!
biogéographie! à! grande! échelle! spatiale! (Article! 7,! Chapitre! V)! mais! aussi! en!
!
)!41!)!
biogéographie! des! microbes! (Article! 8,! Chapitre! VI).! La! deuxième! sous)partie! montre!
comment!une!analyse!conjointe!des!diversités!fonctionnelles!et!phylogénétiques!permet!
de! mieux! comprendre! l’évolution! morphologique! des! assemblages! de! mammifères! à!
large!échelle!(Articles!9!&!10,!Annexe!3.2.1!et!Chapitre!VII,!respectivement).!!
!
6.2.(Organisation(
Chaque! partie! est! constituée! d’un! sommaire! détaillé,! d’une! introduction,! de!
plusieurs! chapitres! comportant! un! ou! plusieurs! articles,! d’une! synthèse! et! d’une!
bibliographie.!Je!propose!une!synthèse!générale!en!guise!de!conclusion!mais!le!cœur!de!
ma! discussion! sera! développée! dans! les! synthèses! de! chacune! des! parties.! Les! dix!
articles! présentés! se! retrouvent! à! l’interface! entre! la! biogéographie! fonctionnelle,!
phylogénétique!et!de!la!conservation!(figure!8).(
!
Conserva)on*Biogeography*
Ar)cles**
1,*5*&*6*
Ar)cles*
9*&*10*
Figure(8.(La!figure!présente!la!répartition!de!mes!articles!de!thèse!à!l’interface!de!trois!
disciplines!majeures!de!la!biogéographie,!illustrant!ainsi!le!caractère!pluridisciplinaire!
de!mon!travail.!(
!
)!42!)!
!
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Ødegaard,!F.!2000.!How!many!species!of!arthropods?!Erwin’s!estimate!revised.!)!Biol.!J.!Linn.!Soc.!71:!583–
597.!
Olson,!V.!a!et!al.!2009.!Global!biogeography!and!ecology!of!body!size!in!birds.!)!Ecol.!Lett.!12:!249–259.!
Pavoine,! S.! and! Bonsall,! M.! B.! 2011.! Measuring! biodiversity! to! explain! community! assembly:! a! unified!
approach.!)!Biol.!Rev.!86:!792–812.!
Petchey,!O.!L.!and!Gaston,!K.!J.!2006.!Functional!diversity:!back!to!basics!and!looking!forward.!)!Ecol.!Lett.!
9:!741–758.!
Platnick,!N.!I.!and!Nelson,!G.!1978.!A!Method!of!Analysis!for!Historical!Biogeography.!)!Syst.!Zool.!27:!1.!
Popper,!K.!R.!1968.!The!Logic!of!Scientific!Discovery.!)!Routledge.!
Qian,! H.! 2009.! Global! comparisons! of! beta! diversity! among! mammals,! birds,! reptiles,! and! amphibians!
across!spatial!scales!and!taxonomic!ranks.!)!J.!Syst.!Evol.!47:!509–514.!
Qian,! H.! and! Ricklefs,! R.! E.! 2012.! Disentangling! the! effects! of! geographic! distance! and! environmental!
dissimilarity!on!global!patterns!of!species!turnover.!)!Glob.!Ecol.!Biogeogr.!21:!341–351.!
Ricklefs,! R.! E.! 1987.! Community! diversity:! relative! roles! of! local! and! regional! processes.! )! Science! 235:!
167–71.!
Ricklefs,!R.!E.!2008.!Disintegration!of!the!Ecological!Community.!)!Am.!Nat.!172:!741–750.!
Ronquist,!F.!and!Sanmartín,!I.!2011.!Phylogenetic!Methods!in!Biogeography.!)!Annu.!Rev.!Ecol.!Evol.!Syst.!
42:!441–464.!
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489–505.!
Root,!T.!1988b.!Energy!constraints!on!avian!distributions!and!abundances.!)!Ecology!69:!330–339.!
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J.!Linn.!Soc.!73:!345–390.!
Sanmartín,!I.!and!Ronquist,!F.!2004.!Southern!hemisphere!biogeography!inferred!by!event)based!models:!
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Linn.!Soc.!London.!Zool.!2:!130–136.!
Simpson,!G.!G.!1944.!Tempo!and!Mode!in!Evolution.!)!Columbia!University!Press.!
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Yale!University!Press.!
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)!44!)!
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Storch,! D.! et! al.! 2012.! Universal! species)area! and! endemics)area! relationships! at! continental! scales.! )!
Nature!488:!78–81.!
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28:!199–204.!
!
!
!
)!45!)!
!
!
)!46!)!
!
! "!47!"!
Partie!I!
PARTIE'I'
'
CLASSER'LA'DIVERSITÉ'DES'DIVERSITÉS'
PHYLOGÉNÉTIQUES'ET'
FONCTIONNELLES'
'
'
! "!48!"!
!
! "!49!"!
Partie!I!!
«"Je"regardai"alentour,"et,"je"ne"sais"pourquoi,"je"vous"assure"que"jamais,"jamais"auparavant"
cette"terre,"[…]"cette"jungle"[…]"ne"m'avaient"paru""
si"privés"d'espoir,"si"sombres,"si"impénétrables"à"la"pensée"humaine."»"
!Joseph!Conrad!
Au"coeur"des"ténèbres,!1899!
!
!
!
!
!
La"jungle"vue"d’un"inselberg,"Guyane"française""©"M."RéjouLMéchain"
! "!50!"!
Partie!I!"!Sommaire!
SOMMAIRE'DE'LA'PARTIE'I'
'
Articles'associés'à'la'partie'I' ' ' ' ' ' ' ' 52'
Annexes'associées'à'la'partie'I' ' ' ' ' ' ' ' 52'
'
INTRODUCTION.'Les'différentes'facettes'de'la'biodiversité' ' ' 53'
1.!Un!constat!alarmant' ' ' ' ' ' ' ' ' 54'
2.!Une!triple!nécessité' ' ' ' ' ' ' ' ' 55'
3.!Les!grandes!facettes!de!la!biodiversité' ' ' ' ' ' ' 55'
'
CHAPITRE'I.'Une'tentative'de'synthèse'exhaustive'des'indices''
phylogénétiques'α'et'β' ' ' ' ' ' ' ' ' 58'
'
Résumé' ' ' ' ' ' ' ' ' ' ' 61!
Article!1' ' ' ' ' ' ' ' ' ' ' 63!
!
CHAPITRE'II.'L’importance'de'l’échelle'phylogénétique' ' ' ' 90'
!
Résumé! ! ! ! ! ! ! ! ! ! ! 91!
Article!2! ! ! ! ! ! ! ! ! ! ! 93!
!
SYNTHÈSE'&'DISCUSSION.'Vers'une'unification'?' ' ' ' ' 108'
1.!Synthèse!du!travail! ! ! ! ! ! ! ! ! 109!
2.!Utilité!de!l’approche! ! ! ! ! ! ! ! ! 111!
3.!Limites!et!perspectives!du!travail! ! ! ! ! ! ! 111!
!
! "!51!"!
Partie!I!"!Contributions!
ARTICLES'ASSOCIÉS'À'LA'PARTIE'I'
'
ARTICLE!1!"
!
C.!M.!Tucker,!M.!W.!Cadotte,!S.!B.!Carvalho,!!J.!T.!Davies,!S.!Ferrier,!S.!A.!Fritz,!R.!Grenyer,!
M.!R.!Helmus,!L.!S.!Jin,!A.!O.!Mooers,!S.!Pavoine,!O.!Purschke,!D.!W.!Redding,!D.!F.!Rosauer,!!
M.!Winter!&!F.'Mazel.!A"unification"of"phylogenetic"metrics"for"conservation,"community"
ecology"and"macroecology.!
En!révision!dans!Biological"Reviews"
!
!
ARTICLE!2!"
!
F.'Mazel,!Davies,!T.J,!Gallien!L.,!Groussin,!M.,!Münkemüller!T.!&!Thuiller,!W.!Influence"of"
tree"shape"and"evolutionary"timeLscale"on"phylogenetic"diversity"metrics."
Accepté!dans!Ecography"
!
!
ARTICLE!3!"
!
Redding,!D.W.,!Mazel,'F.,!and.!A.O.!Mooers.!Measuring"evolutionary"isolation"for"
conservation.""
PloS"one,!9(12),!e113490.!
!
!
!
ANNEXES'ASSOCIÉES'À'LA'PARTIE'I'
!
ANNEXE!1.1.!Matériel!supplémentaire!de!l’article!1!
ANNEXE!1.3.!Article!3!
ANNEXE!1.4.!Résumé!d’un!article!additionnel!
! "!52!"!
Partie!I!"!Introduction!
INTRODUCTION'DE'LA'PARTIE'I''
'
LES'DIFFÉRENTES'FACETTES'DE'LA'BIODIVERSITÉ'
! "!53!"!
'
1.'Un'constat'alarmant'
!
L’utilisation! des! diversités! phylogénétiques! et! fonctionnelles! a! connu! un! essor!
fulgurant!ces!25!dernières!années!(voir!la!figure!4!de!l’introduction!générale).!En!effet,!il!
apparaît! que! leur! utilisation! peut! permettre! de! mieux! comprendre! (1)! les! processus!
générant!les!distributions!des!espèces!à!toutes!les!échelles!spatiales!(Webb!et!al.!2002,!
Graham!and!Fine!2008,!Mouquet!et!al.!2012)!et!(2)!le!fonctionnement!et!les!services!des!
écosystèmes!(Díaz!et!al.!2007,!Srivastava!and!Cadotte!2012).!Ce!potentiel!prometteur!est!
cependant! obscurci! par! les! trop! nombreux! indices! (ou! métriques)! qui! constituent!
actuellement!une!véritable!jungle!(Mouquet!et!al.!2012,!Winter!et!al.!2012).!Bien!que!la!
diversité! phylogénétique! ou! fonctionnelle! d’un! assemblage! d’espèces! ne! puisse! pas! se!
mesurer!qu’avec!un!seul!nombre,!il!paraît!inconcevable!qu’il!y!ait!des!dizaines!de!façons!
indépendantes!et!également!intéressantes!de!mesurer!la!diversité!phylogénétique!d’une!
seule! communauté! (voir! matériel! supplémentaire! 1! de! l’article! 1).! En! fait,! une! part!
substantielle!de!ces!indices!portent!la!même!information!:!il!existe!même!des!indices!qui!
possèdent! des! noms! différents! mais! qui! sont! exactement! identiques.! Certains! auteurs!
ont!déjà!pointé!ce!problème!(Swenson!2011)!:!
«"This"is"therefore"another"clear"example"of"either"authors"not"being"aware"of"
contemporary"metrics"or"not"comparing"their"‘new’"metric"to"known"existing"metrics"first"
either"via"simulation"or"by"comparing"their"equations."»"
!
Il! est! donc! urgent! de! faire! le! tri! dans! cette! jungle.! Nathan! Swenson! le! fait!
justement!remarquer!(2011)!:!
«"As"the"number"of"metrics"continues"to"grow,"further"studies"will"be"needed"to"show"which"
new"metrics"actually"provide"novel"information"and"strengthen"the"statistical"toolkit"of"the"
phylogenetic"community"ecologist."»"!
!
La!première!partie!de!cette!thèse!va!donc!tenter!de!relever!ce!défi!en!se!
demandant!:!
!
Peut&on!synthétiser!les!indices!de!diversités!
!le!long!de!grandes!«"dimensions"»!de!l’information?!
! "!54!"!
!
2.'Une'triple'nécessité'
!
L’objectif!est!donc!de!construire!une!carte!simplifiée!de!la!jungle!des!indices!qui!
pourra!éventuellement!permettre!aux!écologistes!de!ne!plus!se!perdre.!La!construction!
d’une!telle!carte!a!trois!objectifs!:!
!
(1) répertorier!chacun!des!indices!de!la!jungle!(c’est"à"dire!s’y!perdre!plus!d’une!
fois)!
(2) tracer!des!sentiers!autour!de!groupes!d’indices!similaires!
(3) faire!en!sorte!que!ces!sentiers!délimitent!des!groupes!d’indices!certes!similaires!
mais!surtout!utiles!pour!tester!des!hypothèses!écologiques!précises.!
!
On! retrouvera! l’inventaire! (presque!!)! exhaustif! des! indices! dans! le! matériel!
supplémentaire! 1! de! l’article! 1! et! la! table! 1! de! l’annexe! 1.! Je! présente! maintenant! les!
grandes!lignes!des!sentiers!que!j’ai!choisi.!!
!
3.'Les'grandes'facettes'de'la'diversité''
!
Je! pense! qu’une! classification! des! indices! est! possible,! tout! du! moins! pour! ses!
composantes! majeures.! Je! pense! qu’il! existe! de! grandes! dichotomies! sur! lesquelles! on!
peut!tenter!une!classification!:!
!
(1)"Dichotomie"au"niveau"des"types"de"distances"considérées."
C’est! la! distinction! entre! diversité! fonctionnelle! et! diversité! phylogénétique.!
Chacune! de! ces! distances! est! intéressante! en! soi! et! leur! comparaison! paraît! aussi!
prometteuse! (d’où! la! nécessité! de! disposer! d’un! cadre! méthodologique! et! conceptuel!
identique!pour!les!deux).!
!
(2)"Dichotomie"au"niveau"de"l’objet"biologique"considéré."
La!diversité!fait!forcément!référence!à!un!objet!biologique!donné.!Cet!objet!peut!
se! définir! à! plusieurs! échelles! biologiques!:! l’espèce,! la! communauté! ou! la! paire! de!
communautés.!!
! "!55!"!
!
Objet! Diversité!
!
Espèce! Originalité!
!
!
Communauté! α!
!
!
Paire!de!communautés! β!
!
!
Cette! organisation! correspond! en! partie! à! la! distinction! classique! proposée! par!
Whittaker!(1960)!entre!diversités!α,!β!et!γ.!Cette!distinction!est!originellement!basée!sur!
la!diversité!taxonomique,!soit!le!nombre!d’espèces!d’un!assemblage!local!(diversité!α),!le!
nombre!d’espèces!d’un!assemblage!régional!(diversité!γ)!et!la!différentiation!moyenne!
entre!les!communautés!(diversité!β=!α/γ).!Les!diversités!α!et!γ!sont!de!nature!identique,!
à!l’échelle!spatiale!près.!On!considère!donc!ici!deux!mesures!fondamentales!:!
!
"!la!diversité!au!niveau!d’un!seul!site!:!la!diversité!α!
"!la!différence!de!composition!entre!deux!sites!:!la!diversité!β!
"! finalement,! j’ajouterai! ici! la! quantification! d’un! autre! niveau! organisationnel!:!
l’espèce! elle"même.! En! effet,! la! littérature! regorge! de! mesure! «!d’originalité!»!
phylogénétique!ou!fonctionnelle!(Isaac!et"al.!2007;!Buisson!et"al.!2010,!voir!Annexe!1).!!
!
On!peut!donc!déjà!ranger!les!indices!dans!six!grandes!cases!distinctes!(deux!types!
de! distances! *! trois! unités! biologiques).! Les! chapitres! I! et! II! explorent! les! cases!
phylogénétiques! en! répertoriant! et! classant! systématiquement! chacun! des! indices! de!
diversité!des!communautés!(c’est"à"dire!α!et!β)!alors!que!l’annexe!1!se!concentre!sur!les!
originalités!phylogénétiques!des!espèces.!J’explore!donc!ici!les!mesures!phylogénétiques!
uniquement,!mais!je!précise!en!discussion!les!nombreux!parallèles!avec!les!diversités!et!
originalités!fonctionnelles.!!
!
! "!56!"!
!
!
!
! "!57!"!
Partie!I!"!Chapitre!I!
CHAPITRE'I'
'
UNE'TENTATIVE'DE'SYNTHÈSE'EXHAUSTIVE''
DES'INDICES'PHYLOGÉNÉTIQUES'α'ET'β.'
! !
! "!58!"!
! "!59!"!
«"Diversity"indices"do,"however,"have"a"problem."They"combine"the"variable"we"are"trying"
to"measure"[…]."I"find"it"better"to"keep"variables"separated."
"That"sharpens"both"questions"and"analyses."»"
"
"
Michael!L.!Rosenzweig!(1995)!
!
! "!60!"!
!
Ce!premier!chapitre!vise!à!classifier!les!indices!de!diversité!phylogénétique!α!et!β!
en!grandes!familles!ou!«!variables!»!comme!le!précise!Rosenzweig.!
!
Résumé!de!l’article!1!(en!révision!dans!Biological!reviews)!
!!
L’utilisation!des!phylogénies!en!conservation,!en!écologie!des!communautés!et!en!
macro"écologie! est! devenue! commune! et! a! élargi! notre! compréhension! de! la! diversité!
biologique.! Ces! sous"disciplines! ont! reconnu! l’intérêt! de! l’utilisation! des! relations!
évolutives! mais! ont! développé! des! approches! phylogénétiques! de! façon! relativement!
indépendante.!La!prolifération!des!indices!de!diversité!phylogénétique!consécutive!à!ce!
manque! de! collaboration! empêche! aujourd’hui! les! méta"analyses,! les! synthèses! et! les!
généralisations!des!résultats!existants.!Par!ailleurs,!il!est!difficile!pour!les!utilisateurs!de!
sélectionner!un!indice!correspondant!à!une!question!donnée!car!les!indices!ne!sont!pas!
bien! reliés! aux! questions! de! recherche.! Pour! améliorer! ce! choix,! l’application! et!
l’interprétation!des!indices!de!diversité!phylogénétique,!nous!proposons!d’organiser!les!
indices!existant!dans!un!cadre!méthodologique!unificateur.!!
Les! questions! concernant! l’information! phylogénétique! dans! les! assemblages!
d’espèces! peuvent! se! résumer! en! trois! points!(les! «!variables!»! auxquelles! Rosenzweig!
fait! référence! dans! la! citation):! quelle! quantité!?! Quelle! différence!?! Quelle! régularité?!
Nous! montrons! que! ces! trois! questions! reflètent! trois! dimensions! d’un! arbre!
phylogénétique!:! sa! richesse,! sa! divergence! et! sa! régularité.! Nous! classifions! et!
répertorions! 73! indices! de! diversité! phylogénétique.! À! partir! de! cette! liste,! nous!
identifions! trois! indices! représentatifs! de! ces! dimensions! (les! «!variables!»! auxquelles!
Rosenzweig! fait! référence! dans! la! citation).! Dans! le! cadre! de! la! diversité! alpha,! ces!
indices!représentatifs!sont!:!!
!
(1) la!PDFaith!(Faith!1992)!représente!la!somme!des!longueurs!de!branches!reliant!toutes!
les!espèces!de!la!communauté.!
(2) le! MPD! (pour! «"mean! pairwise! distance"»! Webb! et"al.! 2002)! représente! la! distance!
phylogénétique!moyenne!entre!toutes!les!espèces!d’un!assemblage.!
(3) la!VPD!(pour!!«!variance!of!pairwise!distance!»)!représente!la!variance!des!distances!
phylogénétiques!d’un!assemblage.!!
! "!61!"!
!
Ce!cadre!méthodologique!est!dans!un!premier!temps!validé!avec!des!simulations!
et!nous!permet!d’identifier!les!indices!à!cheval!sur!plusieurs!dimensions.!Nous!montrons!
que!le!choix!de!l’indice!repose!sur!le!lien!entre!la!question!de!recherche!et!la!dimension!
correcte.!Le!guide!proposé!dans!ce!papier!aidera!les!chercheurs!à!se!retrouver!dans!la!
jungle!actuelle!des!indices.!!
!
Note!sur!la!participation!
!
Cet!article!est!le!fruit!d’une!collaboration!initiée!par!M.!W.!Cadotte,!J.!T.!Davies,!A.!
Mooers! et! D.! Rosaeur! dans! le! cadre! d’un! workshop! à! Leipzig! sous! la! tutelle! du! centre!
allemand!pour!la!recherche!intégrative!sur!la!biodiversité!(iDiv!&!sDiv)!coordonné!par!
M.! Winter.! C’est! mon! directeur! de! thèse,! Wilfried! Thuiller,! qui! a! soutenu! et! permis! ma!
participation!à!ce!travail!de!synthèse,!notamment!pour!partager!mes!connaissances!sur!
la!jungle!des!indices.!Mon!apport!majeur!dans!ce!travail!est!la!production!de!la!table!de!
classification! (Figure! 1! de! l’article! 1)! et! de! celle! répertoriant! tous! les! indices! utilisés!
(Matériel!supplémentaire!1).!!
! "!62!"!
A'guide'to'phylogenetic'metrics'for'conservation,'community'ecology'and'
macroecology!
'
Caroline!M.!Tucker1,!Marc!W.!Cadotte2,3,!Silvia!B.!Carvalho4,!Jonathan!Davies5,!Simon!Ferrier6,!Susanne!A.!Fritz7,!
Rich! Grenyer8,! Matthew! R.! Helmus9,10,! Lanna! S.! Jin11,! Arne! O.! Mooers12,! Sandrine! Pavoine13,14,! Oliver!
Purschke15,16,!David!W.!Redding17,!Dan.!F.!Rosauer18,!Marten!Winter15,!Florent'Mazel19.!
'
1!Department!of!Ecology!and!Evolutionary!Biology,!University!of!Colorado,!Boulder,!Colorado,!USA.!
2!Biological!Sciences,!University!of!Toronto"Scarborough,!Scarborough,!Ontario,!Canada.!
3!Stake!Key!Laboratory!of!Biocontrol,!Key!Laboratory!of!Biodiversity!Dynamics!and!Conservation!of!Guangdong,!Higher!Education!
Institutes,!College!of!Ecology!and!Evolution,!Sun!Yat"sen!University,!Guangzhou,!PR!China.!
4!CIBIO/InBIO,!Centro!de!Investigação!em!Biodiversidade!e!Recursos!Genéticos!da!Universidade!do!Porto,!Porto,!Portugal.!!
5!Department!of!Biology,!McGill!University,!Montreal,!Quebec,!Canada.!
6!CSIRO!Ecosystem!Sciences,!Climate!Adaptation!Flagship,!Canberra,!Australia.!!
7!Biodiversity!&!Climate!Research!Centre!(BiK"F)!and!Senckenberg!Gesellschaft!für!Naturforschung,!Frankfurt,!Germany.!!
8!School!of!Geography!and!the!Environment,!University!of!Oxford.!!
9!Department!of!Animal!Ecology,!Vrije!Universiteit,!Amsterdam,!The!Netherlands.!
10!Center!for!Biodiversity,!Department!of!Biology,!Temple!University,!Philadelphia,!PA!19122!USA.!
11!Ecology!&!Evolutionary!Biology,!University!of!Toronto,!Toronto,!Ontario,!Canada.!!
12!Department!of!Biology,!Simon!Fraser!University,!Vancouver,!BC,!Canada.!
13!Centre!of!Ecology!and!Conservation!Sciences,!French!Museum!of!Natural!History,!Paris,!France.!
14!Department!of!Zoology,!University!of!Oxford,!U.K.!
15!German!Centre!for!Integrative!Biodiversity!Research!(iDiv)!Halle"Jena"Leipzig!
16!Geobotany!and!Botanical!Garden,!Institute!of!Biology,!Martin!Luther!University!of!Halle"Wittenberg,!Halle!(Saale),!Germany.!!!
17!Centre!for!Biodiversity!and!Environmental!Research,!Department!of!Genetics,!Evolution!and!Environment,!University!College!London,!
London,!Britain.!!
18!Research!School!of!Biology,!Australian!National!University,!Canberra,!Australia.!!
19!Univ.!Grenoble!Alpes!&!CNRS,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France.!
'
The' use' of' phylogenies' in' ecology' has' become' common' and' has' broadened' our' understanding' of'
biological' diversity.' Ecological' subddisciplines,' particularly' conservation,' community' ecology' and'
macroecology,' all' recognize' the' value' of' evolutionary' relationships' but' the' resulting' development' of'
phylogenetic'approaches'has'led'to'a'proliferation'of'phylogenetic'diversity'metrics.'The'use'of'many'
metrics'across'the'subddisciplines'hampers'potential'metadanalyses,'syntheses,'and'generalizations'of'
existing'results.'Further,'there'is'no'guide'for'selecting'the'appropriate'metric'for'a'given'question,'and'
different'metrics'are'frequently'used'to'address'similar'questions.'To'improve'the'choice,'application,'
and'interpretation'of'phyloddiversity'metrics,'we'organize'existing'metrics'by'expanding'on'a'unifying'
framework'for'phylogenetic'information.''
Generally,'questions'about'phylogenetic'relationships'within'or'between'assemblages'tend'to'ask'three'
types'of'questions:'How'much?'How'different?'or'How'even?'We'show'that'these'questions'reflect'three'
dimensions' of' a' phylogenetic' tree:' richness,' divergence,' and' regularity.' We' classify' the' 73' existing'
phyloddiversity'metrics'based'on'their'mathematical'form'within'these'three'dimensions'and'identify'
‘anchor’' representatives:' for' αddiversity' metrics' these' are' PD' (Faith’s' phylogenetic' diversity),' MPD'
(mean' pairwise' distance),' and' VPD' (variation' of' pairwise' distances).' By' analyzing' mathematical'
formulas'and'using'simulations,'we'use'this'framework'to'identify'metrics'that'mix'dimensions,'and'we'
provide' a' guide' to' choosing' and' using' the' most' appropriate' metrics.' We' show' that' metric' choice'
requires'connecting'the'research'question'with'the'correct'dimension'of'the'framework'and'that'there'
are'logical'approaches'to'selecting'and'interpreting'metrics.'The'guide'outlined'in'this'paper'will'help'
researchers'to'navigate'the'current'jungle'of'indices.'
!
Key'Words.!Biodiversity"hotspots,"Biogeography,"Community"assembly,"Conservation,"Diversity"metrics,"
Evolutionary"history,"Phylogenetic"diversity,"Prioritization,"Range"size"
! "!63!"!
'
'
'
'
'
'
Contents.!!
!
I.'Introduction'
!
II.'A'unifying'framework'for'phyloddiversity'metrics!
(1)!Describing!the!framework!
!! (2)!Classifying!phylo"diversity!metrics!using!the!dimensions!framework!
(2a)"Richness"
(2b)"Divergence"
(2c)"Regularity"
(3)!Analysing!the!dimensions!framework!through!simulations!
'
III.'Additional'complexities'in'metric'choice'
(1)!Abundances!
(2)!Parametric!Indices!(Hill!numbers!and!entropies).!
(3)!Metrics!that!depend!on!species!richness!
!
IV.'Connecting'ecological'questions'and'hypotheses'with'phyloddiversity'metrics'
! (1)!Applying!richness!metrics!
! (2)!Applying!divergence!metrics!
! (3)!Applying!regularity!metrics!
'
V.'A'guide'to'phyloddiversity'metrics'
! (1)!Metric!selection!for!ecologists!
! (2)!An!example!of!metric!selection!
!
VI.'Moving'forward''
'
VII.'Conclusion'
'
VII.'Acknowledgements'
'
IX.'Works'Cited'
'
! "!64!"!
I.'Introduction.!! predict! ecosystem! properties! (Mouquet"et"al.,! 2012),!

Phylogenetic! information! is! a! critical! component! of! while!macroecology!uses!phylogenetic!information!to!
modern! ecology,! particularly! for! the! sub"disciplines! help!disentangle!explanations!for!large"scale!patterns!
of! macroecology,! community! ecology,! and! of! diversity! (Fritz! &! Rahbek,! 2012;! Jetz" et" al.,! 2012;!
conservation!biology!(Beck"et"al.,!2012;!Cadotte"et"al.,! Wiens"et"al.,!2004;!Winter"et"al.,!2009).!Despite!these!
2010b;!Crozier,!1992;!Davies!&!Cadotte,!2011b;!Faith,! different! foci,! there! is! considerable! overlap! in! sub"
1992;!Mouquet"et"al.,!2012;!Purvis"et"al.,!2000;!Vane" discipline! approaches! and! interests.! Indeed,! some!
Wright,! Humphries! &! Williams,! 1991;! Webb,! 2000;! metrics! are! commonly! considered! across! all!
Webb" et" al.,! 2002;! Winter" et" al.,! 2009).! The! growing! ecological! sub"disciplines,! such! as! Faith’s! PD! (Faith,!
use! of! phylogenies! recognizes! that! the! branching! 1992),! while! others! are! isolated! to! particular! sub"
pattern! on! a! phylogenetic! tree! reflects! the! disciplines,! e.g.! ED! (Isaac,! 2007;! Redding,! 2003)! for!
accumulation! of! phenotypic,! genetic,! behavioural,! conservation;!MPD!and!MNTD!for!community!ecology!
and/or! phenological! differences! between! (Clarke! &! Warwick,! 1998;! but! see! Davies! &! Buckley,!
evolutionary! lineages! (Harvey! &! Pagel,! 1991).! These! 2011a;!Webb"et"al.,!2002).!
accumulated! differences! may! in! turn! describe,! !
explain,!or!predict!biological!and!ecological!processes.! Choosing!the!most!appropriate!phylogenetic!measure!
The! potential! usefulness! of! phylogenies! to! answer! for!a!particular!ecological!question!is!complicated!by!
ecological! questions,! coupled! with! the! exponentially! the! vast! collection! of! phylo"diversity! metrics!
growing! availability! of! phylogenies! for! many! available.!Recent!overviews!(Chiu,!Jost!&!Chao,!2014;!
taxonomic!groups,!has!given!rise!to!a!proliferation!of! Mouquet" et" al.,! 2012;! Vellend" et" al.,! 2010;! Winter" et"
different! phylogenetic! metrics.! Currently,! there! is! an! al.,! 2013)! have! called! for! a! unifying! framework! for!
increasing! “jungle! of! [phylogenetic]! indices”! (Winter,! phylo"diversity! metrics,! in! order! to! clarify! the!
Devictor! &! Schweiger,! 2013)! of! more! than! 73! conceptual!relationships!between!existing!metrics,!to!
available! metrics! used! to! describe! phylogenetic! highlight!their!redundancies!or!complementarity,!and!
diversity! (here! “phylo"diversity”,! Appendix! S1).! This! to! ultimately! encourage! the! correct! usage! and!
jungle! reflects! not! only! the! increasing! number! of! interpretation! of! metrics! (Chao,! Chiu! &! Jost,! 2010;!
phylo"diversity! metrics! found! in! the! literature,! but! Chao,!Chiu!&!Jost,!2014;!Chiu"et"al.,!2014;!Faith,!2008;!
also! the! confusion! regarding! how! the! different! Pavoine! &! Bonsall,! 2011;! Pavoine,! Love! &! Bonsall,!
metrics!relate!to!each!other!in!both!mathematical!and! 2009;! Pearse" et" al.,! 2014;! Rosauer! &! Mooers,! 2013;!
ecological!terms.!! Schweiger" et" al.,! 2008;! Swenson,! 2011;! Tucker! &!
! Cadotte,! 2013).! A! recent! framework! developed! by!
Metric!choice!is!often!driven!by!historical!precedence,! Pavoine"&!Bonsall!(2011)!based!on!preliminary!work!
individual! experience,! and! sub"discipline! tradition,! by!Mouillot"et"al.!(2005)!and!Ricotta!(2007),!provides!
rather!than!objective!criteria.!Phylo"diversity!metrics! a! broad! clarification! of! the! mathematical!
first!appeared!in!conservation!biology!in!response!to! underpinnings! of! phylo"diversity! metrics,! allowing!
the! perception! that,! in! the! face! of! widespread! them! to! be! grouped! under! three! mathematical!
extinctions,!minimizing!loss!of!evolutionary!diversity! dimensions! (richness," divergence," regularity).!
should! be! a! priority! (Vane"Wright" et" al.,! 1991).! Although! the! Pavoine"Bonsall! framework! represents!
Maximizing! the! evolutionary! diversity! of! a! group! of! an! important! step! forward! in! clarifying! the!
species! should! maximize! their! feature! (i.e.! conceptual! relationships! underlying! metrics,! it! lacks!
phenotypic,! behavioral! and/or! ecological)! diversity,! (1)! comprehensive! classification! of! metrics,! since! it!
and! so! phylogenetic! measures! should! be! more! included! only! a! small! subset! of! published! phylo"
effective! than! species"based! measures! at! preserving! diversity! metrics,! and! (2)! guidance! for! the! correct!
such!diversity!(Faith,!1992).!Community!ecology!and! choice! of! metrics! and! connection! of! research!
macroecology! more! recently! incorporated! questions! with! the! appropriate! dimension.! The!
phylogenies! into! analyses,! using! evolutionary! purpose!of!this!article!is!to!provide!a!comprehensive!
relationships! to! understand! observed! ecological! and! and! practical! guide! to! understanding! and! correctly!
macroevolutionary! patterns! and! processes,! such! as! applying! phylo"diversity! metrics! for! ecological!
community! assembly! or! biodiversity! gradients.! questions.! This! should! help! in! selecting! from! among!
Community! ecology! tends! to! use! phylogenetic! the!73!metrics!currently!available,!while!emphasizing!
relatedness! between! taxa! or! communities! to! infer! the! value! in! distinguishing! between! and! utilizing! the!
local! ecological! processes! (Webb" et" al.,! 2002)! or! to! three!different!dimensions!of!phylo"diversity!metrics.!
! "!65!"!
We! establish! the! connection! between! the! types! of! measures! of! evolutionary! distances! (Pavoine" et" al.,!
ecological! questions! or! hypotheses! researchers! test! 2011;!Pearse"et"al.,!2014).!!
and! the! corresponding! dimension! identified! by! the! A! second! axis! of! information! in! this! framework!
Pavoine"Bonsall! framework.! Our! goals! are! to! reflects!whether!the!metric!uses!information!about!a!
incorporate! existing! phylo"diversity! metrics! into! the! single! set! of! tips! of! a! phylogenetic! tree! within! an!
framework! and! verify! their! fit,! analyse! redundancy! assemblage! (i.e.! questions! about! a! single! community!
and! distinguish! among! metrics! within! dimensions,! or! regional! species! pool,! hereafter! referred! to! as! α"
and!provide!examples!to!guide!their!use.! diversity),! or! about! several! sets! of! tips! (i.e.!
! comparisons! of! assemblages! over! space! or! time,!
II.' A' unifying' framework' for' phyloddiversity' hereafter!referred!to!as!β"diversity).!For!the!purposes!
metrics' of! this! paper,! assemblage! simply! denotes! a! group! of!
! taxa!of!interest:!such!taxa!may,!but!need!not,!co"occur!
(1)'Describing'the'framework.' in! space! or! time.! Examples! include! taxa! in! a! local!
Despite! the! vast! array! of! phylo"diversity! metrics,! a! community,!regional!species!pool,!or!those!selected!in!
simple!set!of!mathematical!underpinnings!provides!a! a! particular! conservation! strategy.! And! similarly,!
natural! scheme! to! group! the! metrics! into! three! though! we! may! refer! to! species! for! simplicity,! note!
conceptual! dimensions! (Pavoine" et" al.,! 2009):! that! the! metrics! discussed! are! often! applied! to!
richness,"divergence,"and"regularity.!These!dimensions! diversity! below! species! level,! or! where! species! have!
capture! the! mathematical! operation! inherent! to! a! not!been!described.!!
metric,! which! includes:! (a.)! the! sum! of! accumulated! !
phylogenetic!differences!among!taxa!(“richness”);!(b.)! This! framework! (1)! provides! an! intuitive! approach!
the!mean!of!the!phylogenetic!relatedness!among!taxa! based! on! the! mathematical! formulations! of! the!
(“divergence”),!representing!the!average!phylogenetic! metrics,! (2)! assesses! both! within"! and! between"
difference!between!taxa!in!an!assemblage;!or!(c.)!the! assemblage!diversity!components,!(3)!is!analogous!to!
variance!in!differences!among!taxa,!representing!how! the! functional! diversity! framework,! thus! aiding!
regular! the! phylogenetic! differences! between! taxa! in! comparisons!between!phylo"!and!functional!diversity!
an! assemblage! are! (“regularity”,! Figure! 1).! We! use! (Villéger" et" al.,! 2008)! ! and! (4)! is! applicable! for! both!
regularity! rather! than! the! similar! term! “evenness”,! abundance!and!presence/absence!formulations.!!
because! the! latter! has! previously! been! used! to! !
describe! how! abundances! are! combined! with! !
!
!
!
!
Figure' 1.' Conceptual' diagrams' illustrating' the' calculation' of' each' of' the' 3' dimensions' of'
phylogenetic'information:'richness'(left),'divergence'(centre),'and'regularity'(right).!The!branching!
diagram!in!each!image!is!a!phylogenetic!tree!representing!the!inferred!evolutionary!relationship!between!
taxa! A"I.! Taxa! A"I! are! grouped! within! three! assemblages! (A"D,! dark! grey;! E"G,! mid"grey;! and! H"I,! light!
grey).!Tree!branches!represent!accumulated!differences!between!taxa.!
!
! "!66!"!
Within! each! dimension,! different! phylogenetic! 2013;!Scheiner,!2012;!Swenson,!2011;!Vellend"et"

metrics!can!be!constructed!using!various!types!of! al.,! 2010;! Villéger" et" al.,! 2008;! Webb,! Ackerly! &!
phylogenetic! components! (referred! to! as! units):! Kembel,! 2008;! Webb" et" al.,! 2002;! Weiher! &!
these! include! branch! lengths," pairwise! Keddy,!1995).!Table!1!also!identifies!the!absence!
phylogenetic! distances! between! taxa,! measures! of! published! phylo"diversity! metrics! in! some!
of' phylogenetic! or! evolutionary! isolation! (e.g.! categories;! for! example,! β"diversity! (row! B)! in!
species! distinctiveness,! fair! proportion;! Isaac,! particular! lacks! metrics! in! a! number! of! possible!
2007;!Redding,!2003),!or!other!measures!of!tree! categories.! However,! particularly! for! α"diversity!
topology.! Thus! within! each! dimension,! we! metrics,! most! categories! in! Table! 1! include!
differentiate! between! metrics! based! on! the! multiple!phylo"diversity!metrics.!Further,!while!it!
phylogenetic!unit!used!for!their!construction.!We! is! likely! that! additional! metrics! will! be! found! in!
refer! to! groups! of! metrics! in! a! particular! the! literature! and! missed! here! (or! will! be!
dimension! that! are! constructed! using! the! same! developed! in! the! future),! we! believe! they! can! be!
units!as!“families”!For!example,!richness!metrics! easily!placed!within!this!framework.!
composed! using! branch! lengths! (e.g.! PD,! PE)! !
would! be! considered! a! family! based! on! their! (2a)'Richness,'Table'1d1.'
shared!dimension!and!unit!of!construction.! Richness! metrics! sum! up! the! quantity! of!
! phylogenetic! differences! present! in! an!
(2)' Classifying' phyloddiversity' metrics' using' assemblage,! and! we! can! further! distinguish!
the'dimensions'framework.' metrics! according! the! type! of! basic! units! they!
Here! we! use! the! dimensions! framework! sum!across.!Metrics!may!sum!branch!lengths!(e.g.!
introduced! in! (1)! to! classify! phylo"diversity! Faith's! phylogenetic! diversity! or! "PD";! ! Faith,!
metrics! used! to! answer! phylogeny"focused! 1992;! Table! 1"1.1a);! pairwise! phylogenetic!
ecological! questions.! We! searched! the! ecological! distances! (e.g.! Phylogenetic! Species! Richness,!
literature! and! identified! many! common! metrics! "PSR";!Helmus"et"al.,!2007;!Table!1"1.2a);!or!they!
not! classified! within! the! Pavoine"Bonsall! may! sum! the! evolutionary! distinctiveness! of! the!
framework,! for! a! total! of! 73! metrics.! These! taxa! in! an! assemblage! (or! total! Evolutionary!
metrics! are! diverse,! but! share! many! common! Distinctness,! "ED";! Jetz" et" al.,! 2014;! e.g.!
properties! (Pavoine" et" al.,! 2011;! Pearse" et" al.,! phylogenetic! endemism,! "PE";! Rosauer" et" al.,!
2014;! Vellend" et" al.,! 2010).! These! metrics! are! 2009;! Table! 1"1.3a).! Richness! metrics! that!
included! in! Table! 1,! classified! based! on! the! compare!diversity!between!sets!(Table!1"b)!may!
mathematical! dimension! (richness,! divergence,! calculate!the!proportion!of!shared!branch!length!
or!regularity)!and!the!diversity!level!(α"diversity,! between! two! communities! (e.g.! Unifrac,!
Table! 1"A;! β"diversity,! Table! 1"B).! Formulas! for! Lozupone" et" al.,! 2005;! Table! 1"1.1b)! or! a!
all! metrics! and! additional! details! are! found! in! proportional! measure! of! pairwise! phylogenetic!
Appendix!1!(metrics!from!Allen,!Kon!&!Bar"Yam,! similarities! among! species! (Pavoine" et" al.,! 2014;!
2009;! Barker,! 2002;! Bryant"et"al.,! 2008;! Cadotte" Table! 1"1.2b).! These! metrics! capture! the!
et"al.,! 2010b;! Chen"et"al.,! 2012;! Chiu"et"al.,! 2014;! difference! in! phylogenetic! composition! between!
Clarke" et" al.,! 1998;! Clarke! &! Warwick,! 2001;! assemblages.!
Colless,! 1982;! Dehling" et" al.,! 2014;! Faith,! 1992;! !
Hardy! &! Jost,! 2008;! Hardy! &! Senterre,! 2007;! (2b)'Divergence,'Table'1d2.'
Helmus"et"al.,! 2007;! Isaac,! 2007;! Ives! &! Helmus,! The! divergence! dimension! contains! metrics! that!
2010;! Izsák! &! Papp,! 2000;! Izsák! &! Szeidl,! 2002;! average!the!distribution!of!units!extracted!from!a!
Jost,! 2006;! Jost,! 2007;! Kembel" et" al.,! 2010;! phylogenetic! tree.! Divergence! metrics! that!
Leinster!&!Cobbold,!2012;!Lozupone"et"al.,!2007;! describe! a! single! assemblage! may! be! calculated!
Lozupone! &! Knight,! 2005;! Miller,! Zanne! &! using! branch! lengths! (Table! 1"2.1a),! pairwise!
Ricklefs,! 2013;! Mouchet! &! Mouillot,! 2011;! distances! (Table! 1"2.2a),! or! phylogenetic!
Nipperess,! Faith! &! Barton,! 2010;! Pavoine" et" al.,! isolation! (Table! 1"2.3a).! Distances! may! be!
2009;!Pavoine,!Ollier!&!Pontier,!2005;!Pavoine!&! measured!using!all!pairwise!distances!for!a!group!
Ricotta,!2014;!Pybus!&!Harvey,!2000;!Rao,!1982;! of! taxa! (e.g.! Mean! Pairwise! Distance,! "MPD";!
Redding,! 2003;! Rosauer" et" al.,! 2009;! Safi" et" al.,! Webb"et"al.,!2002;!Table!1.2.2.1a)!or!only!a!subset!
! "!67!"!
of! the! possible! pairwise! distances! (Table! 1" (δ!statistic)!and!tree!symmetry!(Ic!statistic)!using!

2.2.2a),! in! which! case! generally! the! shortest! sim.bdtree! function! in! the! R! package! geiger"
distances!between!taxa!are!considered!(e.g.!Mean! (Harmon"et"al.,!2008).!For!each!tree!we!created!8!
Nearest! Taxon! Distance,! "MNTD";! Webb" et" al.,! types! of! landscapes! (containing! 256!
2002).! For! metrics! that! compare! divergence! communities)! that! represented! simplified!
between! assemblages! (Table! 1"2b),! distances! outcomes! of! possible! assembly! processes,! using!
may!be!measured!using!branch!lengths!(e.g.!H_β,! the!scape"function!in!the!R!package!pez!(Pearse"et"
which!relies!on!additive!decomposition,!Mouchet" al.,! 2015).! These! landscapes! varied! in! whether!
et" al.,! 2011;! Table! 1"2.1b),! or! else! all! (Table! 1" (1)! there! was! a! phylogenetic! signal! (sensu!
2.2.1b)!or!the!shortest!pairwise!distances!(Table! Blomberg,! Garland! &! Ives,! 2003)! in! species’!
1"2.2.2b).! environmental! optima,! and! whether! that! signal!
! reflected! ‘repulsion’! (divergence! of! optima),!
(2c)'Regularity,'Table'1d3.! ‘attraction’! (convergence! of! optima),! or! no!
The! regularity! dimension! contains! metrics! that! phylogenetic! correlation,! (2)' range! size!
characterize! how! the! phylogenetic! tree! differs! (repulsion,! attraction,! no! signal),! and! (3)! spatial!
from! a! star! phylogeny! (i.e.! a! phylogeny! in! which! autocorrelation! in! range! distribution! ! (Table! 2).!
all!species!are!equally!unrelated).!In!other!words! Thus,!assemblages!in!these!landscapes!could!vary!
these!metrics!quantify!how!regularly!species!are! from! having! spatially! autocorrelated! ranges! and!
located! along! the! phylogenetic! tree! and! how! a! strong! phylogenetic! signal! for! range! size! and!
evenly! distant! they! are! from! each! other! species.! environmental! optima,! to! having! random!
They! are' grouped! into! three! families! based! on! assembly!with!no!phylogenetic!structure!in!range!
the! use! of! tree! topology! (Table! 1"3.1a),! pairwise! size! or! environmental! optima! and! no! spatial!
distances! (all! or! a! subset! of! pairwise! distances;! autocorrelation.!In!total!there!were!8!landscapes!
Table!1"3.2a),!or!phylogenetic!isolation!(Table!1" simulated!for!each!tree,!for!a!total!of!800!distinct!
3.3a).! We! did! not! identify! any! published! metrics! landscapes.!For!the!communities!in!each!of!these!
comparing!regularity!between!assemblages.! 800! landscapes,! we! calculated! values! for! the! α"
! diversity! and! β"diversity! metrics! listed! in! Table!
(3)' Analysing' the' dimensions' framework' 1.!!
through'simulations.' !
Table!1!represents!consensus!built!on!analysis!of! In!addition!to!these!analyses!using!the!trees!with!
mathematical! formulations! as! well! author! 64!taxa,!we!generated!100!trees!with!16!taxa!and!
opinions,! yet! metric! behaviour! may! still! vary! 100! trees! with! 256! taxa.! For! each! tree! size! we!
within! any! particular! subcategory! (e.g.! a! cell! in! similarly! simulated! 800! landscapes,! thus!
Table! 1),! since! metrics! that! share! general! constructing! a! total! of! 2400! landscapes.! We!
characteristics! may! still! differ! in! behaviour.! calculated! a! subset! of! α"diversity! metrics!
Additionally,! some! metrics! may! integrate! (omitting! abundance! weighted! and! parametric!
components! from! more! than! one! dimension! of! a! metrics,!for!a!total!of!27!metrics)!from!Table!1"A!
phylogeny.!Given!the!grouping!of!metrics!into!the! across! each! of! these! landscapes! to! consider!
three! conceptual! dimensions! in! Table! 1,! we! briefly! whether! metric! behaviour! is! sensitive! to!
predict! that! the! similarity! of! metrics! within! a! tree!size.!
dimension! should! be! higher! (e.g.! correlations! !
between! their! values! should! be! higher)! than! the! We! explored! the! underlying! relationships!
similarity!of!metrics!in!different!dimensions.!We! between! α"diversity! metrics! using! principal!
use! simulations! (described! briefly! below,! and! in! component! analysis! (PCA)! based! on! a! pairwise!
detail!in!Appendix!2)!to!evaluate!the!coherence!of! Spearman! correlation! matrix! between! all! α"
metrics!within!their!presumed!dimension,!and!to! diversity! metrics! for! each! landscape.! We! use!
identify! any! metrics! that! deviate! notably! from! Spearman!correlation,!as!it!is!robust!to!nonlinear!
their!dimension.! relationships! and! outliers.! We! included! all!
! metrics!from!Table!1"A!for!the!analysis:!for!visual!
We! simulated! 100! phylogenetic! trees! with! 64! clarity,!Figure!2!presents!only!presence/absence!
taxa,! with! a! wide! distribution! of! branch! lengths! metrics! and! excludes! parametric! metrics! and!
! "!68!"!
metrics! that! include! multiple! dimensions! (these! similarity! of! metrics! that! are! found! in! different!
metrics! are! presented! in! Figure! 5a! &! 5b).! The! dimensions,! although! interesting! divergences!
total! explained! variance! when! all! metrics! were! also!occur!(see!Section!III).!!
included! for! analysis! was! 44.2%! for! principal! !
component! 1,! and! 20.3%! for! principal! β"diversity! metrics! (Figure! 3)! capture! the!
component! 2.! The! remaining! axes! explain! much! dissimilarity! between! assemblages.! The! first! PC!
less! variation! (PC! 3! explained! 6.0%),! and! so! we! axis! explains! 22.9%! of! variance! and! the! second!
display! only! the! first! two! axes.! Note! that! we! use! PC!axis!15.6%.!The!first!axis!captures!a!gradient!
PCA! here! as! a! technique! for! visualizing! the! from!the!richness!dimension!(positive!values)!to!
relationships! between! metrics:! principle! the! divergence! dimension! (negative! values).! The!
component!axes!are!orthogonal!and!independent,! entropic! metrics! (Chiu"et"al.! (2014),! qD (T))! vary!
β
and! thus! not! expected! to! be! equivalent! to! the! from! being! highly! correlated! with! the! richness!
three!dimensions!we!have!identified.!Though!the! dimension!(q=0),!to!being!increasingly!associated!
dimensions! capture! different! aspects! of! that! with! the! divergence! metrics! as! the! value! of! q!
phylogeny,! ultimately! all! are! dependent! on! the! increases.! The! second! axis! captures! a! separate!
same! underlying! processes! of! evolution.! Hence,! source! of! information! from! the! dimensions!
fewer! than! three! independent! PCA! axes! should! framework! presented! here:! Swenson! (2011)!
be!necessary!to!capture!variation!related!to!these! showed! that! β"diversity! metrics! can! emphasize!
three!dimensions.! either! differences! among! communities! towards!
! the! base! (“basal”)! or! tips! (“terminal”)! of! a!
PCA!results!for!the!α"diversity!metrics!(Figure!2)! phylogenetic!tree.!In!our!simulations!large!values!
suggest! that! the! richness,! divergence,! and! along! the! second! axis! appear! to! capture! basal!
regularity! dimensions! are! clearly! divided! within! metrics,! such! as! Rao’s! D! (equivalent! to! Dpw),!
ordination!space!and!to!illustrate!this!we!use!the! while! known! terminal! metrics! such! as! Dnn! fall!
PD,! MPD,! and! VPD! metrics! as! anchors! or! close! to! zero.! This! suggests! that! for! β"diversity!
guidelines! for! the! expected! position.! The! metrics,! metric! choice! should! additionally!
majority! of! the! richness,! divergence,! and! consider!whether!it!is!more!of!interest!to!capture!
regularity! metrics! cluster! with! other! metrics! internal! versus! terminal! tree! structure! (Jin,!
from! the! same! dimension.! In! general,! richness! Cadotte!&!Fortin,!2015;!Swenson,!2011).!
metrics! load! on! positive! values! of! PC! 1! and! 2,! '
divergence!metrics!load!on!negative!values!of!the! Tree! size! of! the! source! pool! used! to! simulate!
second!axis,!while!regularity!metrics!tend!to!load! communities!influenced!the!similarity!of!metrics:!
on!negative!values!of!the!first!axis.!Divergence,!as! the! variation! among! α"diversity! metrics!
represented! by! the! position! of! MPD,! is! also! increased!when!trees!were!small!(16!taxa;!Figure!
captured! by! phylogenetic! species! variability! 4).! In! general,! the! multidimensional! space!
(PSV)! and! the! average! taxonomic! diversity! occupied! by! metrics! measured! on! landscapes!
(AvTD)! because! mathematically! these! metrics! constructed! with! 64! and! 256! taxa! trees!
are!identical!(Appendix!2).!It!is!notable!however,! overlapped,! while! the! metrics! calculated! for! the!
that! for! the! divergence! dimension,! metrics! that! trees! with! 16! taxa! tended! to! occupy! separate!
rely! on! nearest! neighbour! distances! (MNTD)! or! areas! of! the! ordination.! Further,! some! metrics!
phylogenetic!isolation!(mean(ED))!do!not!cluster! (e.g.!Ic,!upper!right!hand!corner,!Figure!4)!behave!
closely! with! MPD,! which! is! composed! using! all! similarly! regardless! of! tree! size.! To! completely!
pairwise! phylogenetic! distances.! Regularity,! as! understand! the! sensitivity! or! robustness! of! the!
represented! by! the! position! of! VPD,! is! closely! different! phylo"diversity! metrics! to! changes! in!
correlated! with! a! number! of! similar! metrics,! tree! size,! more! in"depth! analyses! would! be!
including!variance!in!nearest!taxonomic!distance! required.! Nonetheless! we! feel! our! conclusions!
(VNTD)! and! the! variance! in! evolutionary! about! metric! behaviour! within! the! dimensions!
distinctiveness! (var(ED)).! These! results! framework! will! be! generally! across! a! variety! of!
confirmed! that! the! similarity! of! metrics! within! a! tree! sizes! with! the! smallest! trees! accentuating!
dimension! is! generally! greater! (e.g.! correlations! the! small! differences! in! metric! calculations!
between! their! values! is! higher)! than! the! because! the! phylogenetic! signal! exhibited! by!
! "!69!"!
small! clades! is! inherently! variable! (Blomberg" et" questions! that! consider! a! larger! spatial! scale,!
al.,!2003).!! range! sizes! or! endemism! may! be! alternate!
! sources! of! abundance! information! (Isaac,! 2007).!
III.' Additional' complexities' in' metric' For! example! the! phylogenetic! endemism! metric!
formulation.' (PE;! Rosauer"et"al.,! 2009;! Table! 1"1.1a),! weights!
Though! the! metrics! generally! group! by! the! length! of! a! particular! branch! by! its! whole!
dimensions,! we! also! consider! a! number! of! geographic! extent! (defined! as! the! union! of! the!
additional! factors! that! can! alter! the! usage! and! distribution!of!species!descending!from!it).!Thus!
interpretation! of! phylo"diversity! metrics.! Metric! rarity! is! defined! as! species! with! small! ranges,!
behaviour!may!be!complicated!by!factors!such!as! rather!than!low!abundances.!!
the! inclusion! of! abundances,! underlying! !
correlations! with! species! richness,! and! the! Simulation! results! (Figure! 5a)! suggest! that! the!
emphasis!on!rare!versus!common!species.! incorporation! of! abundance! into! metrics! in! the!
! divergence! and! regularity! dimensions! produced!
(1)'Abundances,'Figure'5a.' metrics!that!behaved!similarly!to!other!metrics!in!
Species! abundances! are! often! an! important! the! same! dimensions.! Therefore,! when!
source! of! information:! for! example,! weighting! abundances!within!an!assemblage!are!of!interest!
schemes!using!abundances!or!range!sizes!have!a! for! questions! about! divergence! and! regularity,!
long! history! for! conservation! prioritization! appropriate! metric! choices! exist! and! can! be!
(Vane"Wright"et"al.,! 1991).! All! of! the! dimensions! clearly! interpreted! and! reasonably! compared! to!
of! phylogenetic! information! can! be! weighted! presence"absence! metrics! in! those! dimensions.!
using! some! measure! of! abundance! or! other! For! richness,! the! abundance! weighted! metrics!
weight! that! allows! information! about! species’! AED! and! PE! clustered! with! other! metrics! in! the!
commonness!or!rarity!to!be!incorporated!(Table! richness! dimension.! However,! several! richness!
1,! metrics! in! red! and! plotted! alongside! metrics! that! include! weighting! for! abundance,!
presence/absence!metrics!in!Figure!5a).!! such! as! abundance"weighted! phylogenetic!
! diversity! (PDaw)! or! average! abundance! weighted!
Abundances! may! be! incorporated! in! several! phylogenetic! diversity! (ΔnPD),! did! not! cluster!
ways.! For! metrics! applied! to! a! local! assemblage,! with! the! richness! metrics.! It! may! be! that!
species’! relative! abundances! may! be! sensitivity! of! these! indices! to! patterns! in!
incorporated.! This! is! the! ratio! between! species’! abundance! evenness! leads! their! behaviour! to!
absolute! abundance! (e.g.! cover,! number! of! converge! with! that! of! indices! from! the! other!
individuals,! or! biomass)! and! total! absolute! phylogenetic!dimensions,!and!so!the!user!should!
abundance! of! the! community! (e.g.! total! cover,! use! caution! when! interpreting! these! particular!
total! number! of! individuals! or! total! biomass).! metrics.!
Relative! abundances! are! then! used! to! weight! !
phylogenetic! units! such! as! pairwise! distances! (2)' Parametric' Indices! (Hill' numbers' and'
(e.g.!MPDAb;!Miller!et"al.,!2013;!Table!1"2.2.1a)!or! entropies),'Figure'5b.!!
branch! lengths! (e.g.! PDAw;! Vellend! et" al.," 2010;! Hill! numbers! are! a! group! of! diversity! measures!
Table1"1.1a).! There! are! two! general! weighting! that! aim! to! quantify! diversity! in! units! of!
schemes:! 1)! those! where! locally! abundant! equivalent! numbers! of! equally! abundant! species!
species!are!de"emphasized!relative!to!locally!rare! (Hill,! 1973).! Hill! numbers! incorporate!
species,!which!are!weighted!more!highly!because! information! about! abundances! and! variance! in!
they!may!be!important!for!conservation!(Cadotte! abundances,!and!retain!constant!units!(“effective!
&!Davies,!2010a);!versus!2)!those!that!emphasize! number! of! species”),! and! have! recently! been!
abundant! species,! such! as! when! analyzing! extended! to! include! phylogenetic! information!
species! contributions! to! ecosystem! function! (Chao"et"al.,!2010;!Chiu"et"al.,!2014;!Leinster"et"al.,!
(Cadotte" et" al.,! 2009).! Such! weighting! schemes! 2012).! These! frameworks! rely! on! a! unified!
allow! the! impact! of! the! number! and! relative! formula! of! phylo"diversity! that! is! adjusted! using!
abundance!of!rare!and!distinctive!species!in!local! a! single! “scaling! parameter”,! q.! The! value! of! q!
communities! to! be! considered! explicitly.! For! determines!the!influence!of!rare!taxa.!!
! "!70!"!
! correlated! with! the! richness! dimension! (PD),! as!

Within! the! richness/divergence/regularity! the! result! of! their! strong! underlying! correlation!
framework,! changes! in! the! value! of! the! q"scaling! with! species! richness! (since! PD! and! species!
parameter!affect!the!dimension!of!the!parametric! richness! are! also! often! highly! correlated).! Rao’s!
index! being! measured,! rather! than! simply! Quadratic! Entropy! (Rao’s! QE;! Table! 1"2.2.1a)! is!
altering! the! influence! of! rare! species,! as! is! the! primarily! an! index! of! divergence! (Clarke" et" al.,!
case! for! the! taxonomic! versions! of! these! metrics! 1998;! Rao,! 1982)! as! most! of! its! variation! occurs!
(Figure! 5b).! For! example! Chao’s! (2010)! q=0! and! along! the! divergence! dimension—but! it! is! also!
q=2! metrics! correspond! to! a! richness! and! a! slightly! correlated! with! the! richness! dimension!
divergence! metric! respectively.! In! contrast! the! since! it! includes! the! diagonal! of! the! distance!
Leinster!framework!(Leinster!et"al.,!2012;!qDZ(p))! matrix.! EED! behaves! differently! from! both! its!
varied! very! little! with! q" in! how! it! classified! component! dimensions! because! it! quantifies! the!
communities! in! our! framework.! Note! that! the! deviation! from! even! ED! and! so! is! uncorrelated!
Scheiner! framework! (Scheiner,! 2012),! although! with!species!richness.!!
reliant! on! q,! differs! from! the! parametric! indices! !
in! that! it! sums! species! level! evolutionary! For!some!metrics,!simple!transformations!can!be!
distinctiveness! (ED)! instead! of! summing! across! applied!to!remove!this!dependence.!For!example,!
edges! in! the! phylogeny.! Parametric! indices! indices!based!on!Hill!numbers!can!be!divided!by!
require! further! theoretical! treatment! and! species! richness! to! remove! its! effect.! The! effects!
applications! to! fully! determine! their! properties,! of! species! richness! and! abundance! evenness! can!
and! so! care! must! be! taken! in! selecting! and! be! removed! by! using! appropriate! null! models!
interpreting!them.! (Pavoine" et" al.,! 2013),! which! can! also! ease!
comparisons! with! functional! diversity,! since!
!
species! richness! and! abundance! evenness! may!
(3)' Metrics' that' depend' on' species' richness,' artificially! exaggerate! correlations! between!
Figure'5b.! phylogenetic!diversity!and!functional!diversity.!!
The! original! Pavoine"Bonsall! framework! was! !
defined!independently!of!species!richness!so!that! IV.' Connecting' ecological' questions' and'
multiplying! an! index! by! species! richness! (e.g.! hypotheses'with'phyloddiversity'metrics.'
PSR=PSV*Species!richness)!would!not!change!its! The! dimensions! classification! framework! unites!
classification!(both!PSR!and!PSV!were!considered! metrics! developed! in! across! ecological! sub"
in! Pavoine"Bonsall! framework! as! divergence! disciplines! and! used! for! different! purposes.!
indices).! Richness! is! here! defined! more! broadly! However,! the! framework! does! not! easily! resolve!
to!include!any!counting!of!evolutionary!units,!be! the! problem! of! choosing! among! metrics! for! a!
they! branch! lengths! or! other! phylogenetic! particular!analysis.!Ecological!questions,!whether!
distances.!As!a!result,!some!metrics!are!classified! from! conservation,! community! ecology,! or!
differently! from! the! original! work,! and! our! macroecology,! all! consider! how! accumulated!
richness! dimension! is! intrinsically! more! differences! between! species! (reflected! by!
influenced!by!species!richness!than!the!other!two! divergences! along! a! phylogeny)! may! relate! to!
dimensions.!! biological! processes! or! patterns.! Evolutionary!
! history!is!considered!an!outcome!or!predictor!of!
Several!indices!that!we!a"priori!classified!in!other! processes! of! interest.! We! suggest! that! questions!
dimensions!were!found!to!be!correlated!strongly! about! these! processes! or! patterns! can! be!
with! the! richness! dimension,! as! a! result! of! their! simplified! and! unified! to! recognize! the! three!
underlying! relationships! with! species! richness.! general! themes! of! How" much" total" diversity" is"
We! suggest! this! explains! the! behaviour! of! the! present"in"an"assemblage"(or"among"assemblages),!
parametric! indices! based! on! Hill! numbers,! How" different," on" average," are" taxa" in" an"
discussed! above,! as! these! are! by! definition! assemblage"(or"among"assemblages),!and/or!How"
dependent! on! species! richness.! HED,! HAED,! and! regular" or" variable" are" the" differences" between"
metrics! in! the! Scheiner! framework! combine! taxa" in" an" assemblage" (or" among" assemblages)!
phylogenetic! regularity! with! species! richness,! (Figure! 6).! We! review! below! the! types! of!
which! leads! their! behaviour! to! be! strongly!
! "!71!"!
questions!asked!by!ecologists!using!phylogenies,! be! an! outcome! of! different! ecological! and!

identify! commonalities,! and! connect! these! evolutionary! processes! (Cavender"Bares" et" al.,!
questions! with! appropriate! phylo"diversity! 2009;! Mouquet" et" al.,! 2012).! For! example,! as!
metrics.!! invasive! species! represent! a! non"random!
! combination! of! traits,! and! phylogenetic! metrics!
(1)' Applying' richness' metrics' (Figure' 6,' can!be!used!to!capture!such!‘feature!diversity’,!it!
column'1).'' may!be!hypothesized!that!invasion!should!lead!to!
Richness! metrics! can! be! used! to! measure! or! differential! changes! in! phylogenetic! richness! (α"!
describe! observed! patterns! of! diversity;! these! or! β"diversity)! compared! to! species! richness.!
values! may! also! be! compared! to! equivalent! Winter" et" al.! (2009)! tested! this! by! comparing!
taxonomic! and! functional! measures.! As! richness! taxonomic! and! phylogenetic! richness! metrics! in!
metrics! sum! the! quantity! of! phylogenetic! invaded! assemblages! (ultimately! showing! that!
differences! in! an! assemblage,! they! are! often! alien! species! led! to! a! decrease! in! phylogenetic!
assumed! to! capture! ‘feature! diversity’! under! distinctness! (i.e.! divergence)! rather! than!
some!models!of!trait!evolution!(Kelly,!Grenyer!&! richness).!In!a!separate!application!Thuiller"et"al.!
Scotland,! 2014).! In! this! context,! measures! of! (2011)! found! that! species’! vulnerability! to!
phylogenetic! richness! may! be! used! to! answer! climate! change! clustered! weakly! along! the!
questions! about! the! quantity! and! distribution! of! phylogeny,! and! used! this! relationship! to! predict!
extant!biodiversity,!arguably!better!than!species" how!the!amount!and!distribution!of!phylogenetic!
based! metrics! (Rosauer" et" al.,! 2013).! richness!will!change!in!the!future.!
Phylogenetics!offers!metrics!which!are!relatively! !
insensitive! to! taxonomic! inflation! (Isaac,! 2007),! (2)' Applying' divergence' metrics' (Figure' 6,'
and! which! can! easily! incorporate! taxa! (or! other! column'2).'!!
evolutionary! units)! for! which! there! is! little! Questions! about! ecological! communities! have!
information,! other! than! their! placement! on! the! frequently! considered! phylogenetic! distance! to!
tree!of!life.!Feature!diversity!may!be!considered!a! be! a! proxy! for! differences! in! functional! traits!
valuable! indicator! of! either! future! utility! or! (Ackerly,!2009;!reviewed!in!Freckleton,!Harvey!&!
future!evolutionary!potential!(Forest"et"al.,!2007;! Pagel,! 2002;! Mouquet" et" al.,! 2012;! Srivastava" et"
Mace,! Gittleman! &! Purvis,! 2003)! and! so! al.,! 2012),! with! the! assumption! that! closely!
conservation! biologists! have! been! interested! in! related!species!are!more!functionally!similar,!and!
the! protection! of! total! feature! diversity! for! thus!overlap!more!in!their!ecological!niche,!than!
questions! of! prioritization! of! taxa! and/or! areas! those!that!are!more!distantly!related!(Connolly"et"
(e.g.! Bennett" et" al.,! 2014;! Forest" et" al.,! 2007;! al.,!2011;!Gerhold"et"al.,!2015;!!but!see!Narwani"et"
Isaac,! 2007;! Jetz" et" al.,! 2014;! Purvis,! 2008;! al.,! 2013;! Purschke" et" al.,! 2013;! Violle" et" al.,!
Rodrigues"et"al.,!2011).!For!example,!Tucker!et"al.! 2011).! Underlying! this! are! additional!
(2012)! asked! how! Proteaceae! phylogenetic! assumptions!that!closely!related!species!occur!in!
diversity! was! distributed! spatially! in! the! Cape! sympatry!and!that!trait!evolution!is!divergent,!so!
Floristic! Province.! To! capture! the! total! the!most!similar!taxa!are!the!most!closely!related!
evolutionary! richness! in! a! spatial! unit,! they! (Gerhold" et" al.,! 2015).! When! these! assumptions!
considered! two! richness! metrics! to! consider! –! hold,! it! is! often! hypothesized! that! if!
PD,! and! the! sum! of! abundance"weighted! ED! environmental! filtering! drives! community!
(BED)!–!and!compared!the!distributions!of!these! assembly,! taxa! within! an! assemblage! will! be!
metrics! with! Proteaceae! species! richness! in! the! more! related! on! average! than! expected! in! a!
region.!! random! or! null! assemblage! (Cavender"Bares! &!
! Wilczek,!2003;!!but!see!Mayfield!&!Levine,!2010;!
Phylogenetic! richness! (either! α"! or! β"diversity)! Webb" et" al.,! 2002).! Alternatively,! if! competitive!
has! also! been! used! as! a! predictor! or! response! interactions! are! important,! it! may! be!
variable! in! numerous! studies,! across! multiple! hypothesized! that! co"occurring! taxa! will! be! less!
spatial!or!temporal!scales!and!for!diverse!natural! related! (i.e.! more! divergent)! than! expected! on!
systems.! Variation! in! phylogenetic! richness! average.! Divergence! indices,! particularly! MPD!
through! space! and! time! is! often! hypothesized! to! and! MNTD! indices,! have! been! used! to! test! these!
! "!72!"!
types! of! hypotheses! about! the! mean! relatedness! addition,! patterns! can! be! compared! to! null!
of! taxa! within! an! assemblage.! For! example,! expectations! generated! from! models! that!
Helmus! et" al.! (2010)! considered! whether! integrate! the! processes! of! speciation,! extinction!
disturbed! communities! tended! to! contain! more! and! colonization! (Pigot! &! Etienne,! 2015)!
closely! related! species,! reflecting! the! role! of! providing! more! powerful! tests! of! the!
environmental! filtering! in! selecting! disturbance" mechanisms! structuring! regional! species!
tolerance! taxa.! They! hypothesized! that! more! assemblages.!
closely! related! species! might! have! similar! traits,! !
and! so! be! similarly! adapted! to! disturbance! (3)' Applying' regularity' metrics' (Figure' 6,'
conditions.!To!test!this,!the!authors!used!the!PSV! column'3).'
metric,! which! is! closely! related! to! MPD,! and! The! regularity! metrics! appear! less! frequently! in!
compared! the! average! relatedness! of! species! in! the! literature,! and! we! identified! no! published!
disturbed! communities! versus! non"disturbed! examples!for!β"diversity.!They!are!typically!used!
communities.!! for! questions! about! how! evenly! evolutionary!
! history! is! distributed! between! taxa! in! an!
Note! that! although! these! are! frequently! assemblage,! and! as! with! divergence! metrics,! are!
expressed! hypotheses! in! community! ecology,! often! applied! with! the! assumption! that!
there! are! many! possible! relationships! between! phylogenetic!distance!is!a!proxy!for!differences!in!
phylogenetic! relatedness! and! co"occurrence! that! functional! traits.! Under! such! a! framework,! one!
can! be! tested! using! divergence! metrics.! Gerhold" might! hypothesize! that! greater! evenness! in! the!
et" al.! (2015)! provide! alternative! scenarios! that! distribution! of! similarity! among! species! should!
may! preclude! the! interpretations! described! result! in! lower! competition! (Kraft,! Valencia! &!
above!–!for!example,!trait!similarity!may!actually! Ackerly,! 2008).! Cadotte! (2013)! manipulated!
facilitate! coexistence! (see! also! Mayfield" et" al.,! phylogenetic!relatedness!and!species!richness!in!
2010),! competitive! exclusion! may! be! incomplete! plant! communities,! and! tested! whether! the!
in! assemblages,! and! regional! species! pools! and! selection! effect! (the! dominance! of! highly!
processes,! rather! than! local! processes,! may! competitive! or! productive! species,! one! putative!
determine!local!assembly.!Thus,!testing!questions! mechanism! underlying! the! diversity"ecosystem!
about! evolutionary! history! requires! both! function! correlation),! might! be! related! to! the!
identifying!the!correct!type!of!metric!for!a!given! topology! of! the! phylogenetic! tree.! In! fact,! the!
question! as! well! as! considering! the! assumptions! selection! effect! was! correlated! with! a! regularity!
that!might!relate!patterns!to!processes.! metric,! IAC.! As! regularity! metrics! reflect!
! evenness! in! the! distribution! of! dissimilarity!
The! phylogenetic! topology! of! species’! among! species,! this! finding! suggests! that! the!
assemblages! can! further! provide! information! selection! effect! is! strongest! when! closely! related!
about! processes! structuring! regional! species! species!are!present.!In!the!field!of!macroecology,!
pools! (Heard! &! Cox,! 2007;! Purvis" et" al.,! 2011),! Davies!and!Buckley!(2011a)!considered!variation!
and! the! likelihood! that! these! will! be! invaded! or! in! pairwise! distances! (VPD)! to! explore!
altered! (Gerhold" et" al.,! 2011).! Macroecological! unevenness!in!the!distribution!of!PD!globally!for!
studies! have! incorporated! information! about! terrestrial!mammals,!which!provided!insight!into!
divergences! in! phylogenies! to! compare! the!historical!processes!behind!global!patterns!of!
phylogenetic!distances!separating!sister!lineages! species!richness.!!
and!capture!variation!in!diversification!rates!(e.g.! '
Ackerly,!2009;!Weir!&!Schluter,!2007),!to!identify! V.'A'guide'to'phyloddiversity'metrics.!
geographical!centres!of!diversification!(e.g.!Jetz"et" Here! we! provide! a! robust! and! intuitive!
al.,! 2012),! or! the! drivers! of! niche! evolution! or! framework! to! guide! researchers! and!
conservation!(e.g.!Dormann"et"al.,!2009;!Wiens"et" practitioners! on! the! selection! and! matching! of!
al.,! 2004).! Such! macroecological! approaches! phylo"diversity! metrics! to! their! research!
allow!tests!of!whether!diversification!rates!differ! questions.! We! have! shown! that! the! different!
between! biogeographical! regions,! across! metrics! align! with! three! dimensions! of! phylo"
latitudes!or!at!different!times!through!history.!In! diversity:! richness,! divergence,! and! regularity;!
! "!73!"!
dimensions! that! themselves! align! naturally! with! confusing!inference!and!we!do!not!recommend!it.!

common! research! questions! (Figure! 6).! In! The! general! “phylogeny! should! be! important”!
highlighting! this! natural! linkage! between! hypothesis! that! accompanies! multi"metric!
research! questions! and! associated! hypotheses,! analyses! obscures! interpretation.! As! we! have!
phylogenetic! dimensions,! and! appropriate! presented! throughout! this! paper,! metrics! from!
metrics,! we! hope! to! facilitate! the! growing! usage! different! dimensions! should! not! be! treated!
of! phylogenies! in! ecology.! Further,! we! hope! that! interchangeably!as!they!represent!different!types!
this! work! will! encourage! researchers! to! choose! of! information! and! effectively! test! different!
amongst! existing! metrics! rather! than! formulate! hypotheses.!!
new!metrics!that!may!have!similar!properties!to! !
those!already!in!existence.!! A! recommended! strategy! is! to! find! the! most!
! appropriate!metric!through!a"priori!identification!
(1)'Metric'selection'for'ecologists.' of! the! key! components! of! the! research!
Importantly,! our! classification! framework! hypothesis.! If! our! question! is! about! the! total!
predicts! metric! behaviour! based! on! their! evolutionary!diversity!contained!within!a!reserve!
mathematical! properties.! Although! particular! (richness),! or! say,! the! average! species!
metrics! have! become! entrenched! in! particular! distinctness! (divergence)! within! assemblages!
fields,! we! show! there! is! mathematical! across! an! environmental! gradient,! then! the!
redundancy!among!them!and!alternative!metrics! correct! dimension! should! be! straightforward! to!
may!be!equally!able!to!address!similar!questions.! identify! (Figure! 6).! Once! the! dimension!
This! suggests! that! the! choice! of! metric! could! be! associated! with! the! question! is! identified,!
simplified.! Researchers! must! first! specify! researchers!can!restrict!their!choices!to!those!the!
whether! they! are! most! interested! in! describing! associated! column! in! Table! 1.! They! can! also!
properties!within!a!set!or!between!sets,!and!then! reduce! the! possible! metric! choices! to! those! for!
determine! whether! their! research! question(s)! either! α"diversity! or! β"diversity,! depending! on!
necessitate! the! use! of! “how! much”,! “how! which!they!are!asking!questions!about.!!
different”! or! “how! even”! dimensions.! By! placing! !
their! questions! within! these! dimensions,! the! In!some!cases!there!can!be!validity!in!comparing!
researcher! can! then! identify! the! set! of! most! multiple!metrics!within!a!dimension,!particularly!
appropriate! metrics! to! choose! from! (Figures! 7).! if!the!metrics!have!different!properties!(e.g.!units,!
The! choice! of! metric! need! not! depend! on! formulation)! of! interest! to! the! researcher,! and!
discipline,! or! whether! the! taxa! of! interest! they! are! all! appropriate! to! the! particular!
represent! those! found! in! an! experimental! question! or! conclusion.! In! addition,! high!
sample,! ecological! community,! biogeographical! redundancy!amongst!metrics!within!a!dimension!
region,!or!clade!of!conservation!interest.!! can! make! selection! among! them! somewhat!
! arbitrary.! As! a! result! it! may! usually! be! easier! to!
It! is! sometimes! suggested! that! the! choice! of! select! the! ‘anchor’! metric! that! represents! a!
statistical! analyses! should! be! made! a" priori,! dimension!(for!α"diversity,!PD!for!richness,!MPD!
during! experimental! design! and! before! or! perhaps! MNTD! for! divergence,! and! VPD! for!
performing! actual! experiments! (Underwood,! regularity),!given!their!ease!of!interpretation!and!
1997).! Although! this! is! frequently! unfeasible,! precedence!in!the!literature.!One!might!use!MPD!
especially! for! studies! using! observational! data,! when! questions! relate! to! branching! occurring!
this!is!meant!to!prevent!issues!related!to!multiple! deep! within! a! tree! versus! MNTD! for! questions!
comparisons! or! bias! in! variable! selection.! Such! related! to! terminal! branching.! ! Users! may!
issues! are! similarly! problematic! as! many! phylo" consider! alternatives! to! the! anchor! metrics! if!
diversity! metrics! are! used! interchangeably! in! these!provide!better!fit!to!a!specific!question!and!
analyses.!Although!simply!comparing!models!for! analysis.!For!example,!parametric!indices!(i.e.!Hill!
all! possible! metrics! and! selecting! the! one! with! numbers! across! a! range! of! values! of! q)" allow!
the! best! explanatory! power! has! been! employed! users! to! fully! consider! the! impact! of! rare! and!
in! the! past! (see,! e.g.! Cadotte,! 2013),! it! results! in! common! species! on! evolutionary! diversity.! In!
poorly! justified! analyses! and! potentially! addition,! they! may! be! used! for! comparative!
! "!74!"!
analysis! of! parametric! indices! across! this! would! be! to! select! a! metric! within! each!
phylogenetic,! taxonomic,! and! functional! dimension!following!the!recommendations!in!the!
diversity.! Alternatively,! users! may! want! to! previous! section! and! then! investigate! nested!
account! for! abundances! in! some! form! (range! models! with! subsets! of! the! metrics.! In! the!
sizes,! rarity,! etc.),! or! compare! results! for! example!above,!if!model!selection!suggests!that!a!
presence"absence! and! abundance"weighted! model! containing! both! richness! and! divergence!
versions!of!metrics!(e.g.!MPD!vs.!MPDab).!In!other! metrics!is!best,!a!researcher!might!conclude!that!
cases,! it! may! be! reasonable! to! select! a! metric! if! both!the!total!amount!of!history!and!the!relative!
direct! comparison! with! previously! published! spacing! of! species! are! important! predictors! of!
values! is! desired.! Even! in! these! cases,! we! stress! productivity.!
that! our! simulation! results! can! be! used! to! guide! !
interpretation! of! alternative! metrics,! including! (2)'An'example'of'metric'selection.'
through!comparison!of!their!behaviour!with!that! To!illustrate!the!process!of!metric!selection!with!
of!anchor!metrics.!! a! more! realistic! scenario,! we! provide! the!
! following! example.! Consider! an! island! mainland!
The! choice! of! phylogenetic! units! merits! system!with!a!number!of!plant!species!(Figure!7)!
additional! discussion.! Metrics! may! be! for! which! a! researcher! is! interested! in! how!
constructed! using! different! countable! units,! evolutionary! diversity! varies! between! the!
including! using! branch! lengths,! pairwise! mainland! and! island! (here,! sites! and! islands! will!
phylogenetic! distances! between! taxa,! or! be! referred! to! interchangeably).! The! researcher!
evolutionary!isolation.!Each!of!these!components! first!asks!whether!there!are!different!amounts!of!
can! be! measured! similarly! (i.e.! time! of! evolution! evolutionary! history! represented! by! the! plant!
in! millions! of! years),! and! should! rather! be! communities! at! each! site.! As! this! is! a! question!
understood! as! differing! in! their! “targets”! or! about!the!amount!or!sum!of!units!of!evolutionary!
objectives.! If! one! wants! to! conserve! as! many! history,! metric! choice! should! focus! on! the!
evolutionary! units! as! possible,! branch! lengths! richness! dimension! (see! questions! in! Figure! 6).!
should! be! the! target! of! interest.! If! users! wish! to! They! may! hypothesize! that! the! most! distant! site!
consider! competition! among! species,! pairwise! (Island! C)! will! share! the! least! amount! of!
distances! may! be! an! appropriate! choice! of! unit.! evolutionary! history! with! the! remaining! sites,!
Phylogenetic! isolation! should! be! the! target! if! since!its!distance!should!decrease!the!probability!
users! want! to! conserve! unique! species! or! relate! that! species! arrive! from! the! mainland! or!
conservation! prioritization! or! ecological! potentially! encourage! diversification! in" situ!
processes! to! differences! in! the! rate! of! (MacArthur! &! Wilson,! 1967;! Wiens"et"al.,! 2004).!
diversification! across! the! tree.! However,! it! is! To!compare!the!evolutionary!history!between!the!
important!to!note!that!metric!behaviour!often!did! three! sites,! the! researcher! chooses! a! β"diversity!
not! differ! significantly! between! metrics! within! richness! metric! (Table! 1"1B,! red! metrics! in!
the! same! dimension! but! constructed! using! Figure! 3),! perhaps! a! branch! length! based! metric!
different!units!(Figure!2).!! such! as! Faith’s! PDβ! that! captures! the! amount! of!
! shared!evolutionary!history.!Figure!3!shows!that!
There!could!be!some!cases!in!which!a!researcher! a!number!of!metrics!cluster!closely!and!appear!to!
wishes! to! consider! the! effect! of! multiple! capture! the! richness! dimension,! and! a! choice!
dimensions! on! a! process! or! variable! (for! between! these! (Unifrac,! SJaccard,! SSorensen)! should!
example,!how!does!primary!productivity!in!a!site! yield!very!similar!results.!
relate! to! richness! and! divergence! in! its! plant! !
community?).! It! is! possible! to! use! an! approach! Using! the! same! system! and! phylogeny,! the!
that! matches! questions! and! inference! to! the! researcher! asks! additional! questions! regarding!
metric,! while! also! assessing! how! the! different! whether! there! are! differences! in! how! evenly!
dimensions!influence!the!variable!of!interest.!For! evolutionary! history! is! distributed! within! the!
this! approach! the! analysis! would! consist! of! plant!assemblages!on!each!of!sites!A"C.!Given!that!
creating!a!statistical!model!that!includes!metrics! they!found!that!Island!C!shares!the!least!amount!
from! multiple! dimensions.! The! logical! way! to! do! of! total! evolutionary! history! with! the! other! sites!
! "!75!"!
(Figure!8"lower!panel!1),!and!Island!C!contains!a! to!data,!and!more!analyses!and!work!is!required!
number!of!endemic!species,!the!researchers!may! to!advance!our!understanding!of!these!metrics.!!
now! be! interested! in! whether! diversification! !
rates! differ! between! sites! and! if! the! endemic! In! our! analyses! we! simulated! a! large! number! of!
species! on! Island! C! reflects! a! recent! radiation.! landscape!types!and!randomly!generated!trees!in!
The!researchers!recognize!that!this!relates!to!the! order! to! capture! typical! or! average! metric!
evenness! or! regularity! of! the! distribution! of! behaviour.!However,!parameter!space!is!vast!and!
evolutionary!history,!and!so!they!choose!a!metric! future! simulations! should! consider! additional!
from!the!regularity!dimension!(Table!1"3A).!They! phylogeny!and!landscape!attributes!that!may!also!
hypothesize! that! assemblages! should! be! least! influence! metric! behaviour.! For! example,! it! is!
even! on! Island! C! because! the! biota! might! derive! understood! that! PD! is! strongly! correlated! with!
from! independent! colonization! events! by! SR,!though!less!so!when!trees!are!unbalanced!or!
evolutionary! distinct! lineages! (i.e.! lineages! distinct! species! are! also! spatially! restricted!
separated!by!large!phylogenetic!distances)!which! (Rodrigues,!Brooks!&!Gaston,!2005;!Tucker"et"al.,!
subsequently! radiated! in" situ,! giving! rise! to! 2013).! Thus,! more! complete! consideration! of!
clusters! of! species! separated! by! short! parameter!space!is!required!to!fully!assess!metric!
evolutionary!distances.!The!researchers!calculate! behaviour! across! a! range! of! phylogenetic!
VPD! for! each! site,! and! can! then! compare! these! topologies! and! branch! length! distributions,! as!
with! the! VPD! expected! were! island! biota! well! as! the! phylogenetic! signal! strength! in! niche!
randomly! assembled.! This! hypothetical! example! position!and!range!size.!Repeating!tests!with!real,!
illustrates! how! a! researcher’s! various! questions! rather! than! simulated! trees! would! also! provide!
can! be! simply! connected! with! phylo"diversity! important! information! on! expected! values! for!
metrics! and! how! careful! choice! leads! to! clear! metrics! in! natural! systems.! In! addition,! we! still!
interpretation!of!results.! must! determine! whether! metric! correlations! are!
! robust!to!all!types!of!phylogenies!and!landscapes,!
VI.'Moving'forward'' or!whether!certain!types!of!perturbations!inflate!
One!result!of!our!categorization!of!metrics!is!that! the!importance!of!subtle!metric!differences.!!
researchers!may!be!encouraged!to!look!beyond!a! !
single! oft"used! metric! and! dimension! and! We! believe! that! our! framework! supplies!
compare! different! dimensions,! as! the! is! already! guidance! to! researchers! and! practitioners! on!
done! with! the! analogous! framework! for! how! to! use! and! interpret! results! from!
functional! diversity! (Villéger" et" al.,! 2008).! For! phylogenetic! analyses.! As! noted! previously,! the!
example,!PD!and,!less!often,!abundance"weighted! three! dimensions! we! employ! are! simplifications,!
versions! such! as! PE,! have! been! the! dominant! although! their! use! in! both! functional! and!
measure! of! phylogenetic! information! in! phylogenetic! approaches! suggests! they! have!
conservation! biology! research.! Although! we! utility.! In! addition,! simulation! results! largely!
question!whether!the!multiplicity!of!phylogenetic! support! the! classification! of! metrics! and! so! we!
metrics!in!the!literature!has!in!general!advanced! suggest! that! this! framework! should! serve! as! a!
research,!conservation!biology,!more!than!for!the! starting! point! for! choosing! metrics,! applying!
other! fields,! has! limited! its! perspective! to! the! questions!and!interpreting!results.!!
richness! dimension! alone.! Metrics! from! the! !
divergence! or! regularity! dimensions! might! VII.'Conclusion.'
provide! complementary! information! about! the! (1)!The!use!of!phylogenies!in!community!ecology,!
distribution! of! biodiversity! across! taxa! in! a! site,! macroecology,! and! conservation! biology! reflects!
for!example.!! the! shared! recognition! that! accumulated!
! evolutionary! differences! may! explain! or! predict!
We! hope! that! this! paper! stimulates! broader! biological! and! ecological! processes.! Phylogenetic!
thinking! and! discussion! about! the! use! of! approaches! have! revolutionized! these!
phylogenies! in! ecology,! conservation! and! disciplines.!!
macroecology.! While! this! paper! represents! a! (2)! The! rapid! growth! of! new! phylogenetic!
starting!point!for!deciding!which!metrics!to!apply! metrics! has! limited! the! development! of!
! "!76!"!
phylogenetic! methods! in! ecology! and!

conservation,! and! prevents! meta"analysis! and!
clear!interpretation!of!metrics.!!
(3)!We!suggest!the!intuitive,!unifying!framework!
of! the! phylogenetic! dimensions! –! richness,!
divergence,! and! regularity! –! is! very! useful,! since!
it! applies! to! biological! questions! at! multiple!
ecological!scales,!for!single!or!multiple!groups!of!
species,!and!across!fields.!!
!(4)! We! encourage! appropriate! metric! selection!
by!highlighting!links!between!research!questions!
and! metrics! falling! in! the! appropriate!
phylogenetic! dimensions;! interpretation! is! made!
simple! by! understanding! the! relationship!
between! a! metric’s! dimension! and! the!
mathematical!basis!of!that!dimension.!!
(5)!Informed!metric!selection!and!interpretation!
will! allow! the! use! of! published! results! across!
subfields! and! applications! and! encourage! future!
work.!
!
VIII.'Acknowledgements.!!
This! paper! is! a! joint! effort! of! the! sPhy! working!
group! and! an! outcome! of! a! workshop! kindly!
supported! by! sDiv,! the! Synthesis! Centre! of! the!
German! Centre! for! Integrative! Biodiversity!
Research! (iDiv)! Halle"Jena"Leipzig! (DFG! FZT!
118).! ! CMT,! TJD,! MWC,! and! AOM! acknowledge!
NSERC! Canada;! MWC! thanks! the! endowed! TD!
Professor! of! Urban! Forest! Conservation! and!
Biology! chair.! SBC! was! funded! by! a! postdoctoral!
grant!from!Fundacão!para!a!Ciência!e!Tecnologia!
(FCT)! (SFRH/BPD/74423/2010),! and! through!
the! project! PTDC/BIA"BIC/118624/2010"
FCOMP"01"0124"FEDER"019676,! supported! by!
FEDER! funds! through! the! Operational!
Programme! for! Competitiveness! Factors! –!
COMPETE! and! by! National! Funds! through! FCT.!
MRH! is! supported! by! the! Netherlands!
Organisation! for! Scientific! Research!
(858.14.040).! FM! received! funding! from! the!
European! Research! Council! under! the! European!
Community’s! Seven! Framework! Programme!
FP7/2007"2013! Grant! Agreement! no.! 281422!
(TEEMBIO).! SAF! acknowledges! funding! by! the!
LOEWE! funding! program,! of!Hesse’s! Ministry! of!
Higher!Education,!Research,!and!the!Arts!
!
!
! !
! "!77!"!
'
0.2
Richness
Divergence
Regularity
0.1
PSR
PE
PD
VPD IC ED
0.0
PC Axis 2
var(ED)
VNTD
-0.1
PEve Hp
ࢢ
Raos QE
-0.2
avPD MNTD
mean(ED) MPD = PSV
=AVTD
-0.3
-0.2 -0.1 0.0 0.1 0.2 0.3

PC Axis 1
'
Figure' 2.! Principle! Components! Analysis! for! the! Spearman! correlation! between! the! alpha"
diversity! metrics! shown! in! Table! 1A.! Results! represent! measures! taken! from! 800! simulated!
landscapes,!based!on!100!simulated!phylogenetic!trees!and!8!landscape!types!defined!in!Table!2!
(detailed!methods!in!Appendix!2).!Excluded!from!this!plot!are!abundance"weighted!metrics!and!
those!classified!as!parametric!indices!(see!Figure!4!for!their!position).!X"and!Y"axes!are!scaled!to!
reflect!explained!variance.!Bolded,!boxed!metrics!reflect!‘anchor’!metrics!(PD,!MPD!and!VPD)!that!
align!most!closely!with!the!richness,!divergence!and!regularity!dimensions,!respectively.!
! "!78!"!
!
!
DIMENSION 1. Richness: How much? 2. Divergence: How different? 3. Regularity: How regular?
=> Sum of… Mean of … Variance of…
1.1 1.2 1.3 2.1 2.2 2.3 3.1 3.2 3.3

Branch Pairwise Phylogenetic Branch Pairwise distances/similarities Phylogenet Tree Pairwise distances Phylogenetic
lengths distances isolation lengths ic topology isolation
Unit =>
2.2.1 2.2.2 isolation 3.2.1 3.2.2
<=Level
All Nearest All Nearest
1.1a 1.2a 1.3a 2.1a 2.2.1a 2.2.2a 2.3a 3.1a 3.2.1a 3.2.2a 3.3a
Sum of branch Variance of species
Amount of lengths divided Effective number of species given Mean isolation metrics:
evolutionary Sum of Sum of by species phylogenetic balance and abundance shortest Mean of Branching Variance Variance Var(EDFP)
history: pairwise evolutionary richness: evenness: distance species symmetry of of nearest EED
q Z
Across distances: distinctiveness: avPD D (p)* between evolutionary and pairwise neighbour HED
species PSR sum(EDFP) Effective number Mean of all distances including zero a species distinctiveness distribution: distances: distances: HAED
!
PD F AED of species given intra-species distances: and all : IC ; ϒ VPD VNTD !! ! ) ∗
!
Across phylogenetic Rao QE, PSE, J others: mean(EDFP) IAC Λ+ VNTDab !!(!")*
A. Diversity individuals balance and Mean inter-species distances: MNTD VPDab PhyloEVE
within sets ΔnPD abundance MPD, MPDab, AvTD, PSV MNTD ab
Effective evenness:
!
!! ! ∗ & q>0
! ! !
!!" ∗ !!(!) ∗ & !!" ∗
Per species and associated
PDaw entropies:
"!79!"!
Endemic Hp*, Iq*
PE
1.1b 1.2b 2.1b 2.2.1b 2.2.2b
Average inter-set relative to intra-set

Amount of Sum of Effective number distances: Average
(un)shared inter-set of sets: SJaccard, Ssokal-Sneath, SSorensen, SOchiai minimum
!
evolutionary distances ! !! ! ∗ (with rel. abundances) distance
history: relative to Amount of Average inter-set distances between
Phylosor, intra-set entropy gained conditionally to intra-set a species
Unifrac distances: on average by (dis)similarities: of a set
Faith’s PDβ SJaccard, merging the PCD and all
Phylosorab, Ssokal-Sneath, sets: Amount of average distances gained species in
B. Diversity Unifracab SSorensen, Iqβ*, Hβ* on average by merging the sets: another
NA NA NA
between sets SOchiai Rao DISC set:
(with Proportion of average distances COMDIS
absolute gained on average by merging the TNT
abundances) sets:
Pst
Proportion of average inter-species
distances gained on average by
merging the sets:
Bst, Πst
Average inter-set distances:
COMDIST, Rao QAB, Dpw
Table'1'(previous'page).'The'dimensions'classification'system'for'phyloddiversity'indices.!
The!row!entries!distinguish!between!α"(within!a!set)!and!β"(between!sets)!diversities!while!the!
column!entries!represent!the!three!proposed!dimensions!of!phylo"diversity.!Within!each!of!these!
three! dimensions! (namely! richness' (red),' divergence' (yellow),! and! regularity' (green)),! we!
distinguish! between! different! phylogenetic! units! with! which! diversity! can! be! computed! (i.e.!
branch!lengths,!tree!topology,!pairwise!phylogenetic!distances!or!phylogenetic!isolation).!Species!
isolation! indices! measure! taxa! originality! within! a! set! (e.g.! species! distinctiveness,! etc.)! while!
pairwise!distances!represent!a!given!set!of!patristic!distances!(we!distinguish!between!pairwise!
distances!that!include!all!distances!and!those!that!include!only!the!nearest!distances).!For!each!
category!we!provide!verbal!descriptions!and!corresponding!published!indices.!For!example,!the!
indices!belonging!to!‘α"diversity/divergence!indices/based!on!nearest!pairwise!distances’!can!be!
defined!as!the!“Mean!shortest!distance!between!a!species!and!all!others”!with!the!corresponding!
published! indices! "! MNTD! and! MNTDab.! Empty! categories! indicate! that! there! are! no!
corresponding! published! indices! (of! which! we! are! aware).! Indices! coloured! in! red! can!
incorporate! abundances.! Starred! indices! (*entropies! and! Hill! numbers)! are! classified! as!
‘parametric!indices’!in!Appendix!S1,!for!their!shared!reliance!on!a!single!“scaling!parameter”,!q,!
that!determines!the!influence!of!rare!taxa!(see!also!Figure!4b).!Finally,!some!β"diversity!indices!
cited! are! dedicated! to! pairwise! comparisons! between! assemblages! while! others,! like! the!
parametric! indices! introduced! below,! can! handle! multiple! comparisons! among! more! than! two!
assemblages.!
!
!
!
Phylogenetic'
Environmental' Phylogenetic' Spatial'
Community' signal,' Range'size,'
optima,'signal' signal,' autocorrelation'
Type' environmental' signal'type'
type' range'size' range'
optima'
1! TRUE! Repulsion!(0.2)! FALSE! N/A! TRUE!
2! TRUE! Attraction!(20)! FALSE! N/A! TRUE!
3! TRUE! Repulsion!(0.2)! TRUE! Repulsion!(0.2)! TRUE!
4! TRUE! Attraction!(20)! TRUE! Attraction!(20)! TRUE!
5! FALSE! N/A! FALSE! N/A! TRUE!
6! FALSE! N/A! FALSE! N/A! FALSE!
7! FALSE! N/A! TRUE! N/A! TRUE!
8! FALSE! N/A! TRUE! N/A! FALSE!
! !
! ' ! ! !
Table'2.'Landscape!types!used!for!simulations!of!metrics:!numbers!indicate!parameter!values!in!
the! scape! function! of! pez.! For! a! trait,! values! of! 1! reflect! Brownian! motion,! values! less! than! 1!
reflect! rates! of! evolution! that! accelerate,! values! greater! than! 1! reflect! rates! of! evolution! that!
decelerate!through!time.!See!Appendix!2!for!additional!details.!
!
! "!80!"!
!
0.5
Richness Dpw Raos D

Divergence DpwAb Raos DAb
0.4
0.3
PC Axis 2
0.2
1
Dȕ(T)
ȆVW
Bst
0.1
2
Dȕ(T)
DnnAb S SSokalSneath
0.0
Beta
0
Dnn Dȕ(T)
Hȕ SOchiai
PhyloSor Unifrac
SSorensen S
-0.1
Jaccard
Faith’s PDȕ
-0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4

PC Axis 1
'
Figure'3.!Principle!Components!Analysis!of!the!Spearman!correlations!between!the!beta"diversity!metrics!
shown! in! Table! 1B.! Results! represent! measures! taken! from! 800! simulated! landscapes! and! 8! landscape!
types!defined!in!Table!2!(see!Appendix!2!for!details).!X"and!Y"axes!are!scaled!to!reflect!explained!variance.!!
! "!81!"!
Effect of species pool size

on alpha-diversity metrics
16 species
0.2
VNTD 64 species
IC YDU(' VNTDab 256 species
MNTD
IC MNTDab
IC ED
PD PHDQ('
0.1
VPDab
PSR
PDAW
ǻQ3'
GAM PE PEve AVTD MPD
AED PSV
IAC VPD PSE
HED
HED
ED GAMIAC PEve
MPDab
PDAW IACHED LQWUD03'ab
0.0
PD VED PD_Ab
PC2 8.946%
AED
PDAW PE VPD EED
VNTDabVNTD MNTDab
PSR
AED MNTD EED
PSR ǻQPD ED PEve
PD YDU(' PHDQ('
PE VPD
GAM
PD VPDab
LQWUD03'ab
-0.1
VNTD MPDab
VPDab
VNTDab
PSE
LQWUD03'DE
MNTDab PSV AVTD
MNTD MPD
ǻQPD PHDQ('
EED
-0.2
MPDab
PSE
AVTD
-0.3
MPD
PSV
-0.2 -0.1 0.0 0.1 0.2 0.3 0.4
PC1 12.83%
!
Figure' 4.' Effect! of! tree! size! on! relationships! between! a! subset! of! alpha"diversity! metrics.! Principle!
Components! Analysis! for! the! Spearman! correlation! between! 27! commonly! used! α"diversity! metrics!
shown! in! Table! 1.! Results! represent! measures! taken! from! 2400! simulated! landscapes,! based! on! 300!
simulated!phylogenetic!trees!with!three!different!sizes!(16,!64!and!256!taxa,!100!trees!of!each!size)!and!8!
landscapes! types! defined! in! table! 2! (detailed! methods! in! Appendix! 2).! Excluded! from! this! plot! are!
abundance"weighted!metrics!and!those!classified!as!parametric!indices!(see!Figure!4!for!their!position).!X"
and! Y"axes! are! scaled! to! reflect! explained! variance.! Bolded,! boxed! metrics! reflect! ‘anchor’! metrics! (PD,!
MPD! and! VPD)! that! align! most! closely! with! the! richness,! divergence! and! regularity! dimensions,!
respectively.! !
! "!82!"!
a) With Abundance-Weighted
Indices
0.2
Richness
Divergence IAC
Regularity AED
0.1
PSR
VNTDab PE
PD
VPD IC ED
0.0
var(ED)
PC Axis 2
PDaw
VNTD
-0.1
ǻQ3' PEve Hp
VPDab interMPDab
ࢢ
MPDab= Raos QE
-0.2
avPD MNTD
MNTDab PSE
mean(ED) MPD = PSV
=AVTD
-0.3
-0.2 -0.1 0.0 0.1 0.2 0.3

PC Axis 1
b) With Parametric Indices

0.2
Richness 1
1
D(P) D(AP)0D(P)
Divergence 2
D(AP) HED
Regularity HAED PSR D(P)
2
0.1
Parametric PE
0
D(T)
indices PD
VPD IC ED
0.0
PC Axis 2
var(ED)
1
VNTD D(T)
-0.1
2
PEve D(T)Hp
ࢢ EED 0
Dz(p)
Raos QE 1
Dz(p)
-0.2
2 z
MNTD D (p)
avPD
mean(ED) MPD = PSV

=AVTD
-0.3
-0.2 -0.1 0.0 0.1 0.2 0.3

PC Axis 1
!
Figure' 5.! Principal! Components! Analysis! showing! the! Spearman! correlation! for! the! alpha"diversity!
metrics!shown!in!Table!1,!results!represent!measures!taken!from!800!simulated!landscapes!(Appendix!2),!
including!A)!abundance"weighted!metrics!(underlined),!or' B)!parametric!indices!(underlined!and!shown!
in! black).! X"and! Y"axes! are! scaled! to! reflect! explained! variance! (PC1! =! 44.2%,! PC2! =! 20.3%! for! the! PCA!
performed!with!all!metrics).!Bolded,!boxed!metrics!reflect!‘anchor’!metrics!(PD,!MPD!and!VPD)!that!align!
with!the!richness,!divergence!and!regularity!dimensions,!respectively.!! !
! "!83!"!
Figure'6.'Connecting'the'dimensions'framework'to'ecological'questions.!Practical!definition!of!each!
dimension! and! example! questions! for! each! from! community! ecology,! macroecology,! and! conservation!
biology.! Included! are! questions! for! which! evolutionary! history! is! considered! as! a! (a.)! response! or! (b.)!
predictor!of!the!processes!of!interest.!Column!colours!correspond!to!the!three!dimensions!from!Table!1:!
richness!(sum,!red);!divergence!(mean!distance,!yellow);!and!regularity!(variance,!green)!
! !
! "!84!"!
!
!
4
5.3
B.
1.2
0.6
2.1 4 6
4.7 4.7
4.2
2.1 2.1
0.8 0.8 A.
C.
VPD = 21.3
B. B.
0.299 VPD = 25.4

Faith’s PDβ =
0.808
0.765
A. A.
VPD = 12.6
C. C.
1) 2)
'
Figure' 7.' Example' involving' the' flora' in' an' hypothetical' island' mainland' system! (top! panel),! for!
which! a! researcher! wishes! to! choose! appropriate! phylo"diversity! metrics! to! test! how! evolutionary!
diversity! varies! between! the! mainland! and! island! sites.! Details! in! Section! V"2.! The! top! panel! shows! the!
distribution! of! species! among! the! sites,! and! their! phylogenetic! relatedness.! Values! on! the! phylogeny!
represent! hypothetical! distances! between! species! (e.g.! branch! lengths,! etc).! Lower! panel! 1! shows! how!
evolutionary! history! is! shared! between! sites! (richness! metric,! β"diversity,! Faith’s! PDβ).! Lower! panel! 2!
shows! how! evenly! evolutionary! history! is! distributed! at! each! site! (regularity! metric,! VPD).
! "!85!"!
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! "!89!"!
Partie!I!–!Chapitre!II!
CHAPITRE'II'
'
L’IMPORTANCE'DE'L’ÉCHELLE'PHYLOGÉNÉTIQUE'
!
! "!90!"!
Partie!I!"!Chapitre!II!
!
!
Ce!deuxième!chapitre!se!focalise!sur!les!trois!indices!de!diversité!phylogénétique!
α!les!plus!couramment!utilisés!dans!la!littérature.!Je!tente!ici!de!comparer!les!propriétés!
de!ces!trois!indices!en!utilisant!un!modèle!nul!courant.!!
!
Résumé!de!l’article!2!(accepté!dans!Ecography)!
'
Durant!les!dernières!décennies,!la!description,!l’analyse!et!la!compréhension!de!la!
structure!phylogénétique!des!assemblages!d’espèces!ont!représenté!un!thème!central!en!
écologie! et! en! macro"écologie.! Parmi! la! grande! variété! des! indices! de! diversité!
phylogénétique,!trois!ont!été!majoritairement!utilisés!:!
!
(1) la! PDFaith! (Faith! 1992)! représente! la! somme! des! longueurs! de! branches! reliant!
toutes!les!espèces!d’un!assemblage.!
(2) le! MPD! (pour! «!mean! pairwise! distance!»! Webb! et" al.! 2002)! représente! la!
distance!phylogénétique!moyenne!entre!toutes!les!espèces!d’un!assemblage.!
(3) la!MNTD!(pour!«!mean!nearest!pairwise!distance!»!Webb!et"al.!2002)!représente!
la!distance!phylogénétique!moyenne!entre!les!espèces!sœurs!d’un!assemblage.!
!
Les! comparaisons! entre! les! études! sont! difficiles! car! il! n’existe! pas! à! l’heure!
actuelle!d’analyse!contrastant!la!structure!phylogénétique!que!chaque!indice!capture.!En!
particulier,!il!est!encore!mal!connu!comment!PDFaith!est!relié!aux!deux!autres!indices.!En!
conséquence,!il!est!possible!que!des!patrons!apparemment!contradictoires!entre!études!
soient!le!fait!d’une!simple!différence!entre!les!propriétés!des!indices.!Dans!cette!étude,!
nous! proposons! de! résoudre! ce! problème! en! comparant! de! façon! systématique! ces!
indices!en!utilisant!des!simulations!mais!aussi!des!données!réelles.!Premièrement,!nous!
utilisons! des! simulations! pour! tester! l’influence! de! la! structure! et! la! taille! de! la!
communauté!sur!les!différences!entre!indices,!tout!en!faisant!varier!la!forme!et!la!taille!
de!l’arbre!phylogénétique.!Dans!un!deuxième!temps,!nous!étudions!ces!différences!pour!
deux! jeux! de! données! empiriques! (microbiotes*! d’intestins! et! assemblages! de!
carnivores! à! l’échelle! planétaire).! Nous! montrons! que! le! MNTD! et! la! PDFaith!quantifient!
en! fait! une! dimension! récente! (c’est"à"dire! près! des! feuilles! de! l’arbre)! de! la! structure!
phylogénétique.!Au!contraire,!le!MPD!montre!un!comportement!totalement!différent!et!
!
"!91!"!
semble! très! sensible! à! la! structure! phylogénétique! profonde! (c’est"à"dire! près! de! la!
racine! de! l’arbre).! Nous! suggérons! qu’il! est! important! de! combiner! les! indices! qui! se!
focalisent! à! différentes! échelles! phylogénétiques! pour! obtenir! une! meilleure!
compréhension!de!la!structure!évolutive!des!assemblages.!!
! !
! "!92!"!
Influence'of'tree'shape'and'evolutionary'timedscale'on'phylogenetic'diversity'
metrics'
!
Mazel,!F.1,2,!Davies,!T.J.!3,4,!Gallien!L.!5,!Renaud!J.!1,2,!Groussin,!M.!6,!Münkemüller!T.!1,2!&!Thuiller,!W.!1,2!
!
1!Univ.!Grenoble!Alpes,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France.!
2!CNRS,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France.!!
3!Department!of!Biology,!McGill!University,!1205,!Avenue!Docteur!Penfield,!Montreal,!Quebec,!Canada.!
4!African!Centre!for!DNA!Barcoding,!University!of!Johannesburg,!PO!Box!524,!Johannesburg,!South!Africa.!
5!Swiss!Federal!Research!Institute!WSL,!8903!Birmensdorf,!Switzerland.!
6'Department!of!Biological!Engineering,!Massachusetts!Institute!of!Technology,!Cambridge,!MA,!USA'
!
Abstract.'
During' the' last' decades,' describing,' analysing' and' understanding' the' phylogenetic' structure' of'
species'assemblages'has'been'a'central'theme'in'both'community'ecology'and'macrodecology.'Among'
the' wide' variety' of' phylogenetic' structure' metrics,' three' have' been' predominant' in' the' literature:'
Faith’s' phylogenetic' diversity' (PDFaith),' which' represents' the' sum' of' the' branch' lengths' of' the'
phylogenetic'tree'linking'all'species'of'a'particular'assemblage,'the'mean'pairwise'distance'between'
all' species' in' an' assemblage' (MPD)' and' the' pairwise' distance' between' the' closest' relatives' in' an'
assemblage'(MNTD).'Comparisons'between'studies'using'one'or'several'of'these'metrics'are'difficult'
because' there' has' been' no' comprehensive' evaluation' of' the' phylogenetic' properties' each' metric'
captures.' In' particular' it' is' unknown' how' PDFaith' relates' to' MDP' and' MNTD.' Consequently,' it' is'
possible' that' apparently' opposing' patterns' in' different' studies' might' simply' reflect' differences' in'
metric' properties.' Here,' we' aim' to' fill' this' gap' by' comparing' these' metrics' using' simulations' and'
empirical'data.'We'first'used'simulation'experiments'to'test'the'influence'of'community'structure'and'
size' on' the' mismatch' between' metrics' whilst' varying' the' shape' and' size' of' the' phylogenetic' tree' of'
the' species' pool.' Second' we' investigated' the' mismatch' between' metrics' for' two' empirical' datasets'
(gut' microbes' and' global' carnivoran' assemblages).' We' show' that' MNTD' and' PDFaith' provide' similar'
information' on' phylogenetic' structure,' and' respond' similarly' to' variation' in' species' richness' and'
assemblage'structure.'However,'MPD'demonstrate'a'very'different'behaviour,'and'is'highly'sensitive'
to'deep'branching'structure.'We'suggest'that'by'combining'complementary'metrics'that'are'sensitive'
to'processes'operating'at'different'phylogenetic'depths'(i.e.'MPD'and'MNTD'or'PDFaith)'we'can'obtain'
a'better'understanding'of'assemblage'structure.'
'
' strongly!than!dissimilar!species!(HilleRisLambers!et!
Introduction' al.! 2012),! it! is! therefore! commonly! expected! that!
During! the! last! decades,! the! phylogenetic! structure! competition"driven! coexistence! will! generate!
of!species!assemblages!has!received!much!attention! patterns! of! phylogenetic! ‘over"dispersion’! (i.e.!
in! community! ecology! and! macro"ecology! since! it! distantly!related!species!with!less!niche!overlap!co"
holds!promise!to!help!unravel!the!drivers!of!species! occur).! Conversely,! phylogenetic! ‘clustering’! is!
coexistence! at! various! spatial! scales! (Webb! et! al.! thought! to! indicate! the! coexistence! of! closely!
2002,! Lozupone! and! Knight! 2005,! Mouquet! et! al.! related! species! because! of! shared! environmental!
2012,!Warren!et!al.!2014).' niches! (Webb! et! al.! 2002,! Mouquet! et! al.! 2012,!
Community! ecologists! have! considered! O’Dwyer! et! al.! 2012).! Although! the! link! between!
phylogenetic! distances! between! species! as! a! pattern! and! process! has! been! a! matter! of! some!
substitute! for! niche! differences! and! have! used! debate! (for! example,! see! Mayfield! &! Levine! 2010),!
phylogenetic! structure! to! disentangle! the! relative! non"random! phylogenetic! community! structure!
effects!of!biotic!and!abiotic!environments!in!shaping! appears!common.!
present!day!species!distributions!(Webb!et!al.!2002,! Recently,! macro"ecologists! have! also! used! the!
Mouquet! et! al.! 2012).! Coexistence! theory! predicts! phylogenetic! structure! of! assemblages! to!
that!species!sharing!the!same!niches!compete!more! understand! the! effects! of! historical! processes! on!
! "!93!"!
large! scale! biodiversity! distribution! (Davies! et! al.! phylogenetic! diversity! for! a! given! species! set!
2011,! Kissling! et! al.! 2012).! For! example,! explosive! relatively! to! the! species! pool! (whose! phylogenetic!
radiation! of! species! within! a! given! area! may! result! relationships! between! species! are! depicted! by! the!
in! the! co"occurrence! of! closely! related! species! “regional! tree”).! As! a! consequence,! a! negative!
resulting! in! phylogenetic! clustering,! while! multiple! standardized! metric! reflects! a! relative! clustering! of!
allopatric! speciation! events! may! lead! to! species!while!a!positive!standardized!metric!reflects!
phylogenetic!over"dispersion!(Warren!et!al.!2014).!! a!relative!overdispersion!of!species.!!
Among! the! plethora! of! phylogenetic! structure! MPD!and!MNTD!highlight!phylogenetic!structure!of!
metrics!that!have!been!developed!and!used!in!both! assemblages! at! different! evolutionary! depths! since!
fields! (Pavoine! and! Bonsall! 2011),! the! three! most! MPD! is! more! strongly! influenced! by! the! ‘basal’!
commonly! used! are! Faith’s! phylogenetic! diversity! structure! of! the! phylogenetic! tree! while! MNTD!
(named!PDFaith!hereafter),!which!represents!the!sum! describes! the! more! ‘terminal’! structure! of! the!
of! the! branch! lengths! of! the! phylogenetic! tree! phylogenetic! tree! (Webb! et! al.! 2002).! This! is! an!
linking!all!species!of!a!particular!assemblage!(Faith! important! aspect! since! different! processes! may! act!
1992),! the! mean! pairwise! distance! between! all! at! different! evolutionary! time! scales.! Some!
species! in! an! assemblage! (MPD)! and! the! pairwise! processes! may! produce! basal! clustering,! while!
distance! between! the! closest! relatives! in! an! others! may! create! terminal! over"dispersion,!
assemblage! (MNTD)! (Webb! et! al.! 2002).! As! PDFaith! generating! “clusters! of! overdispersion”! (see! e.g.!
correlates! closely! and! positively! with! species! blue!assemblages!in!Fig.!1).!For!example,!a!cluster!of!
richness!(SR,!e.g.!Tucker!and!Cadotte!2013),!the!use! overdispersion! could! be! due! to! environmental!
of! a! null! model! that! keeps! SR! constant! while! filtering! at! large! evolutionary! time! scales! and!
randomizing! phylogenetic! relationships! allows! competition! between! close! relatives! at! fine!
comparisons! of! assemblages! with! different! SR.! evolutionary!time!scale!(Hardy!and!Senterre!2007).!
Using!this!null!model,!standard!effect!size!(SES,!Eq.! Conversely,! “overdispersion! of! clusters”! would!
1)! and! relative! position! of! observed! values! with! correspond! to! basal! overdispersion! and! terminal!
respect!to!the!null!distribution!can!be!calculated.!! clustering! (see! e.g.! pink! assemblages! in! Fig.! 1).!
SES!can!be!defined!as:!! Consequently,! owing! to! their! property! to! detect!
! phylogenetic! structure! on! restricted! phylogenetic!
!"!. !"#$%& = !!
!"#$%&!"# !!"#$(!"#$%&!"## )
! (Eq.!1)! scales,! existing! metrics! may! be! limited! in! their!
!"(!"#$%&!"## )
ability! to! capture! complex! structural! patterns! and!
!
may!suffer!from!decreased!power!(i.e.!inflated!false!
where! Metricobs" is! the! observed! metric! in! a! given!
negative)! in! case! clustering! and! overdispersion!
assemblage,! and! Metricnull" is! the! same! metric! but!
occur!in!concert!at!different!phylogenetic!scales.!In!
calculated!n!times!with!n!randomised!assemblages.!
other!words,!if!clustering!and!overdispersion!occur!
The! relative! position! of! the! observed! value! with!
at!different!phylogenetic!scales,!using!a!metric!that!
respect! to! the! null! distribution! is! computed! as! the!
averages! the! information! over! the! entire! tree! may!
proportion! of! null! values! that! are! lower! than! the!
mask!these!two!opposing!patterns.!!
observed! values.! It! represents! the! probability! to!
While! differences! in! the! performance! of! ses.MPD!
draw! the! observed! value! from! the! null! distribution!
and!ses.MNTD!are!widely!recognised,!ses.PDFaith!has!
and! thus! corresponds! to! a! pLvalue! (Hnull! being! the!
mostly! been! considered! independently! or! as!
null! model).! For! normally! distributed! data,!
interchangeable! with! ses.MPD! and! ses.MNTD! (see!
significance! at! pLvalue<0.05! is! equivalent! to! a!
Table!1!and!Supplementary!Material!1!for!examples!
standard!effect!size!>!1.96!(or!<!"1.96).!!
and! their! detailed! justifications,! respectively).! To!
The!standard!effect!size!(and!associated!pLvalue)!of!
our!knowledge,!this!assumed!equivalence!has!never!
MPD! (ses.MPD! hereafter)! and! MNTD! (ses.MNTD!
been! validated! empirically.! Comparisons! between!
hereafter)! are! commonly! used! in! the! community!
studies! using! either! jointly! MPD! and! MNTD! or!
phylogenetic!literature!(also!referred!to!as!NRI!and!
PDFaith!(either!SES!of!metrics!and/or!corresponding!
NTI,! respectively,! Webb! et! al.! 2002),! and! can! be!
p"values)! are! thus! difficult! to! interpret,! and! it! is!
directly! compared! to! the! standard! effect! size! of!
possible! that! apparently! opposing! patterns! of!
PDFaith!(ses.PDFaith!hereafter).!All!three!standardized!
phylogenetic! structure! simply! reflect! differences! in!
metrics! quantify! the! relative! excess!
metric! properties.! While! a! number! of! macro/micro!
(overdispersion)! or! deficit! (clustering)! in!
ecological! studies! have! explored! patterns! of!
! "!94!"!
phylogenetic!metrics,!making!unique!and!important! of!different!sizes!(n!=!20,!40,!100!and!200!species).!
contributions! to! the! literature! (e.g.! Morlon! et! al.! For! each! regional! species! pool,! we! simulated! 100!
2011,! Fritz! and! Rahbek! 2012,! O’Dwyer! et! al.! 2012,! regional! phylogenetic! trees! of! size! n! using! a! pure!
see! Table! 1),! for! the! most! part! they! have! focussed! birth! model! (function! sim.bdtree" of! the! geiger! R!
only! on! PDFaith,! limiting! our! understanding! of! the! package;!Harmon!et!al.!2008)!for!which!we!reported!
phylogenetic! scale! at! which! processes! structuring! two! tree! shape! statistics:! imbalance! (Colless! 1982)!
species! assemblages! operate.! In! constrast,! and! Gamma! values,! quantifying! the! "tippiness"! vs.!
community! phylogeneytic! studies! frequently! "stemminess"! of! the! tree,! respectively! (Pybus! and!
measure! both! MPD! and! MNTD,! but! rarely! consider! Harvey!2000).!For!each!of!these!400!regional!pools!
PDFaith.! Choice! of! metric,! however,! is! often! poorly! (100! regional! trees! *! 4! tree! sizes),! we! constructed!
justified,! and! we! currently! lack! a! comparative! local! species! assemblages! by! randomly! drawing!
analysis! comparing! the! performance! of! these! three! without! replacement! m! species! from! the! regional!
widely!used!indices.! pool! (m" thus! equals! the! species! richness! of! the!
Here,! we! perform! the! first! comprehensive! corresponding! community).! We! repeated! this!
comparative! analysis! of! MPD,! MNTD! and! PDFaith! procedure! varying! m! from! 2! to! n"1! and! randomly!
using! both! simulations! and! emprical! data.! We! first! drawing! five! assemblages! for! a! given! species!
used! simulation! experiments! to! understand! the! richness! m.! To! test! the! influence! of! the! size! of! the!
relative! effect! of! (1)! the! size! and! the! shape! of! the! species! assemblage! on! our! three! metrics,! we! then!
regional!tree,!and,!(2)!the!richness!and!structure!of! grouped! assemblages! according! to! their! SR! and!
the! observed! community,! on! the! mismatches! reported! the! mismatches! between! metrics! for! each!
between! the! three! metrics.! Second,! we! evaluated! group! independently.! For! example,! with! a! regional!
metric! behaviour! on! real! world! datasets! for! gut! species! pool! of! 200! species,! we! created! 10! sets! of!
microbes! and! terrestrial! mammals.! Overall,! we! species! assemblages! with! different! ranges! of! SR!
show! that! MNTD! and! PDFaith,! are! both! ‘terminal’! (from!10!to!30!species!for!the!first!set,!30!to!50!for!
metrics,! and! thus! could! be! used! interchangeably,! the! second,! and! so! on! until! 170! to! 190! species! for!
while! MPD,! a! ‘basal’! metric! sensitive! to! deeper! the! last! set).! For! each! tree! and! each! set! of!
branching! structure,! captures! a! distinct,! but! assemblages! we! calculated! the! strength! of! the!
complementary! dimension! of! phylogenetic! relationship! between! ses.PDFaith! and! ses.MPD! or!
structure.! Their! combined! use! allow! for! a! better! ses.MNTD!as!the!R2!of!the!linear!regression!between!
understanding! of! assemblage! structure,! especially! them! (we! also! checked! for! more! complex! models,!
when! different! processes! operates! at! different! see!Results).!
phylogenetic! depths! simultaneously,! while! the! use! !
of! only! one! metric! could! lead! to! incomplete! Real"world"empirical"data"
interpretations!and!biased!conclusions.! To!compare!the!three!metrics!in!realistic!examples,!
! we!compiled!two!empirical!datasets!that!differed!in!
Material'and'Methods!! spatial!scale!and!assemblage!structure:!mammal!gut!
Simulation"experiments" microbial! assemblages! and! global! terrestrial!
In! a! first! set! of! simulations,! we! illustrated! the! carnivore!assemblages.!!
sensitivity! of! PDFaith,! MPD! and! MNTD! to! tree! shape! !
and! phylogenetic! structure! using! a! straightforward! Mammal"gut"microbial"assemblages"
toy! example.! We! generated! four! balanced! Species!assemblages!were!here!defined!as!the!set!of!
phylogenetic! trees! with! different! basal! vs.! terminal! microbial! Operational! Taxonomic! Units! (OTUs,! a!
branch!lengths!(see!Fig.!1!column!1).!For!each!tree,! taxonomic! concept! based! on! DNA! sequence!
we! compared! the! response! of! the! three! metrics! to! similarities! commonly! used! for! microbes)! living! in!
four! extreme! assemblage! structures:! phylogenetic! the!gut!of!different!mammalian!species.!We!used!the!
clustering! and! overdispersion,! clustering! of! 16S! rRNA! genes! dataset! from! Muegge! et! al.! (2011)!
overdispersion! and! overdispersion! of! clusters! (Fig.! to! derive! occurrences! of! 2,820! OTUs! (defined! at!
1)! 97%! of! similarity! to! create! species"like! entities)! in!
In! a! second! set! of! simulations,! we! tested! the! the! gut! of! 33! mammalian! species! (i.e.! 33! bacterial!
influence!of!regional!pool!sizes,!regional!tree!shapes! species! assemblages! from! a! regional! pool! of! n! =!
and!species!richness!of!the!assemblage!on!the!three! 2,820! OTUs)! and! to! reconstruct! a! regional!
metrics.!We!first!created!four!regional!species!pools! phylogenetic!tree!(see!Supp.!Mat.2.!for!details).!!
! "!95!"!
! short!internal!to!tip!branch!lengths;!tree!A!in!Fig.!1)!
Global"carnivore"assemblages" the!relative!rank!of!observed!MPD!versus!null!MPD!
We! used! the! distribution! maps! provided! by! the! suggests! clustering! while! PDFaith! (and! even! more!
Mammal! Red! List! Assessment! MNTD)! tends! towards! over"dispersion! (see! Fig.! 1).!
(http://www.iucnredlist.org/)! to! derive! the! This!difference!can!be!explained!by!the!sensitivity!of!
occurrence! of! 241! terrestrial! carnivores! (regional! MPD!to!deep!branching!structure!in!the!tree,!which!
species!pool).!We!then!defined!a!species!assemblage! are! counted! multiple! times! when! computing!
as! all! carnivores! co"occurring! in! a! given! 50x50km! pairwise! distance! between! all! species! in! the!
grid! cell.! Analyses! were! thus! carried! out! over! assemblage!(Webb!et!al.!2002).!Thus,!MPD!tends!to!
52,346! assemblages! around! the! world.! For! emphasise! the! basal! clustering! rather! than! the!
phylogenetic! relationships,! we! used! the! recent! overdispersion! within! the! cluster.! In! contrast,!
update! of! the! carnivoran! phylogeny! proposed! by! PDFaith! and! MNTD! are! less! influenced! by! internal!
Nyakatura! and! Bininda"Emonds! (2012)! as! the! branches! (they! are! completely! ignored! by! MNTD!
regional!tree.!! and! counted! only! once! for! PDFaith),! and! therefore!
! tend! to! be! more! sensitive! to! patterns! occurring! at!
Metric"calculation" the! tips! of! the! tree.! When! keeping! the! same!
For! both! simulated! and! empirical! datasets,! we! community! structure! (a! cluster! of! overdispersion,!
computed!the!observed!PDFaith,!MPD!and!MNTD!for! blue! curve)! but! switching! to! a! “stemmy”! tree! (i.e.!
each! assemblage! using! the! function! pd,! mpd! and! one! with! relatively! long! internal! to! tip! branch!
mntd!in!the!R!package!picante"(Kembel!et!al.!2010)." lengths;! tree! D! in! Fig.! 1),! MPD! still! suggests!
We! then! randomly! shuffled! the! tips! of! the! regional! clustering! and! MNTD! over"dispersion! but! PDFaith!
phylogeny! and! calculated! PDFaith,! MPD! and! MNTD! shifts!towards!clustering.!In!this!case!only,!PDFaith!is!
for! the! random! assemblages,! and! repeated! this! closer! to! MPD! than! to! MNTD! because,! even! though!
procedure!100!times!to!obtain!a!null!distribution!of! PDFaith! counts! internal! branches! only! once,! in! our!
values!for!each!assemblage!and!for!each!metric.!We! simple! simulation! they! have! a! profound! effect!
calculated! standard! effect! sizes! using! eq.1,! as! well! because! they! are! disproportionally! (and! perhaps!
as!the!relative!position!of!the!observed!index!in!the! unrealistically)!long!compared!to!tip!lengths.!When!
null! distribution! to! derive! pLvalues" (e.g.! Fig! 1).! All! considering! overdispersion! of! clusters! (red! curve)!
analysis! were! performed! using! R! (R! Development! on! the! same! stemmy! tree,! PDFaith! and! MNTD! were!
Core!Team!2014).! more! sensitive! to! the! signal! of! clustering,! whereas!
! MPD! was! more! sensitive! to! the! signal! for!
Results'&'Discussion' overdispersion.!This!simple!example!illustrates!that!
In! our! first! set! of! simulations! (see! Material! &! different! metrics! can! identify! apparently!
Methods! and! Figure! 1),! we! used! extreme! contrasting! patterns! in! the! same! dataset,! and! that!
assemblage! structures! to! illustrate! the! different! changes! in! tree! structures! can! alter! metric!
phylogenetic! signal! captured! by! PDFaith,! MPD! and! behaviour,! and! thus! the! inferences! we! might! draw!
MNTD,!respectively.!All!three!metrics!produce!very! from! them.! Overall,! PDFaith! and! MNTD! tend! to!
similar! predictions! in! the! case! of! simple! patterns! identify!similar!structure!(although!not!always),!but!
where! a! single! process! structures! species’! are!decoupled!from!MPD.!
assemblages! (Fig.! 1,! clustered! patterns! in! orange! Our!second!set!of!simulations!aimed!at!investigating!
and! over"dispersed! patterns! in! green).! We! also! whether! the! observed! mismatch! between! PDFaith!
explored! more! complex! phylogenetic! structures! and! MPD! was! still! apparent! with! a! less"extreme!
such!as!clusters!of!overdispersion!or!overdispersion! range! of! community! structures,! but! more! realistic!
of! clusters.! These! patterns! might! arise! when! regional! tree! shapes! and! richer! species!
different! processes! acting! at! different! depth! of! the! assemblages.!We!found!that!ses.PDFaith!and!ses.MPD!
tree! jointly! influence! assemblage! phylogenetic! were! still! largely! decoupled! while! ses.PDFaith! and!
structure.! In! these! more! complex! cases,! the! ses.MNTD! showed! congruent! results! (Fig! 2! and!
different! metrics! suggested! different! phylogenetic! Supp.! Mat.! 3"4).! While! regional! phylogenetic! tree!
structures,! with! these! differences! being! further! shape! and! species! pool! size! did! not! influence! the!
affected!by!phylogenetic!tree!shape!(Fig.!1).! discrepancies! between! ses.PDFaith! and! ses.MPD!
In!the!case!of!clusters!of!overdispersion!(blue!line!in! (Supp.! Mat.! 5"6)! correlation! strength! between!
Fig.!1)!on!a!very!‘tippy’!tree!(i.e.!one!with!relatively! metrics! decreased! with! increasing! species! richness!
! "!96!"!
(mean! SR)! of! assemblages! (Fig! 2! and! ! 3"4).! The! show!significant!‘basal’!clustering!(as!indicated!by!a!

richer! the! community,! the! more! complex! they! are,! significant! negative! ses.MPD! values),! but! little!
and!the!more!divergent!are!the!metrics.!Conversely,! structure! towards! the! tips! (as! suggested! by! non"
species! poor! communities! likely! have! less! complex! significant! patterns! of! ses.PDFaith! and! ses.MNTD).!
structures! that! are! easily! detected! by! all! three! This! pattern! may! reflect! the! very! unbalanced!
metrics.!! distribution! of! caniformia! and! feliformia! in! these!
The!analyses!of!empirical!data!match!to!the!results! regions! (see! Sup.! Mat.! 9)! suggested! to! be! the!
from! the! simulations.! Phylogenetic! pattern! of! both! outcome! of! the! interrelation! between! large"scale!
carnivore!diversity!and!gut!microbiomes!revealed!a! competition! and! historical! biogeography! (Pedersen!
clear!mismatch!between!ses.PDFaith!and!ses.MPD!(R2! et! al.! 2014).! In! Eurasia! and! North! America,!
=! 0.36! and! 0.19,! for! carnivores! and! microbes! caniformia! are! over"represented,! while! feliformia!
respectively,! Figs! 3"4),! and! greater! congruence! dominate!in!the!Congo!basin!(Pedersen!et!al.!2014;!
between! ses.PDFaith! and! ses.MNTD! (R2! =! 0.59! and! see! also! Supp.! Mat.! 9).! Thus,! these! regions! show!
0.96,!for!carnivores!and!microbes!respectively,!Figs! taxonomic!dominance!by!a!single!subclade,!which!is!
3"4).! These! results! were! almost! identical! when! apparent! in! the! “basal”! clustering! pattern,! while!
testing! for! linear! or! non"linear! relationships! there!is!little!regional!phylogenetic!structure!within!
between!the!metrics!(see!Supp.!Mat.!7"8).!The!clear! clades.! Taken! together! these! findings! demonstrate!
mismatch! between! indices! further! reveals! complex! that! one! single! phylogenetic! diversity! metric! is! not!
structures! that! cannot! be! summarized! by! a! single! able! to! fully! describe! the! complex! structure! of!
number!(i.e.!a!single!metric).!! assemblage! at! macro"ecological! scales! where!
Comparing! phylogenetic! structure! using! metrics! different! processes! may! operate! in! different!
sensitive! to! process! operating! at! different! geographical! regions! and! are! evident! at! different!
evolutionary! scales! sheds! new! light! on! the! phylogenetic! depths.! It! is! thus! important! to! use!
distribution!of!diversity.!Indeed,!for!carnivores,!the! multiple! metrics! that! focus! on! different!
differences!between!metrics!were!strongly!spatially! evolutionary!scales,!to!be!able!to!draw!more!precise!
structured!(Fig.!4).!In!some!parts!of!South!America,! and!robust!interpretations!of!phylogenetic!diversity!
both! ses.PDFaith! and! ses.MNTD! suggested! patterns! (see! e.g.! Davies! and! Buckley! 2011).! Our!
phylogenetic! clustering! which! were! not! evident! results! further! stress! the! importance! of! using!
from! patterns! of! ses.MPD.! Recent! radiations! of! multiple!metrics!in!the!analysis!of!large!datasets,!as!
particular! clades! within! the! neotropics! following! complex! macro"ecological! phylogenetic! structures!
the!Great!American!Biotic!Interchange!(Webb!2006,! can! emerge! when! studying! relatively! large! groups!
Woodburne! 2010)! "! for! example,! the! ocelot! genus! (see! O’Meara! 2012,! for! a! macro"evolutionnary!
leopardus"(Johnson!et!al.!2006)""!likely!results!in!the! perspective!on!this!subject).!!
co"occurrence! of! closely! related! species! (Pedersen! Our! findings! at! large! spatial! scale! also! extend! to!
et! al.! 2014)! at! the! continental! scale.! Niche! micro"biology,!as!we!observe!very!similar!trends!for!
partitioning! via! fine"scale! habitat! preferences! may! gut! microbial! assemblages! (Fig.! 4! and! Sup.! Mat.! 9).!
then!have!allowed!these!close!relative!species!to!co" For! example,! rodent! microbial! gut! assemblages!
occur! at! the! scale! of! our! analysis! (Araújo! and! appear! clustered! with! ses.PDFaith! or! ses.MNTD,! but!
Rozenfeld! 2014),! leading! to! ‘terminal’! phylogenetic! over"dispersed! with! ses.MPD! (Fig.! 4).! Therefore,!
clustering! (as! detected! by! ses.PDFaith! or! ses.MNTD).! when!using!only!metrics!of!ses.PDFaith!or!ses.MNTD,!
At! the! same! time,! because! South! American! one!would!have!concluded!that!rodent!microbial!gut!
carnivore!assemblages!also!contain!species!from!the! assemblages! mainly! consist! of! some! closely! related!
two!major!clades!of!carnivores!(i.e.!dog"!and!cat"like! lineages.! Whereas,! when! using! only! the! ses.MPD!
clades:! caniformia! and! feliformia,! respectively),! metric,! one! would! have! concluded! the! opposite:!
which! are! evolutionarily! distinct! from! each! other,! microbial! guts! assemblages! consist! of! distantly!
but!contain!approximately!equal!numbers!of!species! related!lineages.!!
(see! Pedersen! et! al.! 2014,! and! Supp.! Mat.! 9),! Again,!these!mismatches!among!metrics!seem!to!be!
regional! assemblages! tend! to! show! random! caused!by!an!over"dispersion!of!clusters!(see!Supp.!
phylogenetic! patterns! (as! indicated! by! ses.MPD! Mat.!10);!the!capybara!(Hydrochoerus"hydrochaeris)!
scores).! is! an! interesting! example.! Because! it! is! a! hindgut"
In!contrast!to!patterns!in!South!America,!the!Congo! fermenter! herbivore,! plant! residuals! reaching! the!
basin!and!some!parts!of!Eurasia!and!North!America! fermentative! part! of! the! gut! are! complex! to! digest!
! "!97!"!
(e.g.! cellulose! and! lignin,! Ley! et! al.! 2008)! and! a! Devictor! et! al.! 2010).! Interestingly,! when! using!
variety! of! plant! secondary! metabolites! need! to! be! presence/absence! data,! Rao! QE! has! a! non"linear!
broken"down! (Dearing! et! al.! 2000).! Consequently,! relationship! with! MPD! (Rao! QE! =! (m"1)/m! *! MPD,!
very! different! bacterial! clades! with! different! with! m! being! the! species! richness! of! the!
enzymatic! equipment! inhabit! the! gut! of! hindgut! assemblage)! so! that! the! two! metrics! essentially!
herbivores,! possibly! generating! observed! patterns! carry! the! same! information.! As! a! consequence,! our!
of! ‘basal’! overdispersion,! i.e.! co"occurrence! of! results!suggest!that!Rao!QE!would!also!represent!a!
distantly!related!bacterial!lineages.!However,!within! ‘basal’! metric! of! phylogenetic! diversity,! although!
these! clades,! host"specific! processes! structuring! this!remains!to!be!verified.!!
bacterial! assemblages,! such! as! mucus! barriers,! To! better! link! macro"ecology,! community! ecology!
oxygen! concentration! and! the! innate! and! adaptive! and!microbial!ecology,!our!analysis!only!focused!on!
immune! systems,! may! select! for! specific! bacterial! presence"absence! data! since! abundance! data! is!
lineages! (Salzman! et! al.! 2010,! Bevins! &! Salzman! often! not! available! at! macro"! and! micro"ecological!
2011,! Hooper! et! al.! 2012)! favouring! clustering! of! scales.!However,!we!suggest!that!issues!raised!here!
bacterial! lineages.! Thus,! similarly! to! the! case! for! for! presence"absence! data! are! likely! to! also! occur!
global!carnivoran!communities!discussed!above,!we! when!metrics!are!computed!with!abundance!data.!It!
show!that!a!set!of!complementary!metrics!is!needed! is! nonetheless! not! trivial! to! extend! our! simulation!
to! accurately! describe! the! complex! phylogenetic! framework! to! incorporate! abundances! because!
structure!of!micro"biomes.!! additional! assumptions! have! to! be! made! on! the!
We! have! classified! phylogenetic! metrics! as! either! relative! abundances! of! species! within! the!
‘terminal’!or!‘basal’,!and!we!show!that!ses.PDFaith!is!a! simulations,! for! which! many! possible! scenarios!
‘terminal’! metric! that! reflects! the! phylogenetic! exist.! Additionally,! since! other! metrics! and! recent!
structure! that! is! dominant! near! the! tip! of! the! tree.! developments! have! been! proposed! to! specifically!
Recent! reviews! on! metrics! of! phylogenetic! beta! include! abundances! (e.g.! Chao! et! al.! 2010,! Faith!
diversity! (Swenson! 2011)! and! evolutionary! 2013),! more! comprehensive! tests! need! to! be!
isolation!(i.e.!phylogenetic!“structure”!at!the!species! conducted! to! evaluate! the! influence! of! species’!
level,! Redding! et" al.! 2014)! have! followed! a! similar! abundance!on!detected!patterns.!!
classification,!placing!emphasis!on!the!phylogenetic! !
depth! at! which! patterns! emerge.! For! example,! Conclusion'
Swenson! (2011)! classified! Unifrac! (Lozupone! and! The! use! of! PDFaith,! MPD! and! MNTD! to! characterize!
Knight!2005)!and!PhyloSor!(Bryant!et!al.!2008),!the! the! phylogenetic! structure! of! assemblages! and!
beta! diversity! equivalents! of! PDFaith,! as! ‘terminal’! regional! species! assemblages! is! common! in! the!
while! Dpw! (Webb! et! al.! 2008),! the! beta! diversity! ecological! literature.! However,! the! choice! of! one!
equivalent! of! MPD,! as! ‘basal’.! Similarly,! Redding! et! metric! over! another! seems! more! the! product! of!
al.! (2014)! suggested! that! the! fair! proportion! historical!contingencies!rather!than!methodological!
evolutionary! distinctiveness! metric! (Isaac! et! al.! properties.! For! example,! studies! linking!
2007),! the! equivalent! of! PDFaith! at! the! species! level,! phylogenetic!diversity!to!area!(Morlon!et!al.!2011),!
best!captures!‘terminal’!isolation,!while!the!‘average! productivity! (Cadotte! et! al.! 2008)! or! functional!
phylogenetic! distance’! (Ricotta! 2007),! the! diversity! (Safi! et! al.! 2011)! have! adopted! PDFaith! as!
equivalent! of! MPD! at! the! species! level,! is! more! the!natural!extension!of!species!richness!(SR).!This!
closely!linked!to!the!‘basal”!isolation!of!species.! is! an! interesting! avenue! but! explores! only! one!
Our!analysis!focused!on!the!three!most!widely!used! single! –recent"! dimension! of! the! phylogenetic!
metrics! in! (macro)! ecology.! There! are,! however,! a! structure! of! communities.! Adding! metrics! that!
large! number! of! available! metrics! in! the! literature! detect!deeper!phylogenetic!structures!(such!as!MPD!
that!have!been!proposed!over!the!last!decades!(see! or! Rao! QE)! may! in! fact! reveal! different! processes!
Pavoine! and! Bonsall,! 2011,! for! a! synthetic! review).! and! thus! complete! our! understanding! of! diversity!
It! is! beyond! the! scope! of! the! paper! to! review! and! distribution.!
compare! all! available! metrics,! and! additional! Here,! we! have! demonstrated! that! the! choice! of!
studies! are! needed! to! extend! our! results! to! other! metric! can! significantly! impact! inferences! on!
metrics.! For! example,! the! Rao! Quadratic! Entropy! dominant! patterns! and! thus! interpretation! with!
(Rao! QE,! e.g.! Pavoine! and! Bonsall! 2011)! is! also! regard! to! potential! underlying! processes.! We! show!
widely!used!to!describe!phylogenetic!structure!(e.g.! that! MNTD! and! PDFaith! behave! similarly,! but! that!
! "!98!"!
MPD! is! more! sensitive! to! deeper! branching!

structures.! Our! results! extend! the! findings! of!
Swenson!(2011)!for!beta!diversity!metrics!to!alpha!
diversity! metrics! in! distinguishing! between!
relatively! ‘basal’! or! ‘terminal’! metrics.! We! call! for!
the! joint! use! of! complementary! metrics! (i.e.! MPD!
and!PDFaith!or!MNTD)!to!better!understand!patterns!
of!species!assemblage.!!
!
Acknowledgments.!
The! research! leading! to! these! results! had! received!
funding!from!the!European!Research!Council!under!
the! European! Community’s! Seven! Framework!
Programme! FP7/2007"2013! Grant! Agreement! no.!
281422! (TEEMBIO).! FM,! TM! and! WT! belong! to! the!
Laboratoire! d’Écologie! Alpine,! which! is! part! of!
Labex! OSUG@2020! (ANR10! LABX56).! All!
computations! were! performed! using! the! CiGRI!
platform! of! the! CIMENT! infrastructure!
(https://ciment.ujf"grenoble.fr),!which!is!supported!
by! the! Rhône"Alpes! region! (GRANT! CPER07_13!
CIRA)! and! France"Grille! (http://www.france"
grilles.fr).!TJD!was!supported!by!a!team!grant!from!
the! Fonds! de! recherche! du! Québec! –! Nature! et!
technologies!
! "!99!"!
TABLE'1'Hypotheses'tested,'key'papers'and'corresponding'metrics'used'across'fields'to'depict'the'
phylogenetic'structure'of'species'assemblages.'The!table!depicts!for!each!of!the!two!considered!field!of!
research! (column! 1)! the! hypotheses! tested! behind! classic! phylogenetic! patterns! (column! 2)! and! key!
papers!using!either!MPD/MNTD!or!PDFaith!(column!3).!
'
Metrics!used!to!quantify!the!pattern;"
! Hypotheses!related!to!the!two!patterns:"
examples!of!key!publications"
Fields" Clustering" Over"dispersion" Biotas" MPD/MNTD"
Micro"biotas" PDFaith"
Goberna!et"al.!2014" O’Dwyer!et"al.!!
Bryant!et"al.!2008" 2012"
Community!ecology"
Environmental!
Competition"
filtering*"
Macro"Biotas"
Webb!et"al.!2002;!! Cadotte!et"al.!2009;!
Graham!et"al.!2009;" Morlon!et"al.!2011"
Biogeographic!!
Macro"ecology"
contact!zones;"
In"situ!! Cardillo!2011b;!! Fritz!&!Rahbek!!
Vicariance;"
speciation! Davies!&!Buckley!2011" 2012"
Competition!!
at!large!scale"
*but!see!Mayfield!&!Levine!2010!
' '
! "!100!"!
'
'
Figure'1.'Sensitivity'of'PDFaith,'MNTD'and'MPD'to'different'assemblage'structures'and'
tree' shapes.' The! figure! depicts! four! balanced! trees! (column! ‘Tree’)! along! with! four!
potential! assemblage! (column! ‘Assemblage’):! coloured! segments! indicate! that! the!
corresponding!tips!on!the!phylogeny!are!present!in!the!assemblages!(i.e.!species!presence);!
from! left! to! right:! simple! simple! overdispersion! in! green;! clustering! of! overdispersion! in!
blue;!overdispersion!of!clusters!in!red;!and!simple!clustering!in!orange.!The!corresponding!
diversities! are! presented! in! the! third! column.! Values! on! the! X"axis! correspond! to! the!
relative! position! of! observed! value! compared! to! a! null! distribution! (interpreted! as! a! pL
value).! For! example,! a! value! of! 0! indicates! that! the! observation! is! lower! than! all! null!
expectations!(‘clustering’)!while!a!value!of!0.5!indicates!that!the!observation!equals!to!the!
median!of!the!null!distribution.!The!different!metrics!are!represented!by!different!symbols!
(see!legend).' !
! "!101!"!
!
!
Figure' 2.' Influence' of' assemblage' species' richness' on' diversity' metrics.' Boxplots!
represent!R2!of!the!linear!regressions!between!ses.!PDFaith!and!ses.MPD,!and!between!ses.!
PDFaith! and! ses.MNTD! for! 10! sets! of! simulated! assemblages! that! differ! in! species! richness!
(SR):!!from!10!to!30!species!for!the!first!set,!30!to!50!for!the!second,!and!so!on,!until!170!to!
190!species!for!the!last!set.!For!each!of!these!sets,!we!computed!the!standard!effect!size!of!
each! metric! and! the! R2! of! the! linear! relationship! between! the! metrics.! We! repeated! the!
whole!procedure!100!times!to!obtain!a!distribution!of!R2!for!each!level!of!SR.!! !
! "!102!"!
Ses.MNTD)(+NTI))Vs.)Ses.PD) Ses.MPD)(+NRI))Vs.)Ses.PD)
60%#
R2#=#0.59# R2#=#0.36#
4%# 16%#
70%#
13%# 12%#
11%#
13%#
Mntd#or#Mpd#AND#Pd#####
Congruences#
Significant) Nothing# # ##
clustering)?) Only#Mntd#or#Mpd#
Mismatches#
Only#Pd# # ##
!
Figure'3.'Phylogenetic'structure'of'carnivoran'assemblages.'The!top!graphs!represent!
the! relationships! between! ses.PDFaith! and! ses.MPD! or! ses.MNTD! together! with! the! R2! of!
their! linear! relationship.! The! proportion! of! congruence! and! divergence! are! also!
represented! in! four! groups:! whether! PDFaith! and! MPD! (or! MNTD)! show! congruent!
(significant/non"significant! clustering:! dark! and! light! brown! dots,! respectively)! or!
diverging!results!(only!significant!PDFaith!/!only!significant!MPD!(or!MNTD);!blue!and!red!
dots,! respectively).! Bottom! graphs! show! the! spatial! structure! of! these! four! types! of!
assemblages.!! !
! "!103!"!
R2=0.96( R2=0.19(
Figure'4.'Mammalian'guts'phylogenetic'structure.!Raw!relationship!between!ses.PDFaith!
(Y"axis)! and! ses.MPD/ses.MNTD! (X"axis)! across! 33! mammalian! gut! assemblages.! Host!
orders!are!represented!by!different!colours!(see!legend).!The!R2!of!linear!models!between!
metrics!are!reported!on!each!graph.!
! "!104!"!
References' Muegge,! B.! D.! et! al.! 2011.! Diet! drives! convergence! in! gut!
Araújo,!M.!and!Rozenfeld,!A.!2014.!The!geographic!scaling!of!biotic! microbiome! functions! across! mammalian! phylogeny! and!
interactions.!"!Ecography!(Cop.).!37:!406–415.! within!humans.!"!Science!332:!970–4.!
Bryant,! J.! A.! et! al.! 2008.! Microbes! on! mountainsides:! contrasting! Nyakatura,! K.! and! Bininda"Emonds,! O.! R.! P.! 2012.! Updating! the!
elevational!patterns!of!bacterial!and!plant!diversity.!"!Proc.! evolutionary! history! of! Carnivora! (Mammalia):! a! new!
Natl.!Acad.!Sci.!U.!S.!A.!105:!11505–11.! species"level! supertree! complete! with! divergence! time!
Cadotte,! M.! W.! et! al.! 2008.! Evolutionary! history! and! the! effect! of! estimates.!"!BMC!Biol.!10:!12.!
biodiversity!on!plant!productivity.!"!Proc.!Natl.!Acad.!Sci.!U.! O’Dwyer,! J.! et! al.! 2012.! Phylogenetic! diversity! theory! sheds! light!
S.!A.!105:!17012–7.! on!the!structure!of!microbial!communities.!"!PLoS!Comput.!
Chao,!A.!et!al.!2010.!Phylogenetic!diversity!measures!based!on!Hill! Biol.!8:!e1002832.!
numbers.!"!Philos.!Trans.!R.!Soc.!London,!Ser.!B!365:!3599– O’Meara,! B.! 2012.! Evolutionary! inferences! from! phylogenies:! a!
3609.! review! of! methods.! "! Annu.! Rev.! Ecol.! Evol.! Syst.! 43:! 267–
Colless,!D.!1982.!Review!of!phylogenetics:!the!theory!and!practice! 285.!
of!phylogenetic!systematics.!"!Syst.!Zool.!31:!100–104.! Pavoine,! S.! and! Bonsall,! M.! B.! 2011.! Measuring! biodiversity! to!
Davies,! T.! J.! and! Buckley,! L.! B.! 2011.! Phylogenetic! diversity! as! a! explain! community! assembly:! a! unified! approach.! "! Biol.!
window!into!the!evolutionary!and!biogeographic!histories! Rev.!86:!792–812.!
of! present"day! richness! gradients! for! mammals.! "! Philos.! Pedersen,! R.! Ø.! et! al.! 2014.! Macroecological! evidence! for!
Trans.!R.!Soc.!London,!Ser.!B!366:!2414–2425.! competitive! regional"scale! interactions! between! the! two!
Davies,!T.!J.!et!al.!2011.!The!influence!of!past!and!present!climate! major! clades! of! mammal! carnivores! (Feliformia! and!
on!the!biogeography!of!modern!mammal!diversity.!"!Philos.! Caniformia).!(D!Russo,!Ed.).!"!PLoS!One!9:!e100553.!
Trans.!R.!Soc.!London,!Ser.!B!366:!2526–2535.! Pybus,! O.! and! Harvey,! P.! 2000.! Testing! macro–evolutionary!
Dearing,!M.!D.!et!al.!2000.!Diet!breadth!of!mammalian!herbivores:! models!using!incomplete!molecular!phylogenies.!"!Proc.!R.!
nutrient!versus!detoxification!constraints.!"!Oecologia!123:! Soc.!London,!Ser.!B!267:!2267–2272.!
397–405.! R!Development!Core!Team!2014.!R:!A!Language!and!Environment!
Devictor,!V.!et!al.!2010.!Spatial!mismatch!and!congruence!between! for!Statistical!Computing.!
taxonomic,!phylogenetic!and!functional!diversity:!the!need! Redding,! D.! W.! et! al.! 2014.! Measuring! Evolutionary! Isolation! for!
for!integrative!conservation!strategies!in!a!changing!world.! Conservation.!(WJ!Murphy,!Ed.).!"!PLoS!One!9:!e113490.!
"!Ecol.!Lett.!13:!1030–1040.! Ricotta,! C.! 2007.! A! semantic! taxonomy! for! diversity! measures.! "!
Faith,! D.! P.! 1992.! Conservation! evaluation! and! phylogenetic! Acta!Biotheor.!55:!23–33.!
diversity.!"!Biol.!Conserv.!61:!1–10.! Safi,! K.! et! al.! 2011.! Understanding! global! patterns! of! mammalian!
Faith,! D.! P.! 2013.! Biodiversity! and! evolutionary! history:! useful! functional! and! phylogenetic! diversity.! "! Philos.! Trans.! R.!
extensions! of! the! PD! phylogenetic! diversity! assessment! Soc.!London,!Ser.!B!366:!2536–2544.!
framework.!"!Ann.!N.!Y.!Acad.!Sci.!1289:!69–89.! Swenson,! N.! G.! 2011.! Phylogenetic! beta! diversity! metrics,! trait!
Fritz,! S.! and! Rahbek,! C.! 2012.! Global! patterns! of! amphibian! evolution! and! inferring! the! functional! beta! diversity! of!
phylogenetic!diversity.!"!J.!Biogeogr.!38:!1373–1382.! communities.!"!PLoS!One!6:!e21264.!
Hardy,!O.!J.!and!Senterre,!B.!2007.!Characterizing!the!phylogenetic! Tucker,! C.! and! Cadotte,! M.! 2013.! Unifying! measures! of!
structure! of! communities! by! an! additive! partitioning! of! biodiversity:! understanding! when! richness! and!
phylogenetic!diversity.!"!J.!Ecol.!95:!493–506.! phylogenetic! diversity! should! be! congruent.! "! Divers.!
Harmon,! L.! J.! et! al.! 2008.! GEIGER:! investigating! evolutionary! Distrib.!19:!845–854.!
radiations.!"!Bioinformatics!24:!129–31.! Warren,! D.! L.! et! al.! 2014.! Mistaking! geography! for! biology:!
HilleRisLambers,! J.! et! al.! 2012.! Rethinking! Community! Assembly! inferring! processes! from! species! distributions.! "! Trends!
through!the!Lens!of!Coexistence!Theory.!"!Annu.!Rev.!Ecol.! Ecol.!Evol.!29:!572–580.!
Evol.!Syst.!43:!227–248.! Webb,! S.! 2006.! The! great! American! biotic! interchange:! patterns!
Hooper,!L.!V!et!al.!2012.!Interactions!between!the!microbiota!and! and!processes.!"!Ann.!Missouri!Bot.!Gard.:!245–257.!
the!immune!system.!"!Science!336:!1268–73.! Webb,! C.! O.! et! al.! 2002.! Phylogenies! and! Community! Ecology.! "!
Isaac,! N.! J.! B.! et! al.! 2007.! Mammals! on! the! EDGE:! conservation! Annu.!Rev.!Ecol.!Evol.!Syst.!33:!475–505.!
priorities! based! on! threat! and! phylogeny.! "! PLoS! One! 2:! Webb,! C.! O.! et! al.! 2008.! Phylocom:! software! for! the! analysis! of!
e296.! phylogenetic! community! structure! and! trait! evolution.! "!
Johnson,! W.! et! al.! 2006.! The! late! Miocene! radiation! of! modern! Bioinformatics!24:!2098–2100.!
Felidae:!a!genetic!assessment.!"!Science!(80".!).!311:!73–77.! Woodburne,! M.! O.! 2010.! The! Great! American! Biotic! Interchange:!
Kembel,! S.! W.! et! al.! 2010.! Picante:! R! tools! for! integrating! Dispersals,!Tectonics,!Climate,!Sea!Level!and!Holding!Pens.!
phylogenies!and!ecology.!"!Bioinformatics!26:!1463–4.! "!J.!Mamm.!Evol.!17:!245–264.!
Kissling,! W.! et! al.! 2012.! Cenozoic! imprints! on! the! phylogenetic! !
structure! of! palm! species! assemblages! worldwide.! "! Proc.! !
Natl.!Acad.!Sci.!U.!S.!A.!109:!7379–7384.!
Ley,! R.! E.! et! al.! 2008.! Evolution! of! mammals! and! their! gut!
microbes.!"!Science!320:!1647–51.!
Lozupone,! C.! and! Knight,! R.! 2005.! UniFrac:! a! new! phylogenetic!
method! for! comparing! microbial! communities.! "! Appl.!
Environ.!Microbiol.!71:!8228–8235.!
Morlon,!H.!et!al.!2011.!Spatial!patterns!of!phylogenetic!diversity.!"!
Ecol.!Lett.!14:!141–149.!
Mouquet,! N.! et! al.! 2012.! Ecophylogenetics:! advances! and!
perspectives.!"!Biol.!Rev.!87:!769–785.!
! "!105!"!
Partie!I!
! "!106!"!
Partie!I!
! "!107!"!
Partie!I!"!Synthèse!
SYNTHÈSE'ET'DISCUSSION'DE'LA'PARTIE'I'
'
! "!108!"!
Cette!première!partie!de!ma!thèse!visait!à!répondre!à!la!question!suivante!:!
!
!
Peut&on!synthétiser!les!indices!de!diversités!
!le!long!de!grandes!dimensions!structurelles?!
!
!
1.'Synthèse'du'travail'
!
Je! proposai! en! introduction! de! construire! une! classification! des! indices! de!
diversité!phylogénétique!en!commençant!par!différencier!l’unité!de!base!que!les!indices!
utilisent!:!
!
(1) la!paire!de!communautés!(diversité!phylogénétique!β)!
(2) la!communauté!(diversité!phylogénétique!α)!
(3) l’espèce!(originalité!phylogénétique).!
!
Les! chapitres! I! et! II! ainsi! que! l’annexe! 1! montrent! qu’une! carte! simplifiée! de! la!
jungle! des! indices! de! diversité! phylogénétique! existe! et! nous! identifions! des! sentiers!
pour!faciliter!l’exploration!de!la!jungle.!Ces!sentiers!n’ont!pas!été!tracés!à!l’aveugle!mais!
regroupent! des! indices! aux! propriétés! similaires,! c’est"à"dire! mesurant! une! même!
dimension!de!la!diversité!phylogénétique.!J'espère!que!ce!type!de!cartographie!évitera!à!
l’avenir!un!grand!nombre!des!marches!aléatoires!contre"productives!dans!la!jungle!des!
indices!de!diversité.!
!
!
1.1.!Les!indices!de!diversité!au!niveau!des!communautés!!
"
Le!premier!chapitre!se!base!sur!les!trois!dimensions!structurelles!fondamentales!
identifiées!par!Pavoine!&!Bonsall!(2011)!:!la!richesse,!la!divergence!et!la!régularité.!Cette!
grille! de! lecture! nous! permet! de! (1)! jalonner! le! sentier! de! panneaux! d’orientation!
indiquant!l’appartenance!des!indices!à!l’une!ou!l’autre!des!dimensions!et!(2)!de!fournir!
un! manuel! d’orientation! qui! relie! les! questions! de! recherche! des! écologistes! avec! les!
! "!109!"!
dimensions! indiquées! sur! le! sentier.! Le! deuxième! chapitre! est! complémentaire! du!
premier!car!il!identifie!une!dimension!transversale,!applicable!à!chacune!des!dimensions!
proposées!:!c’est!l’échelle!phylogénétique!avec!laquelle!les!structures!sont!mesurées.!Par!
exemple,! nous! montrons! que! la! PDFaith! quantifie! en! fait! une! structure! phylogénétique!
«"terminale"»!(c’est!à!dire!près!des!feuilles!de!l’arbre)!et!que,!lorsqu’il!est!utilisé!tout!seul!
il! ne! renseigne! pas! sur! la! structure! phylogénétique! profonde! des! assemblages.!
Finalement,! nous! pouvons! résumer! ces! deux! chapitres! en! trois! groupes!
d’axes!orthogonaux!:"
!
(1) l’échelle!phylogénétique!ou!fonctionnelle!considérée!
(2) la!dimension!structurale!considérée!(richesse,!divergence,!régularité)!
(3) l’intégration!des!abondances!(locales,!régionales!ou!mondiales).!
!
En!définitive,!nous!avons!montré!dans!ces!deux!premiers!chapitres!comment!les!
indices!de!diversité!phylogénétique!pouvaient!être!classés!de!façon!rigoureuse.!Il!nous!
manque! cependant! la! «!diversité!»! d’une! identité! biologique!:! l’originalité! des! espèces.!
Ceci!fait!l’objet!de!l’annexe!1.3,!résumé!ci"dessous.!!
!
1.2.!Les!indices!d’originalité!phylogénétique!des!espèces!
!
L’annexe!1.3!est!le!fruit!d’une!collaboration!avec!David!Redding!et!Arne!Mooers,!
que!j’ai!rencontrés!au!workshop!sur!la!diversité!phylogénétique!à!Leipzig.!L’étude!était!
déjà!largement!avancée!(notamment!les!simulations)!lorsque!j’ai!été!associé!au!projet!et!
ma!contribution!a!donc!été!limitée!(corrections!des!formules!des!indices,!liens!avec!les!
diversités!des!communautés,!correction!du!manuscrit).!!
Dans! cette! analyse,! nous! montrons! que! les! indices! d’originalité! phylogénétique!
s’étalent! en! fait! sur! une! échelle! phylogénétique.! Du! côté! «!récent!»! du! spectre,! l’indice!
phare!représente!l’âge!de!l’espèce!(c’est"à"dire!l’âge!de!l’ancêtre!commun!à!l’espèce!et!à!
son!espèce!sœur,!le!«!pendant!edge!»,!PE)!alors!que!du!côté!«!interne!»!!du!spectre,!on!
retrouve!la!distance!moyenne!de!l’espèce!à!toutes!les!autres!espèces!de!l’arbre.!Ainsi,!on!
s’aperçoit!que!l’échelle!phylogénétique!est!une!caractéristique!fondamentale!de!tous!les!
indices! proposés! dans! la! littérature! et! permet! de! tester! des! hypothèses! écologiques!
différentes.!!
! "!110!"!
!
2.'Utilité'de'l’approche'
!
Cette! carte! des! sentiers,! accompagnée! de! son! manuel! d’orientation,! devrait!
permettre! aux! chercheurs! de! ne! plus! se! perdre! dans! la! jungle! et! donc! de! choisir! un!
indice!pour!quantifier!une!facette!de!la!structure!phylogénétique!d’un!assemblage!ou!de!
l’originalité! d’une! espèce.! Une! fois! choisi,! l’indice! peut! être! utilisé! directement,! par!
exemple!dans!le!cas!des!communautés:!
!
(1) en!le!reliant!à!des!caractéristiques!environnementales!ou!taxonomiques!dans!le!
cadre! d’une! recherche! fondamentale! (Cadotte! et! al.! 2008,! Safi! et! al.! 2011,!
Belmaker!and!Jetz!2015)!
(2) en!maximisant!sa!valeur!dans!le!cadre!de!la!conservation!(Rodrigues!and!Gaston!
2002,!Rodrigues!et!al.!2011,!Pollock!et!al.!2015).!
!
Dans!le!cadre!des!originalités!phylogénétiques,!on!peut!notamment!y!voir!un!outil!
intéressant!en!biologie!des!invasions!(Thuiller!et!al.!2010)!puisqu’il!permet!de!quantifier!
l’originalité!d’une!espèce!invasive!à!la!communauté!résidente.!!
!
3.'Limites'et'perspectives'du'travail'
!
3.1.!Lien!avec!la!diversité!fonctionnelle!
!
Le! travail! de! synthèse! effectué! se! concentre! sur! les! mesures! de! diversité!
phylogénétiques.!Il!est!cependant!important!de!faire!le!lien!avec!les!indices!de!diversités!
fonctionnelles! car! les! deux! approches! sont! souvent! complémentaires.! En! ce! sens,! ils!
permettent! un! rapprochement! entre! les! facettes! fonctionnelles! et! phylogénétiques! et!
donc! un! rapprochement! de! la! biogéographie! évolutive! et! de! la! biogéographie!
fonctionnelle.!!
Nous!avons!constamment!proposé!de!faire!le!lien,!particulièrement!dans!l’article!
1!et!l’annexe!1.3,!entre!indices!phylogénétiques!et!indices!fonctionnels.!Ainsi,!la!carte!de!
classification! que! nous! proposons! pour! les! indices! de! l’article! 1! est! aisément!
transposable! à! l’univers! fonctionnel.! Dans! le! cas! le! plus! simple,! les! dissimilarités!
! "!111!"!
fonctionnelles! sont! représentées! sous! forme! de! dendrogramme! (Petchey! and! Gaston!
2007)! et! dans! ce! cas,! tous! les! indices! de! diversités! phylogénétiques! ont! un! équivalent!
fonctionnel,! qui! d’ailleurs! ont,! dans! certains! cas,! un! nom! (malheureusement)! différent.!
Par!exemple,!l’équivalent!de!PDFaith!en!fonctionnel!est!un!indice!très!utilisé,!il!s’agit!de!la!
FD! sensu! Petchey! &! Gaston! (2007).! Même! dans! les! cas! où! les! distances! fonctionnelles!
entre! espèces! ne! sont! pas! représentées! sous! forme! de! dendrograme,! les! liens! entre!
indices! sont! criants!:! le! MPD! ou! l’entropie! quadratique! de! Rao! sont! utilisables! autant!
dans!un!espace!fonctionnel!que!phylogénétique.!!
!
3.2.! Proposer! une! revue! synthétique! des! indices! d’originalité! phylogénétiques! et!
fonctionnels!
!
Dans!le!cadre!des!originalités!d’espèces,!un!travail!de!synthèse!entre!phylogénie!
et! fonctions! semble! urgent.! En! effet,! on! dénombre! de! très! nombreux! indices! dans! les!
deux!domaines,!mais!aucune!synthèse!ne!permet!d’en!faire!le!lien,!ni!même!de!les!ranger!
dans!des!cases!compréhensibles!et!facilement!utilisables!par!les!écologistes.!Pourtant!les!
parallèles! semblent! clairs! et! je! pense! que! l’on! peut! décomposer,! encore! une! fois,! les!
indices! le! long! (1)! d’une! échelle! phylogénétique! ou! fonctionnelle! et! (2)! d’un! ensemble!
d’espèces!de!référence!et!(3)!d’une!considération!de!l’abondance!de!l’espèce!:!
!
(1) Les!indices!d’originalité!fonctionnelle!s’étalent!eux!aussi!le!long!d’un!continuum!
d’échelle.! Par! exemple,! Buisson! et" al.! (2008)! définissent! «!l’originalité!»! et!
«!l’unicité!»!fonctionnelles!des!espèces!comme!la!distance!moyenne!d’une!espèce!
à!l’ensemble!de!référence!et!la!distance!moyenne!à!l’espèce!la!plus!proche!dans!
l’espace! fonctionnel.! Ces! indices! correspondent! tout! simplement! aux! deux!
extrémités! du! continuum! ! d’originalité! phylogénétique! mais! possèdent! –
!évidemment!"!des!noms!différents,!ce!qui!ne!facilite!pas!une!vision!intégrative.!
!
(2) L’ensemble! d’espèces! de! référence! auquel! une! espèce! donnée! est! comparée!
permet!là!aussi!d’unifier!des!littératures!qui!ne!communiquent!pas!forcément.!!
a. Échelle!locale!de!la!communauté!
Les! indices! d’originalités! à! l’échelle! de! la! communauté! sont! utilisés! en!
biologie! de! l’invasion! pour! comprendre! si! les! caractéristiques! de! la!
! "!112!"!
communauté! résidente! influencent! le! succès! invasif! de! l’espèce! exotique!

(voir! Thuiller! et"al.! 2010! pour! une! synthèse! du! domaine! et! Gallien! et"al.!
2015!pour!une!application,!dont!je!reporte!le!résumé!en!annexe!1.4).!
b. Échelle!plus!large!de!l’aire!de!distribution!de!l’espèce!
C’est! ce! qui! a! été! appelé! les! «!champs! phylogénétiques!»! des! espèces!
(«!phylogenetic! fields!»,! Villalobos! et" al.,! 2013)! et! qui! a! notamment! été!
utilisé! pour! comprendre! la! structure! de! cooccurrence! des! oiseaux!
(Barnagaud!et!al.!2014).!
c. Échelle!regroupant!toutes!les!espèces!d’un!taxon!donné!!
Ceci!correspond!aux!mesures!«!classiques!»!d’originalité.!
!
(3) La!pondération!de!l’originalité!des!espèces!par!leur!rareté!(par!exemple!la!taille!
de! leurs! aires! de! distribution)! est! de! plus! en! plus! employée,! notamment! dans!
une!optique!de!conservation!(Jetz!et!al.!2014).!
!
Je!pense!que!ce!travail!de!synthèse!pourra!clarifier!les!relations!entre!indices!et!
donc!permettre!aux!écologues!de!plus!facilement!choisir!les!indices!en!fonction!de!leur!
question.!!
!
3.3.!Incorporer!l’effet!des!modèles!nuls!
!
Dans!la!synthèse!des!indices!de!diversité!de!communauté!proposée!au!chapitre!I,!
nous!avons!utilisé!la!valeur!brute!des!indices!de!diversité!pour!les!classer.!Cependant,!la!
valeur! des! indices! de! diversités! est! souvent! comparée! à! une! distribution! de! valeurs!
«!nulles!»!qui!dérivent!d’un!modèle!nul!particulier!(Gotelli!and!Colwell!2001,!Gotelli!and!
McGill!2006,!Hardy!2008,!Chalmandrier!et!al.!2013).!Ce!modèle!nul!permet!de!tester!si!
une! structure! de! communauté! est! aléatoire! relativement! à! une! série! d’hypothèses!
précises.! Les! indices! sont! souvent! standardisés! par! la! moyenne! et! l’écart"type! de! la!
distribution! nulle.! Nous! n’avons! pas! intégré! cette! dimension! dans! le! chapitre! I! par!
manque!de!place!et!car!les!indices!peuvent!aussi!s’utiliser!sans!modèles!nuls.!Cependant,!
cette!dimension!est!explorée!dans!le!chapitre!II.!Il!apparaît!que!lorsqu’un!modèle!nul!est!
utilisé,!les!dimensions!mises!à!jour!dans!le!premier!chapitre!sont!moins!apparentes.!En!
effet,! la! PDFaith! considérée! comme! un! indice! de! richesse! phylogénétique! se! trouve! très!
! "!113!"!
proche!du!MNTD,!un!indice!de!divergence!phylogénétique!(voir!le!chapitre!II).!Je!pense!
que! cette! différence! apparente! ne! diminue! pas! l’intérêt! de! mon! premier! chapitre! car!
l’utilisation! des! modèles! nuls! n’est! pas! systématique,! notamment! en! conservation.! Par!
ailleurs,! il! faudrait! probablement! explorer! le! comportement! des! indices! bruts! et!
standardisés! par! le! modèle! nul! de! façon! systématique,! ce! qui! pourra! faire! l’objet!
d’études!futures.!!
!
4.!Transition!
!
La!seconde!et!la!troisième!partie!de!ma!thèse!s’attachent!à!utiliser!quelques!unes!
de!ces!avancées!conceptuelles!en!!biogéographie!de!la!conservation!et!en!biogéographie!
fondamentale.!En!particulier,!la!partie!II!s’intéresse!à!la!richesse!phylogénétique!et!à!sa!
congruence! avec! la! richesse! taxonomique.! Je! propose! aussi! de! comparer! différentes!
dimensions!(richesse!et!divergence)!pour!construire!des!points!chauds!(«!hotspots!»)!de!
biodiversité.! Finalement,! la! troisième! partie! est! bâtie! sur! l’utilisation! de! l’échelle!
phylogénétique.!En!effet,!nous!montrons!dans!ces!trois!premières!analyses!l’importance!
de! l’échelle! phylogénétique! pour! décrire! et! comprendre! la! structure! des! entités!
biologiques.!J’utilise!cette!démarche!pour!distinguer!l’effet!de!différents!processus!dans!
l’assemblage!de!communautés.!!
!
! "!114!"!
Partie!I!"!Bibliographie!
BIBLIOGRAPHIE'GÉNÉRALE'
DE'LA'PARTIE'I''
(HORS'ARTICLES)
! "!115!"!
Partie!I!"!Bibliographie!
Barnagaud,! J."Y.! et! al.! 2014.! Ecological! traits! influence! the! phylogenetic! structure! of! bird! species! co"
occurrences!worldwide.!(D!Mouillot,!Ed.).!"!Ecol.!Lett.!17:!811–20.!
Belmaker,!J.!and!Jetz,!W.!2015.!Relative!roles!of!ecological!and!energetic!constraints,!diversification!rates!
and!region!history!on!global!species!richness!gradients!(H!Arita,!Ed.).!"!Ecol.!Lett.!18:!563–571.!
Buisson,!L.!E.!T.!et!al.!2008.!Climate!change!hastens!the!turnover!of!stream!fish!assemblages.!"!Glob.!Chang.!
Biol.!14:!2232–2248.!
Buisson,!L.!et!al.!2010.!Uncertainty!in!ensemble!forecasting!of!species!distribution.!"!Glob.!Chang.!Biol.!16:!
1145–1157.!
Cadotte,!M.!W.!et!al.!2008.!Evolutionary!history!and!the!effect!of!biodiversity!on!plant!productivity.!"!Proc.!
Natl.!Acad.!Sci.!U.!S.!A.!105:!17012–7.!
Chalmandrier,! L.! et! al.! 2013.! A! family! of! null! models! to! distinguish! between! environmental! filtering! and!
biotic! interactions! in! functional! diversity! patterns.! "! J.! Veg.! Sci.!! Off.! organ! Int.! Assoc.! Veg.! Sci.! 24:!
853–864.!
Díaz,! S.! et! al.! 2007.! Incorporating! plant! functional! diversity! effects! in! ecosystem! service! assessments.! "!
Faith,!D.!P.!1992.!Conservation!evaluation!and!phylogenetic!diversity.!"!Biol.!Conserv.!61:!1–10.!
Gallien,!L.!et!al.!2015.!Contrasting!the!effects!of!environment,!dispersal!and!biotic!interactions!to!explain!
the!distribution!of!invasive!plants!in!alpine!communities.!"!Biol.!Invasions!17:!1407–1423.!
Gotelli,!N.!and!Colwell,!R.!2001.!Quantifying!biodiversity:!procedures!and!pitfalls!in!the!measurement!and!
comparison!of!species!richness.!"!Ecol.!Lett.!4(4), 379-391.!
Gotelli,!N.!and!McGill,!B.!2006.!Null!versus!neutral!models:!what’s!the!difference?!"!Ecography!(Cop.).!29:!
793–800.!
Graham,! C.! H.! and! Fine,! P.! V.! A.! 2008.! Phylogenetic! beta! diversity:! linking! ecological! and! evolutionary!
processes!across!space!in!time.!"!Ecol.!Lett.!11:!1265–77.!
Hardy,!O.!2008.!Testing!the!spatial!phylogenetic!structure!of!local!communities:!statistical!performances!
of!different!null!models!and!test!statistics!on!a!locally!neutral!community.!"!J.!Ecol.!96:!914–926.!
Isaac,!N.!J.!B.!et!al.!2007.!Mammals!on!the!EDGE:!conservation!priorities!based!on!threat!and!phylogeny.!"!
PLoS!One!2:!e296.!
Jetz,!W.!et!al.!2014.!Global!distribution!and!conservation!of!evolutionary!distinctness!in!birds.!"!Curr.!Biol.!
24:!919–30.!
Mouquet,!N.!et!al.!2012.!Ecophylogenetics:!advances!and!perspectives.!"!Biol.!Rev.!87:!769–785.!
Pavoine,! S.! and! Bonsall,! M.! B.! 2011.! Measuring! biodiversity! to! explain! community! assembly:! a! unified!
approach.!"!Biol.!Rev.!86:!792–812.!
Petchey,!O.!L.!and!Gaston,!K.!J.!2007.!Dendrograms!and!measuring!functional!diversity.!"!Oikos!116:!1422–
1426.!
Pollock,! L.! J.! et! al.! 2015.! Phylogenetic! diversity! meets! conservation! policy:! small! areas! are! key! to!
preserving!eucalypt!lineages.!"!Philos.!Trans.!R.!Soc.!Lond.!B.!Biol.!Sci.!370:!20140007.!
Rodrigues,!A.!S.!L.!and!Gaston,!K.!J.!2002.!Maximising!phylogenetic!diversity!in!the!selection!of!networks!of!
conservation!areas.!"!Biol.!Conserv.!105:!103–111.!
Rodrigues,!A.!S.!L.!et!al.!2011.!Complete,!accurate,!mammalian!phylogenies!aid!conservation!planning,!but!
not!much.!"!Philos.!Trans.!R.!Soc.!London,!Ser.!B!366:!2652–2660.!
Safi,!K.!et!al.!2011.!Understanding!global!patterns!of!mammalian!functional!and!phylogenetic!diversity.!"!
Philos.!Trans.!R.!Soc.!London,!Ser.!B!366:!2536–2544.!
Srivastava,!D.!and!Cadotte,!M.!2012.!Phylogenetic!diversity!and!the!functioning!of!ecosystems.!"!Ecol.!!Lett.!
15(7), 637-648.!
Swenson,!N.!G.!2011.!Phylogenetic!beta!diversity!metrics,!trait!evolution!and!inferring!the!functional!beta!
diversity!of!communities.!"!PLoS!One!6:!e21264.!
Thuiller,! W.! et! al.! 2010.! Resolving! Darwin’s! naturalization! conundrum:! a! quest! for! evidence.! "! Divers.!
Distrib.!16:!461–475.!
Villalobos,! F.! et! al.! 2013.! Phylogenetic! fields! of! species :! cross"species! patterns! of! phylogenetic! structure!
and!geographical!coexistence!Phylogenetic!fields!of!species :!cross"species!patterns!of!phylogenetic!
structure!and!geographical!coexistence.!Proc. R Soc Lond B: 280(1756), 20122570.!
Webb,!C.!O.!et!al.!2002.!Phylogenies!and!Community!Ecology.!"!Annu.!Rev.!Ecol.!Evol.!Syst.!33:!475–505.!
Whittaker,! R.! 1960.! Vegetation! of! the! Siskiyou! mountains,! Oregon! and! California.! "! Ecol.! Monogr. 30(3),
279-338.!
Winter,!M.!et!al.!2012.!Phylogenetic!diversity!and!nature!conservation:!where!are!we?!"!Trends!Ecol.!Evol.!
28:!199–204.!
!
! "!116!"!
!
! "!117!"!
Partie!II!
PARTIE'II''
'
UTILISER'LES''
DIVERSITÉS'PHYLOGÉNÉTIQUES'ET'
FONCTIONNELLES'EN'CONSERVATION'
'
'
! "!118!"!
Partie!II!"!Sommaire!
SOMMAIRE'DE'LA'PARTIE'II'
'
!
Articles'associés'à'la'partie'II' ' ' ' ' ' ' ' 120'
Annexes'associées'à'la'partie'II' ' ' ' ' ' ' ' 120'
'
INTRODUCTION.'État'de'l’art' ' ' ' ' ' ' ' 121'
1.Contexte! ! ! ! ! ! ! ! ! ! ! 122'
2.!La!biologie!de!la!conservation!! ! ! ! ! ! ! ! 122'
3.!L’apport!potentiel!des!facettes!fonctionnelles!et!phylogénétiques! ! ! 124'
4.!Synthèse!!et!stratégie!de!travail! ! ! ! ! ! ! ! 125'
'
CHAPITRE'III.'Quantification'de'l’érosion'de'la'diversité'phylogénétique' 128'
Résumé! ! ! ! ! ! ! ! ! ! ! 129!
Article!! ! ! ! ! ! ! ! ! ! ! 130!
!
CHAPITRE'IV.'Les'points'chauds'de'diversité'fonctionnelle''
et'phylogénétique' ' ' ' ' ' ' ' ' ' 140'
Résumé! ! ! ! ! ! ! ! ! ! ! 141!
Article!! ! ! ! ! ! ! ! ! ! ! 142!
!
SYNTHÈSE'&'DISCUSSION' ' ' ' ' ' ' ' 155'
1.!Évaluer!les!menaces! ! ! ! ! ! ! ! ! 156!
2.!La!protections!des!différentes!facettes! ! ! ! ! ! ! 158'
3.!Perspectives! ! ! ! ! ! ! ! ! ! 162'
'
BIBLIOGRAPHIE' ' ' ' ' ' ' ' ' ' 164'
! "!119!"!
Partie!II!"!Contributions!
ARTICLES'ASSOCIÉS'À'LA'PARTIE'II'
'
ARTICLE!4!!
!
Mazel,'F.,!Renaud,!J.,!Guilhaumon,!F.,!Mouillot,!D.,!Gravel!D.,!&!Thuiller,!W.!Mammalian!
phylogenetic!diversity!area!relationships!at!a!continental!scale,!2015.!
Ecology,!96!(10),!2814"2823.!
!
!
ARTICLE!5!!
!
Mazel,'F.,!Guilhaumon,!F.,!Mouquet,!N.,!Devictor,!V.,!Gravel,!D.,!Renaud,!J.,!Cianciaruso,!
M.V.,!Loyola,!R.D.,!Diniz"Filho,!J.A.F.,!Mouillot,!D.!&!Thuiller,!W.!(2014)!Multifaceted!
diversity"area!relationships!reveal!global!hotspots!of!mammalian!species,!trait!and!
lineage!diversity,!2014.!
Global!Ecology!and!Biogeography,!23,!836–847.!
!
!
ARTICLE!6!!
!
Thuiller,!W.,!Maiorano,!L.,!Mazel,'F.,!Guilhaumon,!F.,!Ficetola,!G.F.,!Lavergne,!S.,!Renaud,!
J.,!Roquet,!C.!and!Mouillot,!D.!2015.!Conserving!the!functional!and!phylogenetic!trees!of!
life!of!European!tetrapods,!2014.!
Philosophical!Transactions!of!the!Royal!Society!of!London!B:!Biological!Sciences,!
370(1662).'
!
!
!
ANNEXES'ASSOCIÉES'À'LA'PARTIE'II'
!
ANNEXE!2.3.!Article!6!
! "!120!"!
Partie!II!"!Introduction!
INTRODUCTION'DE'LA'PARTIE'II'
'
! "!121!"!
1.'Contexte''
!
Il!est!aujourd’hui!largement!admis!que!les!activités!humaines!menacent!l’avenir!
de!la!biodiversité!(Pimm!et!al.!1995,!Pimm!and!Raven!2000,!Ceballos!and!Ehrlich!2002,!
Brook!et!al.!2003,!Barnosky!et!al.!2011,!2012,!De!Vos!et!al.!2015).!Ces!menaces!sont!de!
différentes! natures! (appropriation! des! ressources,! fragmentation! des! habitats,!
introduction! d’espèces! exotiques,! déplacement! de! pathogènes,! destruction! directe! des!
espèces,!changements!climatiques)!et!ont!pour!conséquences!le!déclin!des!populations,!
la!modification!du!fonctionnement!des!écosystèmes!et!l’extinction!accélérée!des!espèces!
par!rapport!aux!taux!«!normaux!»!(c’est"à"dire!mesurés!sur!des!temps!géologiques).!!
La!prise!de!conscience!de!telles!menaces!n’est!en!fait!pas!nouvelle!et!date!de!la!fin!
du!XIXe!siècle!(Jepson!and!Whittaker!2002).!Elle!s’est!accompagnée!de!la!naissance!d’un!
mouvement! de! conservation! de! la! nature,! surtout! dans! les! élites! occidentales! dans! un!
premier!temps,!puis!de!toute!la!société!à!partir!des!années!50!et!les!décennies!suivantes!
(à!titre!d’exemple!Greenpeace!et!WWF!sont!fondés!en!1961!et!1971,!respectivement).!Ce!
mouvement! a! été! ensuite! rejoint! par! les! scientifiques! dont! l’expertise! était! vitale! pour!
(1)! prédire! l’impact! des! menaces! et! (2)! protéger! les! espèces! le! plus! efficacement!
possible.!!
!
2.'La'biologie'de'la'conservation'
!
La! biologie! de! la! conservation! en! tant! que! discipline! scientifique! prend! ses!
racines!dans!les!années!50!et!propose!de!décrire!ces!changements,!en!comprendre!les!
mécanismes!pour!éventuellement!les!limiter!et!ainsi!préserver!cette!biodiversité!(Soulé!
1985,!Whittaker!et!al.!2005).!!
!
2.1.'Les'motivations'
'
Les!motivations!de!cette!préservation!peuvent!être!d’ordre!éthique!(c’est"à"dire!
que!l’espèce!humaine!a!un!devoir!moral!de!protéger!les!autres!êtres!vivants)!ou!d’ordre!
utilitariste! (Ladle! and! Whittaker! 2011).! En! effet! les! écosystèmes! sont! de! plus! en! plus!
considérés!comme!des!fournisseurs!de!«!services!»!pour!l’espèce!humaine.!Ces!services!
des!écosystèmes!peuvent!être!des!services!de!régulation!(régulation!de!l’eau,!du!climat,!
! "!122!"!
des! nutriments,! pollinisation,! formation! et! rétention! des! sols,! etc.)! de! production!
(nourriture,!bois,!ressources!médicales,!ornementales!et!génétiques,!etc.)!ou!de!«!bien"
être!»!(valeur!esthétique,!culturelle,!historique)!(de!Groot!et!al.!2002).!Dans!l’économie!
actuelle,! on! tente! alors! d’assigner! une! valeur! monétaire! aux! services! des! écosystèmes!
afin!de!pouvoir!les!intégrer!au!marché!(par!exemple,!voir!Costanza!et!al.!1997).!!!
!
2.2.'Les'approches'
'
On! distingue! en! général! deux! approches! en! biologie! de! la! conservation!:!
l’approche! fonctionnelle! et! l’approche! compositionnelle! (Callicott! et! al.! 1999).!
L’approche! fonctionnelle! privilégie! plutôt! les! propriétés! générales! des! écosystèmes!
comme! la! taille! des! compartiments! et! les! flux! de! matières! alors! que! l’approche!
compositionnelle! se! concentre! davantage! sur! les! entités! biologiques! comme! les!
individus!ou!les!espèces.!Les!deux!approches!ont!leurs!avantages!et!leurs!inconvénients!
et!il!est!donc!généralement!admis!qu’elles!sont!toutes!les!deux!importantes!(Ladle!and!
Whittaker!2011).!!
Dans! le! cadre! de! l’approche! compositionnelle,! l’entité! biologique! de! choix! à!
préserver! est! traditionnellement! l’espèce! (Matthews! et! al.! 2001)! et/ou! la! richesse!
taxonomique!(c’est"à"dire!le!nombre!d’espèces,!Rodrigues!et!al.!2000)!),!et!les!choix!sont!
très! souvent! dictés! par! des! critères! patrimoniaux.! En! particulier,! les! espèces! rares!
localement! ou! endémiques! (c’est"à"dire! dont! l’aire! de! distribution! est! restreinte! à! la!
zone! d’étude)! ont! souvent! un! poids! plus! important! dans! les! plans! de! conservation.! Un!
des! outils! importants! de! la! biologie! de! la! conservation! est! d’aménager! des! aires! de!
protection! des! espèces! où! elles! seront! moins! menacées.! Le! choix! de! l’emplacement! de!
telles!zones!se!base!sur!quatre!critères.!Il!s’agit!d’élaborer!un!projet!flexible!socialement!
et! viable! économiquement! pour! protéger! un! échantillon! représentatif! de! l’ensemble!
biologique!qui!sera!capable!de!se!maintenir!à!plus!ou!moins!long!terme.!!La!planification!
systématique! de! la! conservation! («!systematic! conservation! planning!»,! SCP)! est! une!
discipline! récente! (Margules! and! Pressey! 2000)! qui! propose! des! outils! quantitatifs! et!
transparents! pour! réaliser! ces! objectifs.! Par! exemple,! l’approche! dites! en! «!cœur! de!
zone!»! («!Core! Area!»! in! Zonation,! Moilanen! et! al.! 2009)! permet! de! sélectionner! un!
ensemble!optimal!de!zones!à!protéger,!en!donnant!un!poids!plus!important!aux!espèces!
qui!ont!une!aire!de!distribution!réduite.!!
! "!123!"!
L’approche! fonctionnelle! privilégie! plutôt! les! propriétés! fonctionnelles! des!

écosystèmes! comme! la! taille! des! compartiments! de! matières! et! les! flux! entre! ces!
compartiments! (par! exemple! stock! et! flux! de! carbone,! respectivement).! Ce!
fonctionnement! est! souvent! vital! pour! préserver! les! services! que! fournissent! les!
écosystèmes!aux!sociétés!humaines!(Loreau!2010,!Cardinale!et!al.!2012).!Il!s’agit!donc!
de! prédire! les! conséquences! des! changements! globaux! sur! le! fonctionnement! et! les!
services! des! écosystèmes! et! éventuellement! d’en! restaurer! certaines! composantes!
(Ladle!and!Whittaker!2011).!!
'
'
3.'L’apport'potentiel'des'facettes'fonctionnelles'et'phylogénétiques'
'
3.1.'La'diversité'fonctionnelle''
'
Il!est!maintenant!bien!établi!que!ce!sont!les!traits!fonctionnels!des!individus!qui!
assurent! le! rôle! de! l’espèce! dans! l’écosystème! et! donc! à! terme! son! impact! sur! le!
fonctionnement! et! ses! services! (Díaz! et! al.! 2007,! Lavorel! et! al.! 2011).! En! effet,! la!
diversité! fonctionnelle! apparaît! souvent! comme! un! meilleur! prédicteur! du!
fonctionnement! des! écosystèmes! que! la! richesse! spécifique! (Dı́az' and' Cabido' 2001,'
Petchey! and! Gaston! 2006,! Díaz! et! al.! 2007,! Mouillot! and! Villéger! 2011,! Paquette! and!
Messier!2011,!Lavorel!et!al.!2011).!Il!semble!donc!que!la!perte!d’une!espèce!unique!et!
importante! fonctionnellement! puisse! avoir! des! conséquences! plus! importantes! sur! le!
fonctionnement! de! l’écosystème! que! la! perte! d’une! espèce! redondante! (Mouillot! et! al.!
2013,!2014).!Ainsi,!la!préservation!d’une!telle!facette!pourrait!représenter!une!manière!
efficace!de!conserver!le!fonctionnement!d’un!écosystème.!
!
!
3.2.'La'diversité'phylogénétique'
!
L’importance! de! l’utilisation! de! la! diversité! phylogénétique! en! conservation! est!
reconnue!depuis!longtemps!(Vane"Wright!et!al.!1991,!Faith!1992)!et!a!été!réaffirmée!à!
de!nombreuses!reprises!(Rodrigues!and!Gaston!2002,!Forest!et!al.!2007,!Thuiller!et!al.!
2011,! Pollock! et! al.! 2015).! Cependant,! son! utilisation! dans! la! pratique! reste!
! "!124!"!
extrêmement!limitée!(Winter!et!al.!2012)!mis!à!part!la!mise!en!place!du!projet!‘Edge!of!
Existence’! (EDGE;! Isaac! et! al.! 2007)! qui! se! focalise! sur! la! conservation! des! espèces!
distinctes! évolutivement! et! globalement! en! danger!
d’extinction!(http://www.edgeofexistence.org/).! Pourtant! la! diversité! phylogénétique!
semble!avoir!plusieurs!avantages!en!conservation.!!
Tout! d’abord,! si! les! traits! sont! conservés! le! long! de! la! phylogénie,! la! diversité!
phylogénétique!pourrait!être!un!proxy!intéressant!du!fonctionnement!des!écosystèmes.!
Ceci! a! été! montré! dans! certains! cas,! notamment! pour! la! productivité! (Cadotte! et! al.!
2008,! 2009)! et! il! apparaît! que! l’utilisation! conjointe! de! la! diversité! phylogénétique! et!
fonctionnelle! soit! prometteuse! en! ce! sens! (Flynn! et! al.! 2011,! Srivastava! and! Cadotte!
2012,!Cardinale!et!al.!2012).!Cependant,!ces!expériences!sont!relativement!restreintes!et!
des! évidences! empiriques! plus! robustes! sont! nécessaires! pour! prouver! le! lien! entre!
diversité!phylogénétique!et!fonctionnement.!Ceci!a!fait!dire!à!certains!auteurs!que,!dans!
l’état!actuel!des!connaissances,!l’intérêt!de!l’utilisation!de!la!diversité!phylogénétique!en!
conservation! serait! limité! (Winter! et! al.! 2012).! C’est! oublier! un! aspect! fondamental! de!
l’information! portée! par! cette! facette!:! l’histoire! (Rosauer! and! Mooers! 2013).! En! effet,!
au"delà! de! l’intérêt! utilitariste! des! services! des! écosystèmes,! préserver! une! histoire!
unique! revêt! une! dimension! éthique! fondamentale! (Vane"Wright! et! al.! 1991,! Rosauer!
and! Mooers! 2013).! En! ce! sens,! la! diversité! phylogénétique! est! une! composante!
fondamentale!de!la!biodiversité!et!doit!donc!participer!à!l’objectif!de!représentativité.!!
!
4.'Synthèse'et'stratégie'de'travail'
!
En! définitive,! il! s’agit,! selon! Lecointre! (2011),! de! préserver! les! espèces! pour! ce!
qu’elles! font! (=approche! fonctionnelle)! et! pour! ce! qu’elles! sont! (=approche!
phylogénétique).!Dans!un!premier!temps,!je!vais!tenter!de!comprendre!les!conséquences!
des!changements!globaux!sur!certaines!facettes!encore!mal!explorées!de!la!biodiversité.!
Le!chapitre!III!tente!ainsi!de!quantifier!l’érosion!de!la!diversité!phylogénétique!avec!la!
perte! d’habitat! à! une! échelle! mondiale.! La! prédiction! de! la! perte! de! diversité! n’est!
cependant!que!le!premier!pas!vers!la!protection!de!cette!diversité!à!plusieurs!facettes.!Il!
est! alors! alarmant! de! voir! que! certaines! analyses! commencent! à! montrer! que! les!
différentes!facettes!de!la!biodiversité!ne!sont!pas!interchangeables!ou!«!congruentes!»,!
c’est"à"dire! qu’en! en! préservant! une,! on! ne! garantit! pas! forcément! la! protection! des!
! "!125!"!
autres!(p.!ex.!Devictor!et!al.!2010).!Le!deuxième!chapitre!(chapitre!IV)!de!cette!deuxième!
partie!vise!donc!à!vérifier!ce!résultat!à!une!échelle!mondiale!(Devictor!et!al.!se!focalisent!
à! l’échelle! d’un! seul! pays)! en! utilisant! les! mammifères! comme! exemple.! Finalement,!
l’annexe! 2.3! teste! si! les! aires! de! protection! actuelles! protègent! efficacement! ou! non! la!
diversité!phylogénétique!et!fonctionnelle!des!tétrapodes!en!Europe.!!
'
! "!126!"!
!
! "!127!"!
Partie!II!–!Chapitre!III!
CHAPITRE'III'
'
'
QUANTIFICATION'DE'L’ÉROSION'DE'LA''
DIVERSITÉ'PHYLOGÉNÉTIQUE'DES'MAMMIFÈRES'
'À'L’ÉCHELLE'DU'GLOBE'SUITE'À'LA'PERTE'D’HABITAT'
! !
! "!128!"!
Partie!II!–!Chapitre!III!
Ce!chapitre!pose!la!question!suivante!:!!
!
La#diversité#phylogénétique#est5elle#plus#ou#moins#robuste#que#la#richesse#spécifique#
à#la#perte#d’habitat#?#
#
#
Résumé#de#l’article#
!
De! la! même! façon! que! la! relation! aire"espèce! (SAR! pour! «!species! area!
relationship!»),! la! relation! aire"diversité! phylogénétique! (PDAR! pour! «!phylogenetic!
diversity! area! relationship!»)! décrit! la! tendance! de! la! diversité! phylogénétique! à!
augmenter!avec!l’aire!d’échantillonnage.!La!recherche!sur!les!PDARs!pourrait!permettre!
de! mieux! comprendre! les! processus! influençant! l’assemblage! d’espèces! à! différentes!
échelles!spatiales!et!de!prédire!la!perte!de!diversité!phylogénétique!(PD!pour!‘diversité!
phylogénétique’)!des!suites!de!la!perte!d’habitat.!Cependant!ces!PDARS!sont!encore!très!
peu!étudiés.!Étudier!la!PD!a!de!nombreux!avantages!par!rapport!à!la!richesse!spécifique!
(SR! pour! ‘species! richness’)! puisque! la! PD! nous! renseigne! sur! des! processus! comme!
l’extinction! et! la! spéciation,! les! règles! d’assemblage! et! le! fonctionnement! des!
écosystèmes.! Dans! cette! analyse,! nous! étudions! l’universalité! de! la! forme! des! PDARs! à!
une! échelle! continentale! en! utilisant! les! mammifères! terrestres.! Nous! définissons! une!
mesure!relative!(comparée!à!la!SR)!de!la!robustesse!de!la!PD!à!la!perte!d’habitat!et!nous!
montrons! qu’elle! est! toujours! supérieure! à! la! robustesse! de! la! SR! mais! qu’elle! varie!
selon! les! continents.! Nous! utilisons! ensuite! un! modèle! nul! pour! évaluer! la! part! de!
robustesse!expliquée!par!la!nature!hiérarchique!de!l’arbre!et!la!distribution!spatiale!des!
lignées.! Nous! montrons! que! cette! robustesse! est! relativement! bien! expliquée! par! la!
forme!de!l’arbre!mais!que!dans!certains!cas!la!distribution!spatiale!les!lignées!est!aussi!
importante.!!
! "!129!"!
Ecology, 96(10), 2015, pp. 2814–2822
! 2015 by the Ecological Society of America
Mammalian phylogenetic diversity–area relationships at a

continental scale
FLORENT MAZEL,1,2,7 JULIEN RENAUD,1,2 FRANÇOIS GUILHAUMON,3 DAVID MOUILLOT,4,5 DOMINIQUE GRAVEL,6
1,2
AND WILFRIED THUILLER
1
Universite´ Grenoble Alpes, Laboratoire d’Écologie Alpine (LECA), F-38000 Grenoble, France
2
CNRS, Laboratoire d’Écologie Alpine (LECA), F-38000 Grenoble, France
3
IRD, MARBEC Universite´ de Montpellier, Montpellier, France
4
MARBEC Universite´ de Montpellier, Montpellier, France
5
ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811 Australia
6
Universite´ du Québec à Rimouski, De´partement de Biologie, Chimie et Geógraphie, Que´bec, Quebec G5L 3A1 Canada
Abstract. In analogy to the species–area relationship (SAR), one of the few laws in
ecology, the phylogenetic diversity–area relationship (PDAR) describes the tendency of
phylogenetic diversity (PD) to increase with area. Although investigating PDAR has the
potential to unravel the underlying processes shaping assemblages across spatial scales and to
predict PD loss through habitat reduction, it has been little investigated so far. Focusing on
PD has noticeable advantages compared to species richness (SR), since PD also gives insights
on processes such as speciation/extinction, assembly rules and ecosystem functioning. Here we
investigate the universality and pervasiveness of the PDAR at continental scale using
terrestrial mammals as study case. We define the relative robustness of PD (compared to SR)
to habitat loss as the area between the standardized PDAR and standardized SAR (i.e.,
standardized by the diversity of the largest spatial window) divided by the area under the
standardized SAR only. This metric quantifies the relative increase of PD robustness
compared to SR robustness. We show that PD robustness is higher than SR robustness but
that it varies among continents. We further use a null model approach to disentangle the
relative effect of phylogenetic tree shape and nonrandom spatial distribution of evolutionary
history on the PDAR. We find that, for most spatial scales and for all continents except
Eurasia, PDARs are not different from expected by a model using only the observed SAR and
the shape of the phylogenetic tree at continental scale. Interestingly, we detect a strong
phylogenetic structure of the Eurasian PDAR that can be predicted by a model that
specifically account for a finer biogeographical delineation of this continent. In conclusion, the
relative robustness of PD to habitat loss compared to species richness is determined by the
phylogenetic tree shape but also depends on the spatial structure of PD.
Key words: conservation biogeography; habitat loss; null models; phylogenetic diversity; species–area
relationship; strict nested design.
INTRODUCTION history in species assemblages (Mouquet et al. 2012). To

fill this gap, the phylogenetic diversity–area relationship
The species–area relationship (SAR) describes the
(PDAR; Morlon et al. 2011) can help unravel the
tendency of species richness (SR) to increase with area
processes assembling communities across spatiotempo-
(Rosenzweig 1995). This relationship is documented for
ral scales and provides complementary tools for
a wide range of taxonomic groups and ecosystems
conserving the Tree of Life (Mazel et al. 2014). For
(Guilhaumon et al. 2008, Triantis et al. 2012) and its instance, translating SAR into PDAR allows to predict
understanding is central to ecology and conservation the loss of PD through habitat destruction. This
biogeography (Rosenzweig 1995, Whittaker et al. 2005). prediction is essential since the loss of a given amount
For instance, the SAR is a key tool to estimate species of PD or the loss of an entire lineage could have strong
extinctions from habitat destruction and climate change negative ecological consequences since distinct lineages
(Pimm and Raven 2000, Thomas et al. 2004, Pereira et are likely to perform different functions (Cadotte et al.
al. 2010, Matias et al. 2014). Nevertheless, a SAR 2008, Mouquet et al. 2012).
approach reduces biological diversity to species richness Several mechanisms have been proposed to explain
only and fails to include the amount of evolutionary the SAR, such as sampling effects (Rosenzweig 1995),
the effect of habitat size on extinction rates (MacArthur
Manuscript received 2 October 2014; revised 17 March 2015;
and Wilson 1967), the scaling of environmental hetero-
accepted 9 April 2015. Corresponding Editor: N. J. B. Kraft. geneity with area (Kadmon and Allouche 2007) or
7 E-mail: [email protected] dispersal limitation (Hubbell 2001). In complement to
2814
October 2015 MAMMALIAN PD–AREA RELATIONSHIP 2815
the SAR, the PDAR brings unique information about

the different processes structuring biodiversity at differ-
ent spatial scales, helping, for example, to quantify the
effects of biotic interactions at small scales vs. biogeo-
graphical processes at large scale. A particular feature of
the PDAR is that the shape of the phylogenetic tree
ultimately drives its relative position to the SAR. A star
phylogeny would produce a PDAR proportional to the
SAR, while a complete and recent polytomy at the tips
of the tree would produce an extreme PDAR that would
reach its maximum from the smallest area (see Fig. 1A).
In addition to those mechanisms, biogeographic history
together with ecological processes should also influence
the PDAR (see Fig. 1B). Allopatric speciation and/or
competition between close relative species would result
in a relatively higher PD than expected for a given SR
(overdispersion; Webb et al. 2002, O’Dwyer et al. 2012).
Coexistence theory indeed predicts that similar species
will compete more strongly than dissimilar species,
leading to the exclusion of one of the similar species
(HilleRisLambers et al. 2012). If we assume that niche
differences are properly portrayed by phylogenetic
differences, we predict a phylogenetic overdispersion
(i.e., distantly related species co-occur) under competi-
tive interactions (Webb et al. 2002, but see Mayfield and
Levine 2010). Reciprocally, low PD may be expected if
close relative species tend to co-occur because of shared
environmental niches and/or geographic isolation of FIG. 1. Expected variation of the standardized phylogenetic
land mass (phylogenetic clustering; Webb et al. 2002, diversity–area relationship (PDAR) given (A) different tree
shapes and (B) different eco-evolutionary processes. (A) The
O’Dwyer et al. 2012; see Fig. 1B). Overall the difference three standardized PDARs correspond to the three trees depicted
between SAR and PDAR curves is thus very informative above the graph. Note that the red PDAR also corresponds to
on the way the phylogenetic structure of assemblages the observed species–area relationship (SAR) as the red tree is a
varies across spatial scales. star phylogeny. (B) Different eco-evolutionary processes may
change the PDAR if they act differently among spatial scales. We
In summary, the PDAR is ultimately influenced by (1)
expect that competition and/or allopatric speciation may
the shape of the SAR that depends on species range relatively increase the phylogenetic diversity (PD) at small scale
placement over space (e.g., either clumped or random), while environmental filtering and/or geographic isolation of
(2) the structure of the phylogenetic tree, and (3) the biotas may relatively decrease the PD at small scale.
species range placement in regard to the phylogeny (that
ultimately depends on eco-evolutionary processes).
Since the pioneering work by Morlon et al. (2011), that produce median SAR and PDAR, respectively). First we
first introduced PDAR, no study has tried to explain ask whether PDAR differs from the SAR at a
large scale PDARs and to disentangle the relative continental scale and how this difference may affect
influence of these three factors. the robustness of PD to habitat loss. To do so we define
In this paper, we report the first large-scale analysis of the relative robustness of PD (compared to SR) to
PDAR over the globe for mammal assemblages. We habitat loss as the area between the standardized PDAR
used the calibrated and dated ultrametric phylogenetic and standardized SAR (i.e., standardized by the
tree updated by Fritz et al. (2009) from Bininda-Emonds diversity of the largest spatial window) divided by the
et al. (2007). We extracted the distribution maps area under the standardized SAR only (called the
provided by the Mammal Red List Assessment (avail- relative area under the curve, AUCr,). This metric
able online)8 for 4616 terrestrial species to obtain quantifies the relative increase of PD robustness
occurrence data on worldwide grid cells of approxi- compared to SR robustness (Fig. 2). Second, we ask
mately 110 3 110 km and used a strictly nested design whether PDARs are a simple consequence of the
recently published (SNQ; Storch et al. 2012) to produce observed SAR and a random sampling of species on
median SAR and PDAR at a continental scale (i.e., we the phylogenetic tree or if they also depend on eco-
computed median SR and PD over each spatial scale to evolutionary processes. Assuming that the continental
SAR for mammals can be adequately modelled by a
8 http://www.iucnredlist.org/ random placement model of species ranges (Storch et al.
2816 FLORENT MAZEL ET AL. Ecology, Vol. 96, No. 10
FIG. 2. Hypothetical example to quantify the relative robustness of PD (compared to species richness [SR]) to habitat loss
(relative area under the curve [AUCr]) using PDAR and SAR. The example shows how to quantify the relative PDAR shape by
measuring the area between the two curves (SR, PD, and Area are expressed as percentages) and computing AUCr.
2012), we derive PDAR expectations that only rely on Tucker and Cadotte 2013). The use of any PD metric
the phylogenetic tree shape. To do so, we use a tip- theoretically linked with SR in the description of PDAR
shuffling null model that keeps the observed species has been criticized because PDAR would be biased by
range distribution, SAR and phylogenetic tree shape ‘‘spurious artefacts of a statistical relationship between
while shuffling the phylogenetic relationships among species richness and area’’ (Helmus and Ives 2012). Here
species. Third, we ask whether AUCr depends on the the comparison of the SAR and the PDAR we propose,
phylogenetic tree shape only (see Fig. 1A) or if it is also i.e., with the standardization and the null model that
an outcome of eco-evolutionary processes (see Fig. 1B). removes the effect of SR on PD (see Analyzing SAR and
To do so we take advantage of our null model approach PDR: Understanding the absolute value of PDAR) avoid
to produce null AUCr expectations. More specifically we this artefact while it allows a simple interpretation of the
estimate the effect of tree structure (see Fig. 1A) on the results.
relative robustness of PD to habitat loss across
continents. Our analyses confirm that PD might be Constructing SAR and PDAR
more robust than SR to habitat loss but that this higher
Median and median absolute deviance (MAD) of SR
robustness differs across continents for different rea-
and PD were reported for each spatial scale (from 110 3
sons.
110 km up to 2200 3 2200 km) by using the framework
METHODS proposed by Storch et al. (2012). We do not use mean
Data sets and diversity metrics SR and PD as the data was highly non-normal (see
Appendix A for examples of distributions of diversity).
We used the distribution maps provided by the It uses a strictly nested quadrat design where a moving
Mammal Red List Assessment (see footnote 8) for window (Leitner and Rosenzweig 1997, Lennon et al.
4616 terrestrial species to obtain occurrence data on 2001) reports the SR and PD of all possible windows of
worldwide grid cells of approximately 110 3 110 km. a given size within a continent. The median and MAD of
The best resolution to use the IUCN maps is still under
SR and PD are then computed for each spatial scale.
discussion in the literature (Storch et al. 2012, Jenkins et
This procedure implies that some cells are counted
al. 2013). We here used the resolution commonly used at
several time for a given spatial windows and thus some
global scale (Belmaker and Jetz 2011, Storch et al. 2012).
pseudo-replication is inevitably introduced. Nevertheless
This was our basic unit to construct SAR and PDAR.
all designs have their own drawbacks and SNQ have
Domestic, aquatic, and semiaquatic mammals were
excluded from the analysis. several important advantages (Storch et al. 2012). We
We used the calibrated and dated ultrametric phylo- implemented the algorithm within a reduced subset of
genetic tree updated by Fritz et al. (2009) from Bininda- the five continents (see Appendix B for further details) to
Emonds et al. (2007). avoid some border effect, i.e., for each scale (whatever
To characterize the PD of an assemblage we used the its size), all pixels of the selected area of the continent
Faith’s measure (Faith 1992). This metric represents a will be sampled at least one time. The spectrum of
richness or volume of diversity (Pavoine and Bonsall spatial scale analyzed was set between 1 3 1 to 14 3 14
2011) and simply sums up branch lengths of the given cells for Australia (i.e., from approximately 110 3 110
species assemblage phylogeny (Rodrigues and Gaston km to 1540 3 1540 km) and from 1 3 1 to 20 3 20 cells
2002). Faith’s measure is an intuitive and relatively for North and South America, Africa, and Eurasia (i.e.,
simple measure of PD. It is also, by construction, from approximately 110 3 110 km to 2200 3 2200 km)
generally highly correlated with SR (Huang et al. 2012, following Storch et al. (2012). Note that the resulting
curve corresponds to a type I curve in the terminology distribution of range size and the local species richness
proposed by Scheiner (2003). (Hardy 2008). By repeating this procedure n times, we
were able to assess the significance of the observed
Analyzing SAR and PDAR PDAR relative to our null expectation (using a two-
Comparing the relative shape of SAR and PDAR.—We sided test).
compared the shape of PDAR and SAR using two In other words, for each randomization, we (1)
complementary approaches. First we fitted a power shuffled the tips of the phylogeny within a given species
model (Rosenzweig 1995) to each SAR and PDAR. We pool. The resulting randomized phylogeny was used to
then reported the slope (z) value of the linear model in a (2) compute null PD values for each basic grid cells
log-log space. These values were then used to depict in a (approximately 110 3 110 km) and we (3) applied the
simple way the relative shape of PDAR and SAR. methodology described above to compute the resulting
Because PDAR and SAR are not necessarily best null median and MAD PDARs. Such null model may
modelled by a power function (Guilhaumon et al. help unravel the determinants of the PDAR. For
2008, Mazel et al. 2014) we also (1) fitted alternative example we may expect competition (Pigot and Tobias
statistical models (see Appendix C) and (2) directly 2013) or environmental filtering to occur at smaller
compared PDAR and SAR without an a priori function. scale, potentially leading to phylogenetic overdispersion
As PD is expressed in units of times while SR in number or clustering respectively (Webb et al. 2002; but note
of species, they are not directly comparable. Therefore that competition may also lead to clustering, see
we used a basic standardization procedure by rescaling Mayfield and Levine [2010]). Also, phylogenetic cluster-
each sampling windows PD and SR value by the value ing could be detected at larger scales because of
reached at the maximum sample size (Mazel et al. 2014). biogeographical effect (Rosenzweig 1995). We used
This gives a relative diversity value for each sampling two null models that use either a continental or a
windows, compared to the largest one (that thus biogeographic pool of species. We restricted the analysis
represents 100%). We define the relative robustness of of the biogeographic pool of species for Eurasia only
PD (compared to SR) to habitat loss as the area between because it is the only continent in our design that is a
the standardized PDAR and standardized SAR divided mix of distantly related zoogeographic regions (Wallace
by the area under the standardized SAR only (Eq. 1 and 1876, Holt et al. 2013).
Fig. 2).
Continental pool of species
AUCPDAR " AUCSAR
AUCr ¼ : ð1Þ This null model simply shuffles the tips within the
AUCSAR
entire continental phylogeny. The significance of the
observed values of PDAR was assessed by comparing
If we define the absolute robustness of PD and SR as observed values with 1000 randomized PDARs. We
the AUC under the PDAR and SAR, our metric further confirmed this simulation approach by using
quantifies the relative increase of absolute PD robust- analytical expectations of PD based on the framework
ness compared to absolute SR robustness (Fig. 2). To of Nipperess and Matsen (2013; Appendix D)
study the relative increase of PD and SR with area we
simply computed the local slope (or derivative) of Biogeographical pool of species
PDAR and SAR on the standardized coordinates First we defined zoogeographic regions following the
assuming a first point of null diversity and area. Indeed methodology of Holt et al. (2013). To do so we
when area tends to zero, diversity also necessarily tends computed phylogenetic beta diversity values between
to zero (as sampled area becomes smaller than a single each pair of grid cells from the Eurasian continent by
individual). using an index independent of species richness (Lennon
Understanding the absolute value of PDAR.—Second et al. 2001, Holt et al. 2013):
we used a null model approach to describe and a
investigate the absolute value of PDAR. This approach b¼1" ð2Þ
minðb; cÞ þ a
allows to compare null expectations with the observed
PDAR and avoids the bias caused by the correlation where a ¼ the branch lengths shared by the two grid cells
between PD and SR. and b and c represent the branch lengths unique to each
We chose to use the observed SAR as a starting point grid cell, with min(b,c) representing the minimum value
because it has already been shown to be modelled by a between b and c.
simple null model where species ranges are randomly Then we identified groups of grid cells (zoogeographic
distributed within the continent (Storch et al. 2012). regions) using the unweighted pair group method with
Assuming the SAR, we computed a null PDAR arithmetic mean (UPGMA, function hclust in R; R
expectation by randomly shuffling the tips of the Development Core Team 2014). We varied the number
phylogeny within a given pool of species. This procedure of delimited zoogeographic regions from 1 to 30 (see
breaks the link between species range size/position and Appendix E for examples). We then used these regions
phylogenetic relationships but keep unchanged the to construct a biogeographical null model of the PDAR.
FIG. 3. Observed rescaled median SARs and median PDARs. For each continent, we report the SAR and the PDAR rescaled
by the value of the maximum SR and PD, respectively. The two curves are both expressed in percentage of maximum diversity and
thus are directly comparable. We also report the corresponding AUCr values (see Fig. 2). In the lower-right corner subplots, we
show the corresponding local derivatives.
While we were shuffling species within the entire maximal diversity reached in the data set. The two
continental pool of species in the previous null model, resulting curves are thus expressed as the percentage of
we shuffled here species within the pool of species maximal diversity and are directly comparable (Fig. 3).
belonging to a specific zoogeographic region. Because all We show that PDARs approach their maximum faster
species are not restricted to one unique zoogeographic than SARs for all continents (Fig. 3). To describe the
region, we adopted a probabilistic approach where, for rate of PD and SR accumulation as a function of area,
each randomization independently, a zoogeographic we estimated local derivatives and show that PDARs
region k is assigned to a species i with a probability of accelerate much faster than SARs for small areas and
Pi,k depending on its coverage Ci,k in this region with that this tendency reverses for large areas (see subplots
respect to its total coverage across all regions of Fig. 3). We show that the power model is among the
best models to fit the data set (Appendix F) but fails to
Ci;k
Pi;k ¼ X ð3Þ model the upward acceleration of PD on a log-log scale
Ci;k (e.g., Fig. 4). The slope of the power model is lower for
K
the PDARs than for the SAR (zPDAR , zSAR, see
where K represents the entire set of regions (from 2 to Appendix G). The last point has been previously
30). For each randomization, we computed a null reported at this scale (Mazel et al. 2014) but with a
PDAR and tested significance by comparing the different PDAR/SAR reconstruction based on non-
observed PDAR and 100 null PDAR for each number overlapping ecoregions (Olson et al. 2001). This result is
of zoogeographic regions defined. thus independent of the sampling procedure and
approaches, and is, overall, not surprising. Indeed the
RESULTS AND DISCUSSION SAR fully represents the PDAR in the case of a star
To visually compare the PDAR and the SAR of phylogeny (in this case, the PD is proportional to SR).
mammals we standardized the two curves by the As the phylogenetic tree departs from a star phylogeny
FIG. 4. Median PDARs obtained from the continental null model. For each continent, the envelope corresponding to 1000 null
continental PDARs is shown in black while the observed PDAR is in red. In the corner of each panel, we plot the relative rank of
observed PD value within the null PD distribution as a function of log(area) (logA). For each spatial scale, it is computed as the
proportion of null PD values that are lower than the observed value (a value of 0.5 indicates that observed PD equals the median of
the null distribution). The dashed lines correspond to a relative rank of 2.5% and 97.5%. When the computed relative ranks fall out
of this 95% envelope, a star is reported in the main panel (see Appendix H for the relative ranks associated with power model
parameters).
(i.e., as some branches start to be shared between habitat loss (Pimm and Raven 2000, Thomas et al. 2004,
species), the relationship between PD and SR becomes Halley et al. 2014) has been questioned (He and Hubbell
concave and the PDAR deviates from the SAR (because 2011) but remains useful (e.g., Axelsen et al. 2013,
redundancies between species are introduced, see Fig. Hanski and Zurita 2013, Matias et al. 2014), especially
1A). when species ranges are randomly distributed (He and
As a consequence, AUCr values are positive but we Hubbell 2011). If we assume that the SAR and the
find that they differ across continents (see Figs. 2 and 3). PDAR can be used to predict the loss of species and PD,
The use of the SAR to predict species extinction from respectively, through habitat loss (Mazel et al. 2014), the
FIG. 5. Median PDARs obtained from the Eurasian biogeographical null models. The biogeographical null models shuffle the
tips of the phylogeny according to biogeographical origin (see Methods). We present the results from null models containing
different numbers of biogeographical regions. The top panel presents the median PDAR obtained for different numbers of
biogeographic regions. The four other panels represent the details of four biogeographic null models that used 1 (continental null
model), 2, 15, or 30 biogeographic regions, respectively. The star indicates that the relative rank of the observed PD value within the
null PD distribution is lower (or higher) than 0.025 (or 0.975) for a given area.
AUCr (Fig. 2) then represents the relative robustness of averaged phylogenetic structure across a whole conti-
PD (compared to SR) to habitat destruction. In this nent and different assembly processes may have been
case, we show, for example, that the Australian PD will mixed. In North America, for example, we could expect
be relatively more robust, at the continental scale, to a phylogenetic clustering at high elevation in the Rocky
habitat loss than the Eurasian PD (note that, at the Mountains (e.g., due to environmental filtering) while
global scale, the evolutionary history of Australia is overdispersion could be found in the lowland forest
unique; Holt et al. 2013). This difference could be (e.g., due to competition; Graham et al. 2009), resulting
explained by the different structure of the two trees (see in higher MAD of PD than expected by chance (see
Fig. 1A) and/or by different eco-evolutionary processes Appendix I). Such distribution may likely compensate
leading to a different spatial pattern of PD (e.g., either each other during the sampling process, resulting in a
clustered, random, or overdispersed; see Fig. 1B). null random distribution when averaged across assem-
Teasing apart these two mechanisms called for using blages. Second, the spatial and phylogenetic scale of our
appropriate null models. analysis is perhaps too large to detect any effect of
For all continents except Eurasia, and for most of the repulsion/attraction of species. Indeed, at the smallest
spatial scales, we find that PD values are not signif- resolution we have used (110 3 110 km), co-occurring
icantly different from those obtained with the null model species do not necessarily interact with each other
randomizing the phylogenetic relationships among (probably because this scale is still very large) and
species (Fig. 4 and Appendix H). This means that the may, for example, use different habitats (Araújo and
only significant phylogenetic effect that influences the Rozenfeld 2014, but see Cardillo 2011). Also, specific
PDAR is the shape of the observed continental tree. group of mammals may show repulsion or attraction
Several non-mutually exclusive hypotheses can be while others not, blurring the overall pattern (see, e.g.,
proposed to explain this result. First, we use here an Pedersen et al. 2014).
The Eurasian PDAR is, however, much lower than the robustness of PD to habitat loss depends on the
expected by chance at all spatial scales, indicating structure of the phylogenetic tree (represented here by
phylogenetic clustering (Fig. 4 and Appendix H). This the null model mean expectation) and also on the spatial
continent is a mosaic of biogeographic realms with pattern of phylogenetic structure (represented by the
diverging biogeographic history (Wallace 1876, Holt et departure of the observed PDAR from the mean null
al. 2013) and thus mixes very different faunas: there are model, see subplots in Fig. 4). We indeed find that
many strict Palearctic species (e.g., the wolverine, Gulo Australian observed AUCr is higher than predicted by
gulo) and strict oriental species (e.g., the Asiatic the continental tree structure because small scale
elephant, Elephas maximus). The continental null model Australian PD tends to be relatively higher than
mixes all these faunas and thus tends to overestimate the expected by chance (see Appendix L), providing a buffer
expected median PD of assemblages. For example, against the loss of PD. In contrast, observed Eurasia
Elephas maximus represents the only Afrotherian species AUCr is lower than expected by the tree shape (see
present in our data set so it has a very high Appendix L). This is because Eurasian PD is dispro-
distinctiveness at the continental scale and will consid- portionately low at small scale, reducing the area
erably increase relative local PD. We consequently between the PDAR and the SAR compared to random
develop a biogeographical null model that takes into expectations and thus being more vulnerable to habitat
account the historical origin of taxa. We show that this reduction. Overall, we demonstrate that the additional
null model progressively decreases the random PD robustness of PD to habitat loss compared to species
expectations (Fig. 5) and that 15 realms were sufficient richness is determined by the phylogenetic tree shape but
to correctly predict most of the spatial scale median PD also depends on the spatial structure of PD.
(Fig. 5 and Appendices J–K). Our approach may sound
ACKNOWLEDGMENTS
circular at first glance because we use spatial and
F. Mazel would like to thank Loı̈c Chalmandrier for helpful
phylogenetic data (to define zoogeographic regions) to
discussions on null models, Petr Keil for discussions on the
explain spatial and phylogenetic data (the PDAR). PDARs, and two anonymous referees for helpful comments on
Nevertheless, the aim of any null models is rather to ask a previous version of the manuscript. The research leading to
how much synthetic information we need from the initial these results had received funding from the European Research
data to parsimoniously explain this data. The null model Council under the European Community’s Seven Framework
Programme FP7/2007-2013 Grant Agreement no. 281422
is necessarily constrained by the initial data but if this (TEEMBIO). F. Mazel, W. Thuiller, and J. Renaud belong to
constrain is too high (i.e., a lot of the initial data is used) the Laboratoire d’Écologie Alpine, which is part of Labex
the null model will necessarily be plausible (the OSUG@2020 (ANR10 LABX56).
‘‘narcissus effect’’; Gotelli 2001). Here our aim is to
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SUPPLEMENTAL MATERIALS
Ecological Archives
Appendices A–L are available online: http://dx.doi.org/10.1890/14-1858.1.sm
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phylogénétique! à! l’échelle! des! biomes! terrestres! et! de! les! comparer! aux! points! chauds!
«!classiques!»! basés! sur! la! richesse! spécifique! uniquement.! Nous! utilisons! les!
mammifères! sur! l’ensemble! globe! terrestre! comme! cas! d’étude.! Nous! avons! calculé! la!
richesse! spécifique,! la! diversité! fonctionnelle! et! phylogénétique! pour! 782! écorégions!
terrestres!en!utilisant!les!aires!de!distributions!de!4616!mammifères.!Nous!avons!utilisé!
un!ensemble!d’indices!de!diversité!qui!incorpore!les!couverts!relatifs!des!espèces!dans!
chaque!écorégion.!Nous!avons!ensuite!construit!des!relations!aireQdiversité!à!plusieurs!
facettes! afin! d’ordonner! les! écorégions! selon! leur! niveau! de! diversité.! Nous! avons!
finalement!défini!les!points!chauds!comme!les!écorégions!avec!le!plus!de!diversité.!Nous!
montrons!que!les!points!chauds!de!diversité!phylogénétique!et!fonctionnelle!ne!sont!en!
général!ni!congruents!entre!eux!ni!avec!les!points!chauds!classiques.!Ceci!démontre!que!
les! plans! de! conservation! qui! se! focalisent! sur! la! richesse! spécifique! uniquement!
peuvent! passer! à! côté! des! autres! facettes! de! la! diversité.! En! conséquence,! il! est! d’une!
importance! vitale! d’adopter! une! perspective! à! plusieurs! facettes! de! diversité! pour!
solidifier!l’approche!de!conservation!intégrative.!
! 141!
Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2014) 23, 836–847
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RE S E A RCH Multifaceted diversity–area relationships

PA P E R
reveal global hotspots of mammalian
species, trait and lineage diversity
Florent Mazel1*, François Guilhaumon2, Nicolas Mouquet3,
Vincent Devictor3, Dominique Gravel4, Julien Renaud1,
Marcus Vinicius Cianciaruso5, Rafael Loyola5,
José Alexandre Felizola Diniz-Filho5, David Mouillot2,6 and Wilfried Thuiller1
1
Laboratoire d’Ecologie Alpine, Grenoble, ABSTRACT
France, 2Laboratoire ECOSYM Université
Montpellier 2, Montpellier, France, 3Institut
Aim To define biome-scale hotspots of phylogenetic and functional mammalian
des Sciences de l’Evolution, UMR 5554, CNRS, biodiversity (PD and FD, respectively) and compare them with ‘classical’ hotspots
Université Montpellier 2, Montpellier, France, based on species richness (SR) alone.
4
Département de Biologie, Chimie et Location Global.
Géographie, Université du Québec à Rimouski,
Québec, Canada, 5Departamento de Ecologia, Methods SR, PD and FD were computed for 782 terrestrial ecoregions using the
ICB, Universidade federal de Goiàs, Goiâna, distribution ranges of 4616 mammalian species. We used a set of comprehensive
Brasil, 6ARC Centre of Excellence for Coral diversity indices unified by a recent framework incorporating the relative species
Reef Studies, James Cook University, coverage in each ecoregion. We built large-scale multifaceted diversity–area rela-
Townsville, Qld 4811, Australia tionships to rank ecoregions according to their levels of biodiversity while account-
ing for the effect of area on each facet of diversity. Finally we defined hotspots as the
top-ranked ecoregions.
Results While ignoring relative species coverage led to a fairly good congruence
between biome-scale top ranked SR, PD and FD hotspots, ecoregions harbouring a
rich and abundantly represented evolutionary history and FD did not match with
the top-ranked ecoregions defined by SR. More importantly PD and FD hotspots
showed important spatial mismatches. We also found that FD and PD generally
reached their maximum values faster than SR as a function of area.
Main conclusions The fact that PD/FD reach their maximum value faster than
SR could suggest that the two former facets might be less vulnerable to habitat loss
than the latter. While this point is expected, it is the first time that it has been
quantified at a global scale and should have important consequences for conserva-
tion. Incorporating relative species coverage into the delineation of multifaceted
hotspots of diversity led to weak congruence between SR, PD and FD hotspots. This
means that maximizing species number may fail to preserve those nodes (in the
phylogenetic or functional tree) that are relatively abundant in the ecoregion. As a
consequence it may be of prime importance to adopt a multifaceted biodiversity
perspective to inform conservation strategies at a global scale.
Keywords
*Correpondence: Florent Mazel, CNRS, LECA,
Conservation biogeography, diversity indices, functional diversity–area rela-
2233 Rue de la Piscine, Grenoble, Isère, 38041,
France. tionship, Hill’s numbers, mammals, phylogenetic diversity–area relationship,
E-mail: [email protected] species–area relationship.
DOI: 10.1111/geb.12158
836 © 2014 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/geb
Global hotspots of multifaceted mammal diversity
The most recent comparisons of the world-wide distribution

INTRODUCTION
of hotspots have been limited to different taxonomic groups and
Understanding the ecological and evolutionary processes components of SR for a given taxon (e.g. endemic, total, endan-
driving the distribution of life on Earth is essential from both gered; Orme et al., 2005; Ceballos & Ehrlich, 2006; Lamoreux
applied and theoretical perspectives. The quantification of bio- et al., 2006) or when carried out in a multifaceted context, have
diversity, central to conservation science, has recently moved included only limited functional information [e.g. Huang et al.
from a focus on pure species counting (e.g. species richness, SR) (2012) used only geographic range size and body mass as descrip-
to a more integrative approach. Assessments of biodiversity now tors of mammal FD to define hotspots]. This lack of relevant trait
consider the overall evolutionary history embedded within a set information makes it difficult to adequately represent the spatial
of taxa (i.e. phylogenetic diversity, PD) along with the diversity distribution of FD because geographic range size may not prop-
of ecological traits (i.e. functional diversity, FD). In conservation erly portray species niches, rather it is mostly influenced by
science, this novel approach has redefined the identification of historical biogeography and macroevolution (Gaston, 2003).
species of conservation interest by taking their high evolution- Here we identified global hotspots of mammalian taxono-
ary or functional distinctiveness into consideration (Isaac et al., mic diversity (TD), PD and FD. We based our analyses on the
2007; Mouillot et al., 2013) and has also made it possible to updated version (Fritz et al., 2009) of the dated phylogeny
detect unique macroecological assemblages (Forest et al., 2007), of Bininda-Emonds et al. (2007) and a set of functional traits
for example ‘cradles’ and ‘museums’ of life (Chown & Gaston, encompassing important aspects of mammal resource use,
2000). Furthermore, the loss of FD or PD per unit of habitat loss selected to represent independent and informative niche dimen-
is likely to be a better predictor of ecosystem vulnerability than sions (Safi et al., 2011). We used the world’s ecoregions (Olson
the loss of single species. Indeed, the loss of a given amount of et al., 2001) to define geographical units harbouring unique
FD or PD, often assumed to be related to particular combina- species assemblages and ecosystems. Ecoregions have proven
tions of functional traits or of a certain lineage, respectively, may valuable for addressing a range of questions in macroecology
threaten the functioning of the ecosystem, whereas the loss of a and more applied conservation issues (Lamoreux et al., 2006;
given single species might not be noticeable if redundant species Guilhaumon et al., 2008).
persist (Loreau et al., 2002; Srivastava et al., 2012). To account for expected area effects on TD (Triantis et al.,
This new perspective also provides fundamental insights into 2012), PD (Morlon et al., 2011) and FD (Cumming & Child, 2009)
community assembly at multiple spatial scales (Mouquet et al., we constructed diversity–area relationships (DARs hereafter) for
2012). A multifaceted approach may help unravel the different 13 terrestrial biomes (global-scale regions gathering ecoregions
drivers of community structure (e.g. competition or environ- experiencing similar environmental conditions such as tundra or
mental filtering; Webb et al., 2002) or ecosystem functioning mediterranean forests). We used a model-averaging approach that
(Cadotte et al., 2009; Gravel et al., 2012). In macroecology, con- fits 19 mathematical functions to the data (Guilhaumon et al.,
trasting SR, PD and FD offers a potential means for disentan- 2008; Triantis et al., 2012) and then computed an Akaike informa-
gling the processes shaping large-scale diversity distribution tion criterion (AIC)-weighted average of the 19 predicted curves.
(Davies & Buckley, 2011; Safi et al., 2011; Huang et al., 2012). To quantify the different types of diversity, we used a set of unified
For example, the global latitudinal diversity gradient has TD, PD and FD indices that weigh species coverage differently
recently been re-interpreted from a novel evolutionary perspec- (Chao et al., 2010) and correspond to modified versions of Faith
tive, merging Earth’s climatic history, phylogenetic diversity and PD (Faith, 1992), Phylogenetic entropy (Allen et al., 2009) and Rao
species richness in a unified and testable framework (Hawkins quadratic entropy (Rao, 1992) (see Methods). For each diversity
et al., 2012). A multifaceted perspective thus represents a prom- index we identified as hotspots those ecoregions with the largest
ising avenue for exploring the distribution of diversity because it positive deviations from, respectively, SARs (species–area relation-
is at the crossroads between ecology, evolution and conservation ships), PDARs (phylogenetic diversity–area relationships) and
biology but also palaeontology and palaeoclimatology (Hawkins FDARs (functional diversity–area relationships) and investigated
et al., 2006). their spatial congruences.
One of the most striking features of biodiversity is the spatial Our global exploration of mammals SARs, PDARs and
heterogeneity of its distribution, with some regions harbouring FDARs reveals important mismatches between the spatial
extraordinary levels of biodiversity: the so-called biodiversity scaling and the geographical extremes of SR, PD and FD, calling
hotspots (Reid, 1998; Ceballos & Ehrlich, 2006; Guilhaumon for integrative approaches.
et al., 2008). These have not only fascinated macroecologists,
who try to understand their origins (e.g. the historical perspec-
METHODS
tive; Wiens et al., 2011), but also conservationists seeking the
best opportunities to allocate the limited resources available for
Dataset
global-scale conservation. For example the biodiversity hotspots
concept has been proposed to prevent the extinction of large
Mammal assemblages
numbers of endangered species, by protecting places ‘where
exceptional concentrations of endemic species are undergoing We used the distribution maps provided by the Mammal
exceptional loss of habitat’ (Myers et al., 2000). Red List Assessment (http://www.iucnredlist.org/) for 4616
Global Ecology and Biogeography, 23, 836–847, © 2014 John Wiley & Sons Ltd 837
F. Mazel et al.
terrestrial species (for which we have functional traits; see local abundance, for example because it uses an abundant
below) to obtain occurrence data for each of the 827 ecoregions resource that is restricted to a small area of the ecoregion. Never-
defined by Olson et al. (2001). We retained 782 ecoregions theless, we believe that our measure of species coverage was a
(mean number of ecoregions per biome = 60.1, SD = 53.3, needed first step to incorporate abundances into the definition
min. = 17, max. = 223). Ecoregions are a valuable tool for study- of PD/FD hotspots.
ing multifaceted hotspots because they also serve as the basis
of World Wildlife Fund conservation planning (Olson &
Dinerstein, 1998), the international efforts of Nature Conserv- Phylogeny and functional traits
ancy (Groves, 2003) and the delineation of Conservation Inter- We used the calibrated and dated ultrametric phylogenetic
national’s Biodiversity Hotspots (Mittermeier et al., 2004) and tree updated by Fritz et al. (2009) from Bininda-Emonds et al.
High Biodiversity Wilderness Areas (Mittermeier et al., 2003). (2007). We computed functional diversity indices using body
Furthermore, ecoregions have commonly been used to define mass (log-transformed), diet (vertebrates, invertebrates, foliage,
taxonomic hotspots (Lamoreux et al., 2006; Guilhaumon et al., stems and bark, grass, fruits, seeds, flowers, nectar and pollen,
2008) because they encompass relatively homogeneous biologi- roots and tubers), habits (aquatic, fossorial, ground-dwelling,
cal systems. We retained ecoregions harbouring more than one above-ground-dwelling), activity period (diurnal, nocturnal,
mammal species and excluded mangrove ecoregions and large cathemeral, crepuscular) and litter size (data from Safi et al.,
uninhabited parts of Greenland and Antarctica because of low 2011). These traits encompass important aspects of mammal
data reliability or availability for these areas (Lamoreux et al., resource use, including the temporal and spatial windows used
2006). Domestic mammals were also excluded from the analysis. to get their food. They represent independent and informative
For each ecoregion and species, species coverage (Ci) was niche dimensions for evaluating variability in mammal traits
calculated as the intersected surface (in km2) between the range related to important ecosystem processes, such as decomposi-
of the species and the ecoregion. We then computed, for each tion and seed dispersal, as well as trophic control (Sekercioglu,
species i, the following relative coverage (RCi, equation 1) 2010).
Ci
RCi = .
∑i
Ci (1)
Diversity indices
A myriad of methods have been proposed in the last years to
Basically a species will have low relative coverage in a given
include species traits in diversity indices (Pavoine & Bonsall,
ecoregion if its distribution range is small. The relative coverage
2011). Here we follow the comprehensive framework from
was used to calculate diversity indices incorporating relative
Chao et al. (2010), which unifies a set of TD, PD and FD indices
abundance (see below). By doing this we were able to differen-
based on Hill numbers. There were three reasons for this. First
tiate a species that is poorly represented in an ecoregion, but
it unifies most of the TD, PD and FD indices used in the litera-
with a unique evolutionary history (e.g. a monotreme species)
ture (see below and Table 1). Second it represents equivalent
or with unique functional traits (e.g. a top predator), from
numbers of species to satisfy the replication principle that
species with a similar evolutionary history (or functional traits)
ensures intuitive results for ecologists and conservation biolo-
but with greater occupancy in the ecoregion. This weighting
gists (Jost, 2006; Chao et al., 2010). For example, if the PD of an
scheme emphasizes species that are well distributed in the
assemblage equals d (d being a real positive number), it has the
ecoregion. Establishing how our measure of relative coverage is
same diversity as a community consisting of d equally abundant
important for conservation and ecosystem functioning is not
and maximally distinct species (i.e. with the maximum distance
straightforward. Nevertheless we believe that the evolutionary
observed in the phylogeny). Third, we present here one of the
history/functional characteristics of a species that shows a very
only comprehensive and intuitive frameworks that incorporates
small distribution range in a given ecoregion should not have
relative species coverage (or abundance) into biodiversity
the same theoretical influence on PD/FD as a widespread species
indices.
in this ecoregion. Although it is unlikely that our measure of
relative coverage represents a direct measure of local species
abundance, it has been shown that a positive relationship Phylogenetic diversity
between range size and local abundance is common (Gaston
et al., 2000). Nevertheless departure from this relationship prob- Consider a phylogenetic tree composed of a set Bt of i branches.
ably exists. First, we did not use the complete range size of the PD can be defined as the ‘mean diversity of order q over T years’
species but only its extent in the ecoregion. Second, we acknow- (Chao et al., 2010):
ledge that the potential important residual variation that
1 (1−q )
exists around the relationship may depend on species life-  Li q 
history traits. For example species with high dispersal abilities
q
∑
D (T ) =  ai 
i∈BT T 
(2)
(or a species at a high level in the trophic hierarchy) may have a
large range size but be relatively rare at the local scale. It is also where Li is the length of branch i in the set Bt, ai is the
possible that a species with a narrow range may exhibit a high total abundance descended from branch i (i.e. the summed
838 Global Ecology and Biogeography, 23, 836–847, © 2014 John Wiley & Sons Ltd
Table 1 The set of diversity indices used in the analysis.
Type of indices
Original version
Without species differences SR Shannon Simpson
With species differences Phylo. PD (Faith, 1992) Hp QE*
Functio. FD (Petchey & Gaston, 2006) Not named QE*
Hill numbers version
Without species differences SR exp (Shannon) 1 / Simpson
With species differences Phylo. Faithcor PD Allencor PD Raocor PD
Functio. Faithcor FD Allencor FD Raocor FD
Link between original and Faithcor PD = PD / T Allencor PD & Raocor PD &
Hill numbers version Faithcor FD = FD / T FD = exp (Hp/T) FD = 1/ (1- QE)
q value 0 1 2
Weighting by species’ coverage No Yes Yes
For this study we used the Hill numbers version with species differences. These transformed versions obey the replication principle and can be grouped
in a unified formula using the q parameter (see equation 2 and Chao et al., 2010). The table gives the abbreviations used in the text. It also provides the
link between original and transformed indices and indicates if coverage is used in the calculation of the indices.
*QE can be calculated with any distances (phylogenetic or functional) between species.
T represents the height of the phylogenetic tree or the functional dendrogram. PD, Phylogenetic diversity; FD, Functional diversity; Hp, Phylogenetic
entropy (Allen et al. 2009); QE, Rao quadratic entropy (Rao, 1982); SR, Species richness; Phylo, Phylogenetic; Functio, Functional.
abundance or relative coverage of species descending from this ing the ultrametric property (note that using non-ultrametric
branch) and T is the height of the tree. The parameter q affects functional distances did not change our conclusions) using
the influence of node (or branch segment) abundance on the the unweighted pair group method with arithmetic mean
diversity index: a high q-value gives more weight to nodes with (UPGMA) (function hclust in R; R Development Core Team,
high relative abundances. This general formula encompasses 2010). The corresponding FD indices were named Faithcor FD,
a set of well-known diversity indices. With q = 0, Faithcor Allencor FD and Raocor FD (see Table 1). Note that Faithcor FD
PD = PDFaith/T, PDFaith being the phylogenetic diversity defined is equivalent to the Petchey & Gaston (2006) definition of FD
by Faith (1992) and Faithcor PD being the corrected version of (i.e. ‘the total branch length of a functional dendrogram’). Like
the Faith PD. With q = 1, Allencor PD = exp(Hp/T), Hp being the Faithcor PD, Faithcor FD is intrinsically correlated to SR (Huang
phylogenetic entropy as defined by Allen et al. (2009) and et al., 2012). This is the case for all the dendrogram-based
Allencor PD being the corrected version of Hp.. With q = 2, Raocor approaches for estimating functional volume. Nevertheless it is
PD = 1/(1 − QE), QE being the quadratic entropy defined by interesting to use it here because it is directly comparable with
Rao (1982) and Raocor PD being the corrected version of QE (see Faithcor PD and represents a diversity volume (or ‘richness’ sensu
Table 1 for details). To summarize, q influences the relative Pavoine & Bonsall, 2011). In addition we computed FD using
weight of widespread versus rare species in the computation of body mass only to test to what extent the use of multiple traits
the diversity index. It gives progressively more weight to wide- influences our results. Note also that the expected correlation
spread species and progressively ignores rare species. This point between SR and FD/PD based on dendrogram becomes weaker
could be problematic if a species is rare and endemic in this when moving from q = 0 to q = 2.
ecoregion because we will progressively ignore this unique
species. Nevertheless our study aims to characterize the evolu-
tionary history and the functional characteristics that are wide- Species diversity
spread in a given ecoregion (and somehow representative), For maximally distinct species (i.e. a star phylogeny or star func-
which justifies the use of Chao et al.’s (2010) framework. tional dendrogram), these indices actually constitute species
diversity indices, namely SR when q = 0, the exponential of
Shannon entropy when q = 1 and the inverse of Simpson diver-
Functional diversity
sity when q = 2 (see Table 1; Chao et al., 2010). We used these
We adapted previous indices for FD. First, we calculated func- TD indices to compare appropriately PDAR/FDAR with the cor-
tional distance among pairs of species using the Gower distance, responding SAR (i.e. comparing DARs that are built with diver-
which can mix categorical and continuous traits with equal sity indices based on the same q). However, we always compared
weight and can cope with missing values (some traits were PD/FD hotspots with those based on SR (and not Simpson
missing for 80 species, representing less than 2% of our dataset). or Shannon indices) since a list of hotspots based only on TD
We then applied a hierarchical cluster algorithm to convert the indices (i.e only quantifying evenness in abundances) might not
functional distance matrix into a functional dendrogram ensur- be appropriate in a conservation context.
F. Mazel et al.
report the percentage of maximal diversity reached in this

Constructing DARs
largest ecoregion. The resulting standardized DAR therefore
To account for expected area effects on SR, PD and FD, we ranges between 0 and 1, which makes it possible to compare the
provide a construction of DARs for 13 terrestrial biomes (Olson scaling of different diversity facets with area (see below).
et al., 2001). Such DARs correspond to a non-overlapping
design, i.e. they are built from single data points, which corre- Hotspot lists and spatial congruence
sponds to a type IV curve in Scheiner’s (2003) terminology.
Hotspot selection
Set of models Averaged residuals were calculated from the standardized aver-
A wide range of statistical models have been proposed to aged model (as defined above). A positive residual for a given
describe SARs (Tjørve, 2009). Here, 19 models were selected to ecoregion means that observed diversity is higher than expected
fit SAR, PDAR and FDAR following Triantis et al. (2012) (see given its area. Hotspots were defined as those ecoregions with
Appendix S1 in Supporting information). Recent attempts to the highest residuals. We ranked ecoregions according to their
model PDAR only used the power model (Morlon et al., 2011) averaged residuals: the higher the residuals, the higher the con-
but, given the uncertainty regarding the shape of PDAR and centration of biodiversity in the ecoregion. Note that ranking in
FDAR, we tested a large spectrum of models. These models were terms of original or standardized curve/observed diversity gives
chosen because they vary in form (e.g. sigmoid or convex, exactly the same results because standardization is linear (see
including asymptotic relationships) and complexity (two to four Appendix S2). We also derived an averaged rank across SR, PD
parameters). and FD hotspots to provide an integrative definition of a
hotspot by summing up the ranking for each ecoregion across
the biodiversity facets (i.e. SR, PD and FD).
Model fitting
We constructed 117 datasets (9 indices × 13 biomes) and fitted Impact of DAR shape on hotspot lists
19 models to each dataset, for a total of 2223 DARs. We carried
We investigated whether PDARs and FDARs were different
out our analyses using another dataset that also adds an ‘arti-
enough from corresponding SAR to deeply modify the hotspot
ficial’ point of null diversity and null area (0.001 and 0.001 to
rankings. In other words we wanted to test whether PDARs/
avoid computing problems).
FDARs are needed to define hotspots or if SAR is a good proxy
Models were fitted using nonlinear regression with minimi-
for FDAR/PDAR when defining hotspots. SAR, PDAR and
zation of the residual sum of squares. Models were further
FDAR were directly comparable thanks to the standardization
evaluated by examining the normality and homoscedasticity of
procedure explained above (they are all expressed as a propor-
residuals. To do so, we applied the Lilliefors’s test for normality
tion of the maximal diversity predicted for the largest ecoregion
and a Pearson correlation between squared residuals and
and thus vary between 0 and 100%). We computed the differ-
area for homoscedasticity. Previous studies (e.g. Guilhaumon
ence between the standardized PD/FD in each ecoregion and the
et al., 2008) considered a model valid when the P-value associ-
proportion of diversity predicted by the area using the SAR (and
ated with the normality and homoscedasticity tests exceeded the
not PDAR/FDAR as previously done) and ranked these differ-
arbitrary threshold of 5%. All DAR analyses were carried out
ences to compute lists of hotspots. Then, we compared the con-
using an updated version of the ‘mmSAR’ package (Triantis
gruence between PD/FD hotspot lists derived from SAR and the
et al., 2012) for the R statistical and programming environment
‘natural’ PD/FD hotspot lists derived from the PDAR/FDAR (as
(R Development Core Team, 2010).
explained in the previous section). If SARs correctly model the
scaling of PD/FD with area, the lists of hotspots should be very
Model averaging similar. In this case, SARs would be well suited to direct model-
For each dataset, we discriminated between different models ling of the spatial scaling of PD/FD to define hotspots and it
using an information-theory framework designed to evaluate would not be necessary to construct explicit PDAR/FDAR.
multiple working hypotheses (Burnham & Anderson, 2002).
The AIC can be used to evaluate the goodness of fit of different R E S U LT S
non-nested models on a given dataset. The weights of evidence We start first by reporting the general results of the statistical
were then derived from the AIC values to evaluate the relative procedures related to the DAR estimations and then by describ-
likelihood of each model given the data and the set of models ing the outcomes of this procedure for the hotspot lists.
(Burnham & Anderson, 2002). Using these weights we derived
averaged DARs for each biome and each diversity index. DAR modelling
Model standardization and comparison Convergence, homoscedasticity and normality
For each DAR, we divided each predicted diversity value by that One of the 19 models showed unrealistic fits (Epm2, see Appen-
of the largest ecoregion in the considered biome in order to dix S1) and was not considered in the analysis. Of the remaining
2106 model fits (13 biomes × 18 models × 9 indices), 1895 (90%) markedly across biomes and diversity indices and revealing sub-
converged. Amongst the different indices, models fitting stantial levels of uncertainty with different models showing
Rao-based DAR showed the highest non-normality of residuals equivalent levels of support (see Appendix S4).
(homoscedasticity was not the limiting factor; results not
shown). Indeed at the 1% level test of homoscedasticity and
Model shape
normality of the residuals, 53, 68 and 75% of the models were
valid for the Rao-, Allen- and Faith-based indices, respectively. To illustrate the difference between the rate of increase in SAR
and FDAR/PDAR, we plotted the difference between predicted
PDAR/FDAR and the corresponding predicted SAR for four
biomes that cover the latitudinal gradient (Fig. 1, Appendix S5).
Relative model fit
The starting value of the curve was zero in most cases, while
The variation in diversity indices explained by area was generally differences between PDAR/FDAR tended to zero as area
high (the median R2 of the best function in each dataset was 0.5; increased. This means that PDAR/FDAR and SAR have the same
see Appendix S3) but was quite variable. The R2 of the best proportion of diversity when area tends to zero (generally it was
model for each dataset ranged from R2 = 0.0001 (asymptotic 0% of maximum diversity) and also end at the same point
model fitting SR in Montane grasslands and shrublands) to because of the standardization (their respective maximum
R2 = 0.95 (the P2 function fitting Raocor PD in temperate coni- 100%). In the intermediate area between the two extremes,
ferous forest; see Appendix S3). No single best model out- PDAR and FDAR were in general higher than SAR (i.e. a positive
performed across all data sets, with model selection varying difference), indicating that PDAR and FDAR reached their
PDARíSAR FDARíSAR
0.6
Relative Div.
Tundra
0.4
0.4
0.2
0.2
0
0 50 180 1000 0 50 180 1000

Temperate Forest
0.6
Relative Div.
0.4
0.4
0.2
0.2
0
0 40 100 800 0 40 100 800

Figure 1 Differences between predicted
phylogenetic diversity–area relationship
Medit. Forest
(PDAR)/functional diversity–area
Relative Div.
relationship (FDAR) values and

0 0.15 0.35
corresponding predicted species–area

relationship (SAR) values. Rows
0 0.15
correspond to different biomes, while

columns represent differences between
0 20 50 340 0 20 50 340
diversity–area relationship (DAR):
PDAR–SAR and FDAR–SAR. For
Trop. moist Forest
0.6
0.6
each plot, the differences between

PDAR/FDAR and SAR are represented
Relative Div.
0.4
0.4
for three values of q: 0 (Faithcor index), 1

(Allencor index) and 2 (Raocor index).
0.2
0.2
Positive differences mean that PDAR or

FDAR are higher than SAR. Area is given
0
in km2. Trop moist Forest, tropical moist 0 40 100 700 0 40 100 700
forest; Medit. F., mediterranean forest; Area*1000km2 Area*1000km2
Relative Div., relative diversity. q=0 (Faithcor) q=1 (Allencor) q=2 (Raocor)
F. Mazel et al.
maximum diversity faster than SAR. This difference increased

DISCUSSION
with the q parameter defining the weight given to species cov-
erage in the diversity indices (Faithcor to Raocor). PDAR and We found considerable geographical mismatches between global
FDAR had a similar shape in most cases. Results were qualita- mammal hotspots of SR, PD and FD and, quite importantly,
tively equivalent when fitting DARs without artificial zeros found that the magnitude of the mismatches depends on the
except when area tended to zero: PDAR/FDAR started at a rela- index considered, which highlights the importance of consider-
tively higher percentage of diversity than SARs and thus the ing a variety of indices (Huang et al., 2012). Mismatches were
difference between PDAR/FDAR and SAR curves tended to start higher with Rao-based indices (Raocor), lower when using the
with positive values for some biomes (see Appendix S5). Faithcor indices and in between for the Allencor indices, whatever
the facet considered. This is not entirely surprising given the
correlation between SR and PD/FD (high with Faithcor, medium
with Allencor and weak with Raocor).
Functional and phylogenetic hotspots
Rodrigues et al. (2011) have already pointed out a high
We extracted residuals (i.e. observed minus predicted diversity) congruence between Faithcor PD hotspots and SR hotspots. As a
from each averaged DAR and ranked them to define hotspots of result, they concluded that incorporating phylogenetic infor-
diversity. As an example, we mapped diversity ranks for tropical mation is not a major concern in conservation. Nevertheless,
moist forests (Fig. 2; but also see Appendix S6 for all biomes and incorporating relative species coverage into the definition of
indices) considering Allencor PD and FD hotspots as well as the multifaceted hotspots alters this conclusion. Faithcor indices do
traditional SR hotspots. SR rankings were relatively well distrib- not incorporate species abundance or coverage and give equal
uted in the three continents whereas PD Allencor hotspots were weight to rare and dominant evolutionary history in a given
much more concentrated in the Afrotropics (and Central location (Chao et al., 2010). However, it seems appropriate to
America) or in the Afrotropical and Indomalaysian realms for give less weight to particular evolutionary histories (i.e. particu-
FD Allencor hotspots. Interestingly, when focusing on the five lar branch paths) that are rare in a given ecoregion because
hottest hotspots for this biome (Table 2), two important results they are less representative than a widespread species in this
emerged: (1) the list of SR hotspots shared few ecoregions with ecoregion. Allencor and Raocor indices give more weight to a given
the lists of Allencor PD, FD and integrative hottest hotspots (i.e. branch if it is long and well represented in an ecoregion. For
two, one and three ecoregions, respectively); and (2) the hottest instance, hotspots defined using PD Raocor are mostly concen-
FD and PD hotspots shared only two ecoregions. trated in the Australasian realm because of the presence of
The same hotspot mismatches were found across all biomes marsupials. This group has a unique evolutionary history since
(Fig. 3). For example, with the cut-off point for defining a they diverged 147 million years ago from placentals (extant
hotspot set at the 5% richest ecoregions we found that congru- eutherians, containing the majority of mammals) and are widely
ence ranged from 5% (FD Raocor hotspots versus SR hotspots) distributed (i.e. have large coverage) through the Australasian
to 74% (PD Faithcor hotspots versus SR hotspots). Interestingly, ecoregions (and not in South American ecoregions). These
when compared with hotspots defined with SR, hotspots results are congruent with those of a recent study revealing
defined with the Faithcor index strongly matched, while those important mismatches between global hotspots of mammal
defined with Raocor strongly mismatched; those defined with trait variance and SR (Huang et al., 2012). Although these
Allencor fell in between. In other words, the hotspot rankings authors used a different approach (they used grid cells as geo-
were significantly correlated – but were not equal – across dif- graphical units and did not use information about species cov-
ferent indices (see Appendix S7). These differences were robust erage), these close results are probably explained by the fact that
against the threshold used to define valid DAR models (i.e. Raocor indices are linked to a measure of variance (Pavoine &
the P-value threshold used to reject a model based on the Bonsall, 2011). We also showed that the use of body mass alone
non-normality and/or homoscedasticity of its residuals; see to define FD hotspots is not sufficient to match the FD hotspots
Appendix S8) due to the weak influence of this threshold on the defined with our complete set of traits, but it still represents
definition of hotspots (see Appendix S9). We also explored to an acceptable approximation. We also showed that PD and FD
what extent the use of multiple traits influences the definition of hotspots are not always congruent, suggesting that PD is not
hotspots. We show that FD hotspots lists based on body mass necessarily a good surrogate for FD (at least for the functional
only differ from FD hotspots defined with our complete set of traits selected here).
traits (Appendix S9). As well as defining hotspots, DARs have been shown to be
On average, using SAR instead of PDAR/FDAR to define useful in both applied and fundamental ecology. We found that
PD/FD hotspots marginally modified the hotspot list (Appendix Faithcor PDAR and FDAR generally reach their maximum faster
S10). However, it turns out that there is still high variability than SAR (Cumming & Child, 2009). This result was expected,
between biomes. For some of these, using SAR instead of PDAR/ since Faithcor PD and FD explicitly account for redundancy
FDAR dramatically changes the hotspot lists. Note also that between species while SR does not. More specifically, it is pos-
the nonlinear fit of the power model alone gave fairly similar sible that small sample areas already contain a broad set of
results to those obtained when using model averaging to define phylogenetic history and FD (e.g. a mouse and an elephant),
hotspots (Appendix S11). whereas large sample areas contain relatively more redundant
1A. Maps of the averaged ranks 1B. SAR
2A. Maps of the averaged ranks 2B. PDAR
3A. Maps of the averaged ranks 3B. FDAR
Ranks
1 223
Hotspots Coldspots
Figure 2 Taxonomic, phylogenetic and functional mammal hotspot selection for tropical moist forests. For each biodiversity facet
(1, species richness; 2, phylogenetic diversity (Allencor PD); and 3, functional diversity (Allencor FD)) a map (a) and a diversity area
relationship (b) are presented. Graphs (b) represent the species–area relationship (SAR), phylogenetic diversity–area relationship (PDAR)
and functional diversity–area relationship (FDAR). Model fits are shown with a coloured curve (see legend) and the averaged fit is
presented in black. Red circles indicate hotspots, the larger the diameter, the higher the ranking. Maps (a) represent the derived ranks from
the residuals of the averaged model presented in (b).
F. Mazel et al.
Table 2 The five hottest hotspots of

Rank Ecoregions Area (km2) REALM tropical and subtropical moist broadleaf
forest.
Traditional hotspots (SR)
1 Albertine Rift montane forests 103,403 AT
2 East African montane forests 65,199 AT
3 Eastern Panamanian montane forests 3031 NT
4 Atlantic Coast restingas 7850 NT
5 Mount Cameroon and Bioko montane forests 1141 AT
Phylogenetic hotspots (Allencor PD)
2 Knysna–Amatole montane forests 3061 AT
3 Peninsular Malaysian peat swamp forests 3610 IM
4 Eastern Panamanian montane forests 3031 NT
5 Chimalapas montane forests 2077 NT
Functional hotspots (Allencor FD)
1 Knysna–Amatole montane forests 3061 AT
3 KwaZulu–Cape coastal forest mosaic 17,779 AT
4 Southern Zanzibar–Inhambane coastal forest mosaic 146,463 AT
5 Eastern Arc forests 23,556 AT
Integrative hotspots (Allencor PD and FD and SR)
2 Eastern Arc forests 23,556 AT
3 East African montane forests 65,199 AT
4 Albertine Rift montane forests 103,404 AT
5 Peninsular Malaysian peat swamp forests 3610 IM
AT, Afrotropics; IM, Indomalaysian; NT, Neotropics; PD, phylogenetic diversity; FD, functional
diversity; SR, species richness. Allencor PD and FD correspond to modified version of Allen entropy.
species (e.g. several species of mice) and thus PDAR/FDAR This result suggests that the evolutionary history or functional
reach their maximum faster than SAR. traits of well-represented taxa are relatively more rapidly
Morlon et al. (2011) obtained a similar result for PDAR on sampled when area increases. For example, branches of major
nested Mediterranean plant communities ranging from 6.25 to mammal lineages (e.g. bats, rodents or carnivores) are probably
400 m2 of spatial extent. They used a power law (see Appendix already well sampled in small ecoregions and thus PD or FD
S1) to model PDAR and SAR and found that the rate of increase reach their maximum faster than TD in larger sample areas. It
in Faith PD with area (zPDAR) was slower that in SR (zSAR). When follows that well-represented functional/phylogenetic biodiver-
standardizing DARs, PDAR is above SAR if zPDAR < zSAR. They sity might be robust to habitat loss, a point that is not detected
showed that protected areas in Australian mediterranean-like when considering all lineages having the same coverage.
regions (representing 13% of the regions) capture 72% of PD, Although SARs have been thoroughly investigated (Scheiner,
but only 56% of SR, indicating that PDAR accumulates total 2003), we have shown that there is not a single best model that
diversity faster than SAR. fits all the data. Thus the automatic use of a single model (tra-
Our results show that if only a fraction of the total biome area ditionally the linear version of the power model) is not justified.
is protected, the percentage of remaining PD (compared with Conversely, to date PDAR and FDAR have been subject to very
the initial PD) will be higher than the percentage of remaining little investigation (but see Cumming & Child, 2009; Morlon
species. If we consider that PD or FD are better predictors of et al., 2011; Wang et al., 2011; Helmus & Ives, 2012). Here, given
ecosystem functioning, resistance or resilience (Cadotte et al., the important variability across biomes and indices, we also
2009; Gravel et al., 2012) than SR, it means that ecosystem show that a single best model does not exist for PDAR and
features might be more robust to species loss than previously FDAR. Nevertheless the model-averaging framework allows
predicted (but see Mouillot et al., 2013). these uncertainties to be taken into account and we used an
We also found that a key feature of a comprehensive measure averaged prediction to remove the area effect on PD/FD. We also
of diversity is that when rarely represented evolutionary history asked whether the averaged SAR could be a good proxy of the
is progressively removed (i.e. using different values of q), the averaged PDAR/FADR to remove this area effect to define
differences between PDAR/FDAR and SAR increase. In other PD/FD hotspots. We demonstrated that there is a notable dif-
words, PD/FD of abundant lineages reaches its maximum faster ference between PD/FD hotspot lists defined using PDAR/FDAR
than when considering all lineages having the same coverage. and those defined using SAR, suggesting that the construction
SR Vs. PD SR Vs. FD PD Vs. FD SR Vs. Int.
100
100
100
100
Faith
50
50
50
50
0
0
5 50 100 5 50 100 5 50 100 5 50 100
100
100
100
100
% Similarity
Allen
50
50
50
50
0
0
5 50 100 5 50 100 5 50 100 5 50 100
100
100
100
100
Rao
50
50
50
50
0
0
5 50 100 5 50 100 5 50 100 5 50 100
% of ecoregions defined as hotspots
Figure 3 Relationships between the threshold used to define hotspots (expressed in percentage of ecoregion defined as a hotspot) and the
similarity between corresponding hotspot lists. From the left to the right columns we compared species richness and phylogenetic diversity
hotspots (SR Vs. PD, species richness and functional diversity hotspots (SR Vs. FD), phylogenetic and functional diversity hotspots (PD Vs.
FD), species richness and integrative hotspots (agreement between the three facets, SR Vs. Int.). From the top to the bottom row we used
Faithcor, Allencor and Raocor as PD and FD. The dark continuous line represents the mean percentage of congruence of hotspot lists averaged
across biomes; the shaded polygon is the associated standard error of the mean. The relative congruence among hotspot lists of two
biodiversity facets was determined as the number of ecoregions identified as hotspots by both, divided by the total number of ecoregions
in a group.
of PDAR/FDAR is required to define functionally or phylo- coarse-scale assessment of the conservation value of different
genetically based hotspots and that SAR alone cannot be used regions (Lamoreux et al., 2006), several challenges would need
for this purpose. to be addressed before our results could be directly transferred
We constructed DARs using a particular experimental design into conservation planning actions.
(Scheiner, 2003) but we are aware that all methods for con-
structing DARs have their own drawbacks and we suggest that
ACKNOWLEDGEMENTS
the next challenge in the study of large-scale multifaceted DARs
is to test different methodological designs. For example, the We thank J. Lawler, G. Cumming and an anonymous referee,
strictly nested design (SNQ) of Storch et al. (2012) seems par- who provided useful comments on an earlier version of this
ticularly interesting to analyse. Nevertheless, since our work was manuscript. The research leading to these results received
about delineating hotspots of diversity, we had to construct funding from the European Research Council under the
DARs using a non-overlapping design. European Community’s Seven Framework Programme FP7/
2007–2013 grant agreement no. 281422 (TEEMBIO). M.V.C.,
R.D.L. and J.A.F.D.F. received productivity research grants from
CONCLUSION
CNPq, Brazil. D.M. has received funding from the Marie Curie
Here we used a unified framework for building large-scale DARs International Outgoing Fellowship (FISHECO) with agreement
for each facet of mammal diversity. The spatial scaling of each number IOF-GA-2009-236316. FM, WT and JR belong to the
facet revealed that PD/FD reach their maximal diversity faster Laboratoire d’Écologie Alpine, which is part of Labex OSUG@
than SAR, suggesting that PD/FD might be less vulnerable than 2020 (ANR10 LABX56).
SR to habitat loss. In addition, we extracted the area effect on
the diversity of individual terrestrial ecoregions to identify
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Vienna, Austria. area relationship and functional diversity-area relationship
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Rodrigues, A.S.L., Grenyer, R., Baillie, J.E.M., Bininda-Emonds, mammal hotspots.
O.R.P., Gittlemann, J.L., Hoffmann, M., Safi, K., Schipper, J., Appendix S7 Correlation of ranks between facets.
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lian phylogenies aid conservation planning, but not much. hotspots and the congruence between hotspots.
Philosophical Transactions of the Royal Society B: Biological Appendix S9 Robustness of the hotspots lists to choice of
Sciences, 366, 2652–2660. diversity–area relationship model.
Safi, K., Cianciaruso, M.V., Loyola, R.D., Brito, D., Appendix S10 Congruence between functional diversity
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standing global patterns of mammalian functional and Appendix S11 Importance of diversity–area relationship con-
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! "!154!"!
Partie!II!–!Synthèse!
SYNTHÈSE(ET(DISCUSSION(DE(LA(PARTIE(II(
(
! "!155!"!
(
Cette! deuxième! partie! part! du! principe! que! les! diversités! phylogénétiques! et!
fonctionnelles! représentent! des! facettes! importantes! de! la! biodiversité! biologique! et!
qu’elles! doivent! donc! être! prises! en! compte! dans! les! plans! de! conservation.! Elles!
apportent! en! effet! des! informations! uniques! que! la! diversité! spécifique! ne! peut! pas!
représenter!puisque!cette!dernière!ignore!les!différences!entre!espèces!(Vane"Wright!et!
al.! 1991,! Lecointre! 2011).! Les! intérêts! de! leurs! utilisations! sont! d’ordre! éthique!
(Rosauer! and! Mooers! 2013)! et! utilitariste! (Díaz! et! al.! 2007,! Srivastava! et! al.! 2012).! En!
admettant!une!telle!approche,!il!faut!donc!s’attacher!à!comprendre!si!ces!diversités!ont!
les! mêmes! répartitions! et! les! mêmes! comportements! face! aux! changements! globaux.!
Ceci! pourrait! alors! permettre! de! confirmer! les! plans! de! conservation! actuels! si! les!
facettes! sont! congruentes,! c’est"à"dire! que! la! protection! des! espèces! et! de! la! richesse!
spécifique! (le! paradigme! actuel)! permet! dans! le! même! temps! de! protéger! les! autres!
facettes.! Au! contraire,! si! les! facettes! ne! sont! pas! congruentes,! il! faudra! essayer!
d’aménager! les! plans! de! conservation! (par! exemple! la! création! ou! l’extension! d’aires!
protégées)!pour!prendre!en!compte!ces!nouvelles!facettes.!!
!
1.(Évaluer(les(menaces(qui(pèsent(sur(l’arbre(de(la(vie((de(certains(vertébrés)(
!
Les!changements!globaux!qui!menacent!la!biodiversité!sont!de!natures!multiples.!
Les!changements!climatiques!par!exemple!semblent!menacer!les!espèces!(Thomas!et#al.!
2004;!Thuiller!et#al.!2005;!Bellard!et#al.!2012).!Il!a!ainsi!été!récemment!montré!que!de!
tels!changements!pouvaient!aussi!avoir!des!effets!négatifs!sur!la!PD!(Thuiller!et!al.!2011)!
et! sur! la! FD! (Thuiller! et! al.! 2014).! La! destruction! et! la! fragmentation! de! l’habitat!
représentent! aussi! une! menace! majeure! pour! la! biodiversité.! Morlon! et#al.! (2011)! ont!
ainsi! proposé! d’utiliser! la! PDAR! pour! estimer! la! perte! de! PD! consécutive! à! la! perte!
d’habitat.!!
!
1.1.(Apport(de(l’analyse(
!
En!utilisant!cet!outil,!nous!avons!montré!qu’à!l’échelle!continentale!la!PD!est!plus!
robuste!à!la!perte!d’habitat!que!la!SR.!Cette!découverte!n’est!en!fait!pas!nouvelle!mais!
nous! le! quantifions! pour! la! première! fois! à! cette! échelle.! En! particulier,! nous!
! "!156!"!
développons!un!modèle!nul!qui!permet!de!différencier!l’effet!de!la!forme!de!l’arbre!(et!
donc! de! «!l’assurance!»! que! représentent! les! branches! internes,! voir! l’article! fondateur!
de!Nee!&!May!,1997)!de!l’effet!de!la!distribution!spatiale!de!la!PD.!Nous!montrons!pour!
la!première!fois!que!les!deux!processus!sont!importants.!
!
1.2.(Limites(de(l’analyse(
!
Notre!analyse!est!cependant!assez!simplifiée!et!plusieurs!limites!sont!à!noter.!!
!
(1)!Tout!d’abord!notre!échelle!d’étude!est!déconnectée!des!échelles!de!destruction!et!de!
fragmentation! de! l’habitat,! qui! sont! souvent! inférieures! à! notre! grain! minimal! de!
110*110! km.! Cependant,! le! développement! de! l’indice! de! robustesse! relative! de! la! PD!
ainsi!que!notre!approche!du!modèle!nul!peuvent!être!théoriquement!appliqués!à!toutes!
les!échelles!spatiales,!démontrant!l’intérêt!de!notre!analyse.!!
!
(2)! Nous! faisons! l’hypothèse! que! toutes! les! espèces! sont! également! vulnérables! à! la!
perte! d’habitat,! ou! que! les! extinctions! sont! aléatoires! dans! la! phylogénie.! Cette!
hypothèse!est!en!fait!loin!d’être!vérifiée!et!il!semble!plutôt!que!les!risques!d’extinction!
montrent!un!signal!phylogénétique!(Purvis!2000,!2008).!Ceci!peut!être!un!effet!indirect!
du! signal! phylogénétique! que! montrent! certains! traits! liés! au! risque! d’extinction,! par!
exemple!la!masse!moyenne!de!l’espèce!(Fritz!et!al.!2009).!On!notera!cependant!que!les!
risques! d’extinction! liés! aux! changements! climatiques! ne! semblent! pas! impacter! de!
façon!disproportionnée!la!diversité!phylogénétique!(Pio!et!al.!2011,!Thuiller!et!al.!2011).!
!
(3)!Enfin,!l’utilisation!de!la!relation!aire"espèce!pour!prédire!les!taux!d’extinction!reste!
controversée!(May!et!al.!1995,!Lewis!2006,!He!and!Hubbell!2011,!Matias!et!al.!2014).!En!
particulier,!il!n’y!a!pas!de!raison!a!priori!que!l’on!puisse!inverser!le!SAR!pour!produire!
des! estimations! des! taux! d’extinctions! (notamment! car! il! s’est! construit! sur! des! temps!
évolutifs!longs!or!on!l’applique!sur!des!temps!courts).!Par!ailleurs,!la!perte!d’habitat!(1)!
n’est! jamais! totale! mais! peut! simplement! représenter! une! modification,! et! (2)! n’est!
jamais!uniforme!mais!peut!prendre!des!formes!complexes.!En!définitive,!l’application!du!
SAR!est!donc!limitée!mais!reste!pourtant!un!des!seuls!outils!disponibles.!!
!
! "!157!"!
2.(Les(différentes(facettes(de(la(diversité(sontNelles(congruentes(et(également(
protégées(?(
!
2.1(Les(points(chauds(:(des(aires(à(conserver(?(
!
Quelques! études! commencent! à! montrer! que! les! différentes! facettes! de! la!
biodiversité!ne!sont!pas!congruentes.!C’est!le!cas!pour!les!oiseaux!à!l’échelle!de!la!France!
(Devictor! et! al.! 2010),! les! vertébrés! à! l’échelle! de! l’Europe! (Zupan! et! al.! 2014)! ou! les!
poissons!à!l’échelle!du!monde!(Stuart"Smith!et!al.!2013).!Cependant,!une!telle!étude!n’a!
pas! été! menée! à! l’échelle! du! globe! pour! les! mammifères! terrestres.! Nous! développons!
une!telle!analyse!et!montrons!que!les!différentes!facettes!ne!sont!pas!congruentes!entre!
elles,! mais! ceci! dépend! de! l’indice! de! diversité! phylogénétique! ou! fonctionnelle!
considéré.! Nous! comparons! en! fait! trois! indices! de! diversité! fonctionnelle! et!
phylogénétique! à! la! richesse! spécifique.! Ces! trois! indices! proviennent! du! cadre!
méthodologique!proposé!par!Chao!et#al.!(2010)!et!sont!censés!représenter!des!mesures!
de! diversité! (phylogénétique! ou! fonctionnelle)! étalées! sur! un! continuum! d’importance!
donnée!à!l’abondance!des!espèces.!En!effet,!les!indices!sont!unifiés!par!les!nombres!de!
Hill! (Hill! 1973)! et! se! définissent! tous! avec! une! même! formule! qui! dépend! d’un!
paramètre!q.#Ce!paramètre!est!censé,!selon!les!auteurs,#faire!varier!le!poids!donné!aux!
espèces!rares.#Ainsi!le!premier!indice!(q=0,!PDFaith)!n’est!pas!sensible!à!l’abondance!alors!
que!le!troisième!(q=2,!Rao!QE)!donne!un!poids!important!aux!espèces!abondantes.!Nous!
proposons!d’utiliser!le!couvert!relatif!de!chaque!espèce!dans!chaque!écorégion!comme!
mesure! «!d’abondance!».! Ainsi! l’indice! censé! donner! plus! de! poids! aux! espèces!
abondantes! va! quantifier! la! diversité! phylogénétique! (ou! fonctionnelle)! qui! est!
représentée! de! façon! importante! dans! une! écorégion! alors! que! l’indice! insensible! aux!
abondances! (q=0)! donnera! un! poids! identique! à! toutes! les! abondances.! Nous! voulons!
ainsi!tester!si!le!couvert!relatif!de!chaque!espèce!dans!les!écorégions!impacte!la!nature!
des!points!chauds.!Dans!l’article,!nous!concluons!par!l’affirmative!puisque!l’indice!à!q=0!
est!très!proche!de!la!SR!alors!que!l’indice!q=2!est!très!fortement!découplé!de!SR.!!
!
Note#importante#sur#les#indices#utilisés#dans#l’article#
En! fait,! je! me! suis! rendu! compte! au! cours! de! ma! thèse! que! le! cadre!
méthodologique! proposé! par! Chao! et# al.! (2010),! bien! qu’apparemment! très! élégant!
! "!158!"!
mathématiquement,! était,! d’une! certaine! façon,! un! peu! trompeur.! L’interprétation! des!
indices! proposée! par! ces! auteurs! me! paraît! incomplète.! Ils! expliquent! en! effet! que! le!
paramètre!q!de!leur!cadre!méthodologique!fait!uniquement!varier!l’importance!donnée!
aux!abondances!relatives!des!espèces.!Ceci!paraît!discutable.!En!effet,!si!ce!paramètre!ne!
faisait! varier! que! l’importance! de! l’abondance,! l’utilisation! des! données! de!
présence/absence! (c’est"à"dire! sans! information! d’abondance)! devrait! conduire! à!
retrouver!les!mêmes!indices,!peu!importe!la!valeur!de!q!(voir!Chen!et#al.!2012!pour!un!
raisonnement! similaire! et! le! matériel! supplémentaire! 1! de! l’article! 2! pour! une!
justification!plus!précise).!Ceci!ne!semble!pas!être!vérifié.!En!effet!nous!montrons!dans!
le! chapitre! I! que! PDFaith! (q=0)! est! un! indice! de! richesse! alors! que! Rao! QE! (q=2)! est! un!
indice!de!divergence.!Ces!indices!ne!sont!donc!a!priori!pas!comparables!en!soi!et!le!cadre!
méthodologique!de!Chao!est!donc!à!réinterpréter!:!le!paramètre!q!impacte!effectivement!
le!poids!donné!aux!abondances!mais!aussi!la!dimension!de!la!structure!phylogénétique!
décrite.!En!ce!sens,!l’interprétation!consistant!à!dire!que!les!différents!résultats!trouvés!
pour! différentes! valeurs! de! q! proviennent! de! différences! d’abondances! est! incomplète.!
Je!note!que!ceci!est!particulièrement!alarmant!pour!les!études!fondamentales!essayant!
d’expliquer!les!processus!responsables!de!l’assemblage!des!communautés.!!
!
Réinterprétation#et#discussion#des#résultats.#
#
Mais!en!quoi!cette!découverte!impacte"t"elle!notre!analyse!des!points!chauds!de!
biodiversité?!
En! fait,! nous! montrons! donc! que! les! points! chauds! de! richesse! phylogénétique!
sont!très!proches!(mais!pas!identiques)!de!ceux!de!richesse!spécifique.!Ceci!est!cohérent!
avec!les!résultats!de!Rodrigues!et#al.!(2011)!et!montrent!que!les!deux!facettes!sont!très!
congruentes.! Néanmoins! notre! étude! ne! prend! pas! en! compte! la! complémentarité! de!
richesse! phylogénétique! entre! les! sites! (voir! Margules! &! Pressey! 2000;! Rodrigues! &!
Gaston! 2002)! et! ne! peut! donc! pas! directement! être! utilisée! en! conservation.! Ainsi,! les!
points! chauds! ne! représentent! pas! nécessairement! des! zones! à! conserver! absolument!
car! elles! sont! potentiellement! redondantes.! Cependant,! notre! analyse! constitue! un! pas!
intéressant!dans!la!comparaison!des!facettes!de!la!biodiversité.!Un!aspect!novateur!de!
notre!étude!est!qu‘elle!compare!différentes!dimensions!de!la!structure!phylogénétique!
des! assemblages! (voir! Chapitre! 1).! Ainsi,! Rao! QE! représente! une! divergence!
! "!159!"!
phylogénétique!ou!fonctionnelle!et!nous!montrons!que!cette!dimension!est!découplée!de!
la! richesse! spécifique.! En! quoi! une! telle! mesure! de! diversité! est"elle! importante! en!
conservation!?! L’indice! de! choix! en! conservation! est! généralement! la! richesse! (qu’elle!
soit! phylogénétique,! fonctionnelle! ou! spécifique)! car! elle! représente! une! quantité! qu’il!
est!aisé!de!maximiser!dans!le!cadre!d’une!recherche!d’aire!à!protéger.!En!revanche,!les!
indices! de! divergence! ont! des! comportements! très! inattendus! en! conservation! si! l’on!
désire! les! maximiser.! En! effet,! l’ajout! d’une! espèce! dans! un! assemblage! peut! faire!
diminuer! la! valeur! de! l’indice,! ce! qui! est! totalement! contre"intuitif! en! conservation!!!
Cependant,!je!pense!que!de!tels!indices!peuvent!être!extrêmement!intéressants,!et!cela!
pour!différentes!raisons.!
!
(1) Dans! le! cadre! d’un! objectif! de! représentativité! (Margules! and! Pressey! 2000,!
Ladle!and!Whittaker!2011),!les!indices!de!divergences!peuvent!nous!renseigner!
sur! les! assemblages! évolutivement! uniques,! par! exemple! les! musées!
(rassemblant! des! espèces! «!anciennes!»)! ou! les! berceaux! de! la! vie! (centres! de!
diversification),!ce!que!ne!peuvent!pas!faire!les!indices!de!richesse!(Devictor!et!
al.! 2010,! Stuart"Smith! et! al.! 2013,! Zupan! et! al.! 2014).! Je! note! ici! que! les! points!
‘froids’! de! divergence! phylogénétique! représentent! donc! potentiellement! des!
berceaux!de!diversité!mais!que!je!ne!les!ai!pas!pris!en!compte!dans!l’analyse.!!
!
(2) Dans! le! cadre! d’un! objectif! utilitariste! nous! avons! vu! en! introduction! que! la!
diversité! fonctionnelle! (ou! phylogénétique)! pouvait! potentiellement! être! un!
meilleur! prédicteur! du! fonctionnement! des! écosystèmes! et! donc! de! leurs!
services.!En!fait!la!divergence!fonctionnelle!est!effectivement!un!indice!de!choix!
(Lavorel! et! al.! 2007).! Il! est! donc! intéressant! de! montrer! que! de! tels! indices! ne!
sont!pas!congruents!avec!la!richesse!spécifique.!!
!
Nous!avons!montré!qu’il!existe!un!découplage!entre!les!différentes!facettes!de!la!
diversité! de! certains! vertébrés! alors! que! la! plupart! du! fonctionnement! et! surtout! des!
services!des!écosystèmes!sont!assurés!par!les!producteurs!primaires!comme!les!plantes!
et! les! décomposeurs! comme! les! champignons.! Ainsi,! il! semble! qu’il! existe! un! certain!
découplage! entre! notre! analyse! et! sa! justification! dans! le! cadre! du! maintien! du!
fonctionnement! des! écosystèmes! et! de! leurs! services.! Néanmoins,! plusieurs! fonctions!
! "!160!"!
essentielles! semblent! être! assurées! par! les! tétrapodes! en! général! (mammifères! mais!
aussi! oiseaux,! voir! Sekercioglu! et! al.! 2004,! Wenny! et! al.! 2011,! Luck! et! al.! 2012).! Par!
exemple,! certaines! espèces! permettent! la! dispersion! des! graines! et! la! pollinisation! de!
certaines!espèces!végétales!(Sekercioglu!2011)!alors!que!d’autres!peuvent!façonner!les!
paysages! (les! espèces! «!ingénieurs!»).! Aussi,! il! est! généralement! admis! que! la!
perturbation! d’un! seul! niveau! trophique! peut! avoir! des! effets! importants! pour!
l’écosystème!dans!son!ensemble!(voir!Daskin!et#al.!(2015)!pour!un!exemple!récent).!En!
particulier,! les! modifications! de! la! structure! des! niveaux! trophiques! supérieurs!
(herbivores! et! prédateurs)! peuvent! avoir! des! conséquences! en! cascade! sur! tous! les!
niveaux! de! la! chaine! alimentaire! (Schmitz! et! al.! 2000,! Shurin! et! al.! 2002,! Myers! et! al.!
2007).! Ainsi,! notre! analyse! représente! un! premier! pas! vers! l’inclusion! des! facettes!
fonctionnelles! de! la! biodiversité! en! conservation! mais! ne! représente! pas! un! outil!
directement!utilisable!si!l’on!veut!inclure!les!relations!trophiques.!!
!
!
2.2(Les(aires(de(protection(préservent(elle(les(arbres(de(la(vie?(
!
Les!points!chauds!de!biodiversité!son!des!éléments!importants!en!biologie!de!la!
conservation! (même! si! leur! définition! précise! est! sujette! à! débat,! Rodrigues! 2013).!
Cependant,! il! ne! sont! pas! directement! utilisables! en! conservation,! contrairement! aux!
approches! de! conservation! systématique! (Margules! and! Pressey! 2000).! Ces! approches!
permettent! de! créer! des! espaces! protégés! pour! répondre! à! des! critères! précis! pré"
établis!(par!exemple!représentativité,!complémentarité).!Dans!le!cadre!de!la!protection!
de!la!diversité!à!plusieurs!facettes,!il!s’agit!donc!dans!un!premier!temps!de!tester!si!les!
aires! de! protection! existantes! protègent! ou! non! les! diversités! fonctionnelles! et!
phylogénétiques.!C’est!ce!que!nous!avons!fait!à!l’échelle!de!l’Europe!pour!les!tétrapodes!
(mammifères,! oiseaux,! squamates! et! amphibiens,! voir! Annexe! 1.3).! Une! analyse! de!
trouée! (‘gap! analysis’)! nous! permet! d’estimer! dans! quelle! mesure! l’organisation!
géographique! des! aires! de! protection! actuelle! (parcs! et! réserves! nationales! et! réseau!
Natura! 2000)! coïncident! avec! la! distribution! des! espèces,! et! en! particulier! celle! des!
espèces! rares.! En! effet,! nous! définissons! dans! un! premier! temps! le! pourcentage! de!
distribution!(‘objectif!de!protection’)!permettant!d’assurer!le!maintien!d‘une!espèce.!Ce!
pourcentage!est!définit!en!fonction!de!la!taille!de!l’aire!de!distribution!:!ainsi!une!espèce!
! "!161!"!
rare!aura!un!objectif!de!protection!de!100%!alors!qu’une!espèce!très!répandue!aura!un!
objectif! inférieur.! Ensuite,! nous! calculons! la! différence! (le! ‘gap’)! entre! l’objectif!
théorique!et!la!réalité!de!terrain!(réalisation!de!l’objectif!de!protection,!qui!oscille!entre!
30!et!50%!selon!les!groupes!de!notre!étude).!Nous!évaluons!ensuite!dans!quelle!mesure!
ce! degré! de! protection! des! espèces! se! répercute! sur! les! arbres! phylogénétiques! et!
fonctionnels! des! tétrapodes.! Nous! montrons! qu’en! général! l’arbre! fonctionnel! est! bien!
mieux!conservé!que!l’arbre!phylogénétique,!mais!ceci!dépend!du!groupe!étudié.!Ainsi,!il!
semble! important! que! l’extension! future! des! aires! protégées! européennes! tente! de!
maximiser! la! représentation! de! la! diversité! phylogénétique! et/ou! fonctionnelle.! Une!
première!approche!pourrait!par!exemple!utiliser!la!méthodologie!proposée!par!Pollock!
et#al.!(2015)!et!de!l’étendre!au!contexte!global!en!prenant!plusieurs!facettes!de!diversité!
et!plusieurs!groupes!(travail!en!cours!dans!l’équipe!EMABIO).!
!
3.(Perspectives(futures(
!
Nous! montrons! dans! cette! partie! que! les! facettes! phylogénétiques! et!
fonctionnelles! de! la! biodiversité! ne! sont! pas! nécessairement! géographiquement!
congruentes!avec!la!facette!taxonomique.!En!d’autres!termes,!une!focalisation!excessive!
sur! la! protection! d’une! des! facettes! ne! pourra! pas! protéger! les! autres! efficacement.! Si!
l’on!considère!que!ces!trois!facettes!doivent!être!également!protégées,!il!est!alors!urgent!
de!les!incorporer!toutes!les!trois!dans!les!plans!de!conservation.!Cependant,!on!peut!se!
demander!à!quel!point!la!protection!des!trois!facettes!est!indispensable.!Je!rappelle!ici!
que!les!deux!arguments!majeurs!pour!la!protection!de!toutes!les!facettes!peuvent!être!
d’ordre! éthique! ou! d’ordre! utilitariste.! Je! suis! convaincu! que,! d’un! point! de! vue!
purement! éthique,! protéger! la! diversité! fonctionnelle! et! surtout! la! diversité!
phylogénétique!est!essentiel.!D’un!point!de!vue!utilitariste,!la!discussion!me!paraît!plus!
ouverte.! Un! des! arguments! utilitaristes! central! est! de! dire! que! la! perte! de! diversité!
(provoquée! par! l’action! de! l’homme)! va! engendrer! des! dysfonctionnement! des!
écosystèmes! (d’où! la! prolifération! des! études! entre! fonctionnement! et! diversité)! et,! à!
terme,! une! diminution! potentielle! des! services.! Cependant,! l’excellente! revue! de!
Srivastava!&!Vellend!(2005)!semble!mettre!en!doute!certains!points!de!ce!raisonnement.!
En! effet,! les! auteurs! montrent! qu’il! existe! un! fossé! important! entre! les! évidences!
empiriques! de! la! relation! diversité"fonctionnement! et! les! attendus,! les! mesures! et! les!
! "!162!"!
moyens! dont! dispose! la! biologie! de! la! conservation.! Une! première! série! de! limites!
provient! du! fait! que! la! diversité! spécifique! ne! permet! pas! de! correctement! décrire! le!
fonctionnement! des! écosystèmes.! Cette! limite! apparaît! justement! contournable! si! la!
diversité! fonctionnelle! est! utilisée! (ou! la! diversité! phylogénétique! si! les! traits! sont!
conservés),! et! c’est! tout! le! sens! de! cette! seconde! partie.! Cependant,! plusieurs! autres!
limites!persistent,!notamment!:!
!
(1) la! perte! de! diversité! semble! être! une! cause! (indirecte)! mineure! du!
dysfonctionnement!des!écosystèmes,!notamment!par!rapport!aux!effets!directs!
(par!exemple,!la!destruction!d’une!forêt).!
(2) les! indices! de! diversité! fonctionnelle! actuels! ne! prennent! en! compte!
qu’indirectement! la! structure! des! réseaux! trophiques! (mais! voir! Poisot! et# al.,!
2012).!
!
Ces!limites!pourront!êtres!dépassées!en!combinant!des!approches!empiriques!et!
des!avancées!théoriques,!je!pense!notamment!à!la!structure!et!la!dynamique!des!réseaux!
trophiques.! En! particulier,! je! considère! qu’il! serait! important! de! mieux! décrire! la!
structure! de! tels! réseaux! (voir! par! exemple! Morales"Castilla! et# al.! 2015),! de! mieux!
comprendre! les! conséquences! de! la! perte! de! certains! maillons! de! la! chaîne! sur! le!
fonctionnement!des!écosystèmes!et!de!mieux!relier!les!indices!de!diversité!fonctionnelle!
et!la!structure!du!réseau.!!
!
! !
! "!163!"!
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!
! "!167!"!
!
!
"!168!"!
!
!
"!169!"!
Partie!III!
PARTIE'III'
'
UTILISER'LES'DIVERSITÉS'
PHYLOGÉNÉTIQUES'ET'
FONCTIONNELLES'POUR'MIEUX''
COMPRENDRE'CERTAINS'PATRONS'
BIOGÉOGRAPHIQUES'
'
'
!
"!170!"!
Partie!III!"!Sommaire!
SOMMAIRE'DE'LA'PARTIE'III'
!
!
Articles'associés'à'la'partie'III' ' ' ' ' ' ' ' 172'
Annexes'associées'à'la'partie'III'' ' ' ' ' ' ' 172'
'
INTRODUCTION'GÉNÉRALE' ' ' ' ' ' ' ' 173'
'
'
III.1.'IMPORTANCE'DE'L’ÉCHELLE'PHYLOGÉNÉTIQUE' ' ' ' 176'
'
INTRODUCTION!SOUS"PARTIE!III.1' ' ' ' ' ' ' 177!
CHAPITRE!V.!L’environnement!et!l’espace!modulent!la!répartition!mondiale!des!
oiseaux!et!des!mammifères!à!différentes!échelles!évolutives! ! ! ! 184!
CHAPITRE!VI.!Le!régime!alimentaire!et!la!phylogénie!de!l’hôte!modulent!
!la!composition!des!micro"biomes!à!différentes!échelles!évolutives! ! ! 198!
SYNTHÈSE!SOUS"PARTIE!III.1! ! ! ! ! ! ! ! 210!
!
!
III.2.'LA'GÉOGRAPHIE'DE'LA'CONVERGENCE' ' ' ' ' 216'
!
INTRODUCTION!SOUS"PARTIE!III.2! ! ! ! ! ! ! 217!
CHAPITRE!VII.!La!convergence!évolutive!des!assemblages!de!mammifères! ! 222!
SYNTHÈSE!SOUS"PARTIE!III.2! ! ! ! ! ! ! ! 238!
!
!
SYNTHÈSE'&'DISCUSSION'GÉNÉRALE'' ' ' ' ' ' 240'
BIBLIOGRAPHIE' ' ' ' ' ' ' ' ' ' 248'
!
"!171!"!
Partie!III!"!Contributions!
ARTICLES'ASSOCIÉS'À'LA'PARTIE'III'
ARTICLE!7!
F.' Mazel,!R.!Wüest,!J.!Renaud,!S.!Lavergne!and!W.!Thuiller.!Decomposing+the+global+beta+
diversity+of+mammals+and+birds+along+a+phylogenetic+scale+reveals+the+differential+effects+of+
space+and+contemporary+climate.!En!préparation!
!
ARTICLE!8!
M.!Groussin*,!F.'Mazel*,!J.!Sanders,!C.!Smillie,!S.!Lavergne,!W.!Thuiller!and!E.!Alm.!
Phylogenetic+decomposition+of+mammalian+gut+microbiota+reveals+the+evolution+of+
community+symbiosis. En!préparation
*!Contribution!égale.!
!
ARTICLE!9!
F.'Mazel,!T.!J.!Davies,!D.!Georges,!S.!Lavergne,!W.!Thuiller!and!P.!R.!Peres"Neto.!Improving+
phylogenetic+regression+under+complex+evolutionary+models.+Accepté!dans!Ecology!
+
ARTICLE!10!
F.' Mazel,! R.! Wüest,! J.! Renaud,! S.! Lavergne! and! W.! Thuiller.+The+global+biogeography+of+
non=neutral+trait+evolution+in+mammals."+En!préparation"
!
!
ANNEXES'ASSOCIÉES'À'LA'PARTIE'III'
!
ANNEXE!3.1.1.!Matériel!supplémentaire!de!l’article!7!
!
ANNEXE!3.2.1.!Article!9!
!
!
"!172!"!
Partie!III!–!Introduction!générale!
'
INTRODUCTION'GÉNÉRALE''
DE'LA'PARTIE'III."
"
"
"
Si!l’on!veut!résumer,!les!grandes!questions!biogéographiques!se!concentrent!sur!:!
!
" la"diversité"α,!notamment!le!gradient!latitudinal!de!diversité!
" la"diversité"β,!notamment!les!variations!de!composition!spécifique!en!fonction!des!
régions!du!monde.!
!
Je!fais!l’hypothèse!que!l’utilisation!des!facettes!phylogénétiques!et!fonctionnelles!
de! la! biodiversité! va! permettre,! en! décrivant! plus! finement! la! structure! des!
assemblages,!de!tester!des!hypothèses!précises!concernant!l’origine!de!ces!deux!grands!
patrons.! J’ai! notamment! donné! un! exemple! d’une! telle! application! pour! la!
compréhension! du! gradient! latitudinal! de! diversité! avec! l’étude! de! Belmaker! &! Jetz!
(2015).! Dans! cette! troisième! partie,! je! vais! en! fait! uniquement! me! concentrer! sur! les!
patrons! de! diversité! β! en! abordant! la! facette! phylogénétique! dans! la! première! sous"
partie! (III.1)! et! en! combinant! les! facettes! phylogénétiques! et! fonctionnelles! dans! la!
deuxième!partie!(III.2).!!
!
Nous! avons! montré! dans! le! chapitre! II! l’intérêt! potentiel! de! l’utilisation! de!
l’échelle!évolutive!pour!mieux!décrire!et!comprendre!les!patrons!biogéographiques.!En!
effet,! il! apparaît! clair! que! différents! processus! peuvent! influencer! la! répartition! de! la!
biodiversité! à! différentes! échelles! évolutives,! et! même! que! des! patrons! opposés!
peuvent! exister! à! différentes! échelles.! Le! chapitre! II! se! concentrait! sur! la! diversité,! α!
mais! il! est! probable! que! de! tels! résultats! soient! observables! avec! la! diversité! β.! Je!
m’attache! donc! à! tester! cette! hypothèse! dans! deux! systèmes! d’études! emboités!:! les!
"!173!"!
!
Partie!III!–!Introduction!générale!
mammifères!à!l’échelle!du!globe!(Chapitre!V)!ainsi!que!les!communautés!bactériennes!
ectosymbiotiques! vivant! dans! l’intestin! de! certains! de! ces! mammifères! (microbiotes*!
intestinaux,!Chapitre!VI).!En!particulier,!je!teste!si!les!processus!liés!à!l’histoire!et!ceux!
liés!à!la!niche!agissent!à!la!même!échelle!évolutive.!
!
L’approche!phylogénétique!précédente!n’explicite!pas!les!différences!fonctionnelles!
entre!les!espèces.!Or,!ces!différences!peuvent!permettre!de!tester!de!façon!plus!robuste!
l’importance!des!processus!de!niche!dans!la!distribution!de!la!biodiversité.!En!effet,!la!
niche!écologique!des!espèces!est!le!reflet!de!phénotypes*!particuliers!qui!sont!adaptés!à!
certaines! conditions! abiotiques! ou! biotiques.! Ainsi,! l’utilisation! des! traits! fonctionnels!
pourrait!permettre!de!mieux!comprendre!l’importance!relative!des!processus!de!niche.!
Dans! cette! deuxième! sous"partie! (Chapitre! VII),! j’utilise! les! traits! fonctionnels! des!
mammifères! pour! tester! leur! relation! "! à! l’échelle! de! la! communauté! "! avec! les!
caractéristiques!environnementales!dans!une!perspective!évolutive.!!
"!174!"!
!
!
!
"!175!"!
Partie!III.1!
!
SOUSVPARTIE'III.1.''
'
L’IMPORTANCE'DE'L’ÉCHELLE'
PHYLOGÉNÉTIQUE'
!
"!176!"!
Partie!III.1!"!Introduction!
!
'
INTRODUCTION'DE'LA'SOUSVPARTIE'III.1'
!
"!177!"!
!
'
'
'
«!The!normal!human!organism!can!be!said!
!to!be!composed!of!over!1014!cells,!of!which!about!10%!are!animal!cells.!»!
Savage,!1977!
'
'
1.'Contexte'
'
'
Les! microbiotes! intestinaux! sont! des! communautés! bactériennes!
ectosymbiotiques!vivant!dans!l’intestin!de!certains!organismes!et!notamment!ceux!des!
mammifères!(Savage!1977).!Ces!communautés!forment!des!systèmes!complexes!qui!se!
révèlent! d’une! importance! capitale! pour! certaines! fonctions! physiologiques!
fondamentales! de! l’hôte,! comme! sa! nutrition! ou! sa! réponse! immunitaire,! et! participe!
donc!à!sa!fitness!(Hooper!&!Gordon!2001;!Bäckhed!et+al.!2005;!Ley!et+al.!2008;!Hooper!et+
al.! 2012).! Par! exemple,! les! (cellules! animales! des)! herbivores! n’ont! pas! les! capacités!
biochimiques! de! digérer! la! cellulose! qui! est! pourtant! le! composant! majeur! de! leur!
régime!alimentaire.!Par!contre,!les!bactéries!de!leur!microbiote!possèdent!quant!à!elles!
les!enzymes!capables!de!métaboliser!ce!sucre.!Ainsi,!l’herbivore!dépend!directement!de!
la! fermentation! assurée! par! son! microbiote! pour! acquérir! les! ressources! nécessaires! à!
sa!survie.!!
!
! Il! m’apparaît! donc! intéressant! de! comprendre! l’évolution! et! la! structure! des!
microbiotes! intestinaux! de! mammifères! tout! autant! que! l’évolution! et! la! structure! des!
assemblages! de! mammifères.! Par! ailleurs,! nous! allons! voir! qu’au"delà! de! cet! aspect!
intégratif,! la! biogéographie! et! l’étude! des! microbiotes! intestinaux! posent! en! fait! des!
questions!proches!et!utilisent!des!méthodes!quasi!similaires.'
'
'
'
!
"!178!"!
!
2.' Les' parallèles' conceptuels' et' théoriques' entre' l’étude' des' relations' hôtesV
symbiontes'et'la'biogéographie'
'
La! biogéographie,! qu’elle! soit! historique! ou! écologique,! entretient! de! nombreux!
liens!conceptuels!avec!l’étude!des!relations!hôtes"symbiontes!(ou!parasites).!
'
2.1."Biogéographie"historique,"relations"hôtes;parasites"et"évolution"des"génomes"
'
«+Evolutionary+associations+among+genes,+organisms+and+geographical+areas+have+
traditionally+been+studied+by+biologists+from+different+disciplines,++
with+little+interaction+between+them.+»+
!
Page!&!Charleston,!1998!
+
La! description! et! la! compréhension! de! la! dynamique! évolutive! d’un! système! à!
deux! «!partenaires!»! avec! l’un! des! deux! partenaires! «!emboîtés! dans!»! ou! «!suivant!»!
(«!tracking!»)! l’autre! est! un! problème! général! qui! trouve! des! applications! dans!
différentes!disciplines.!Ainsi,!l’étude!de!l’évolution!du!couple!parasite"hôte!présente!des!
similitudes!importantes!avec!l’étude!de!la!biogéographie!historique!(p.!ex.!Brooks!1981),!
tout!comme!l’étude!de!l’évolution!du!couple!gène/espèce!(p.!ex.!Doyle!1992).!En!fait,!les!
trois! disciplines! (biogéographie! historique,! étude! des! relations! hôtes"symbiontes! (ou!
parasites)! et! évolution! des! génomes)! utilisent! les! mêmes! objets! conceptuels! avec! des!
méthodes! très! proches! pour! répondre! à! des! questions! similaires! (Page! &! Charleston,!
1998).!En!effet,!on!peut!s’apercevoir,!en!s’appuyant!l’encadré!4,!que!les!trois!disciplines!
manipulent!toutes!deux!objets!et!quatre!concepts!qui!prennent!des!formes!et!des!noms!
différents! mais! qui! sont! similaires.! Simplement,! le! système! d’étude! est! radicalement!
différent! ce! qui! provoque! l’émergence! de! disciplines! différentes! et! relativement!
cloisonnées,! nuisant! clairement! au! développement! de! chacune! d’entre! elles! (Page! &!
Charleston,!1998).!Heureusement,!la!reconnaissance!de!la!similarité!conceptuelle!entre!
les! trois! disciplines! semble! aujourd’hui! mieux! établie! (Page! &! Charleston! 1998;!
Felsenstein!2004).!!
!
!
!
"!179!"!
!
2.2."Biogéographie"écologique"et"microbiologie""
!
Par!ailleurs,!il!apparaît!aussi!de!plus!en!plus!que!la!microbiologie!en!général!(et!
l’étude! des! relations! hôtes"symbiontes! ou! hôtes"parasites! en! particulier)! peut! utiliser!
une!approche!de!biogéographie!écologique!(ou!d’écologie!des!communautés).!Le!cadre!
conceptuel! et! théorique! proposé! par! Vellend! (2010)! pour! l’écologie! des! communautés!
est! en! fait! fort! utile! en! microbiologie! (Nemergut! et+ al.! 2013)! et! en! particulier! dans!
l’étude! des! microbiotes! (Costello! et+ al.! 2012).! Par! exemple,! dans! le! cas! du! microbiote!
humain,! Costello! et+ al.! (2012)! rapprochent! des! concepts! venant! des! deux! disciplines!
comme!le!couple!perturbation/prise!d’antibiotiques,!ou!utilise!les!concepts!écologiques!
de!méta"communauté!ou!d’invasion!pour!tenter!de!mieux!comprendre!l’assemblage!du!
microbiote! humain.! Les! parallèles! entre! les! deux! disciplines! sont! donc! forts,! mais! il!
existe!tout!de!même!des!zones!encore!mal!explorées,!notamment!l’influence!de!l’histoire!
ancienne!(i.e.!la!co"évolution)!sur!l’assemblage!des!microbiotes!actuels.!!
!
3.'L’apport'des'diversités'à'plusieurs'facettes'en'microbiologie'
+
Dans! cette! thèse,! je! me! suis! demandé! comment! les! indices! de! diversité!
phylogénétique! et! fonctionnelle! pouvaient! participer! au! rapprochement! de! la!
biogéographie!écologique!et!de!la!biogéographie!historique,!notamment!pour!parvenir!à!
une!approche!unifiée!et!une!compréhension!élargie!des!patrons!de!diversités!(Wiens!&!
Donoghue! 2004;! Cavender"Bares! et+al.! 2009,! 2012).! Je! pense! qu’un! tel! rapprochement!
est! aussi! nécessaire! dans! l’étude! des! microbiotes,! et! que! les! indices! de! diversité! à!
plusieurs!facettes!peuvent!jouer!un!rôle!clef.!En!fait,!on!peut!s’apercevoir!:!
!
(1) que! de! tels! indices! sont! très! utilisés! en! microbiologie.! En! effet,! comme!
l’atteste! clairement! la! figure! 4! de! l’introduction! générale,! près! de! 30%! des!
articles! qui! utilisent! le! terme! «!diversité! phylogénétique!»! sont! classés! dans!
la!catégorie!«!microbiologie!»!
(2) qu’une! part! importante! des! indices! de! diversité! phylogénétique! ont! en! fait!
été! créés! par! des! microbiologistes! (voir! le! matériel! supplémentaire! 1! de!
l’article!1)!
!
!
"!180!"!
!
Ainsi,! les! conclusions! de! la! partie! I! sont! aisément! transposables! à! l’étude!
microbiologique! et! des! microbiotes.! Dans! cette! optique,! je! propose! dans! le! chapitre! VI!
d’étudier!la!composition!du!microbiote!de!33!espèces!de!mammifères.!!
!
!
4.'Stratégie'de'travail'
!
! Dans! cette! sous"partie! III.1,! je! vais! me! focaliser! sur! la! compréhension! de! deux!
systèmes! emboîtés!:! la! répartition! géographique! des! mammifères! sur! la! terre! et! la!
répartition! des! bactéries! au! sein! des! intestins! de! différentes! espèces! de! mammifères.!
Bien! que! très! différents! en! terme! d’échelle! spatiale,! ces! systèmes! sont! tous! les! deux!
complexes,!car!ils!comprennent!un!grand!nombre!de!lignées.!En!ce!sens,!je!pense!que!le!
cadre!méthodologique!et!conceptuel!du!chapitre!II,!!qui!propose!de!décomposer!le!long!
d’une! échelle! phylogénétique! la! structure! des! assemblages,! est! adapté! aux! deux!
systèmes.!En!particulier!je!vais!tester!dans!les!deux!cas!si!les!processus!proposés!dans!la!
littérature,!et!parfois!considérés!comme!mutuellement!exclusifs,!n’agissent!en!fait!pas!à!
différentes!échelles!phylogénétiques.!'
!
!
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d’études) (Aire,) Espèce,) Gènes)) accompagné) de) l’illustra6on) des) quatre) processus)
fondamentaux) ) (transfert) horizontal,) duplica6on,) coAsépara6on) et) ex6nc6on).) Le)
document)B)précise)les)termes)employés)pour)décrire)les)objets)et)les)processus)dans)
trois) champs) disciplinaires) différents,) meRant) ainsi) en) évidence) leurs) similarités)
conceptuelles.) La) légende) du) document) A) est) associée) au) document) B) pour) plus) de)
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"!183!"!
Partie!III.1!–!Chapitre!V!
!
CHAPITRE'V'
'
L’ENVIRONNEMENT'ET'L’ESPACE'MODULENT'LA'
RÉPARTITION'MONDIALE'DES'OISEAUX'ET'DES'
MAMMIFÈRES'À'DIFFÉRENTES'ÉCHELLES'
PHYLOGÉNÉTIQUES'
!
"!184!"!
!
Résumé'
'
La! compréhension! des! processus! responsables! de! la! distribution! des! espèces! à!
large! échelle! spatiale! est! un! enjeu! majeur! en! écologie.! Classiquement,! on! distingue! les!
processus! de! type! historique! (dispersion! et! diversification)! et! des! processus! de! type!
écologique! (essentiellement! des! processus! de! niche).! Dans! cette! analyse,! nous!
développons! une! nouvelle! méthode,! appelée! BDTT! (Beta"Diversity! through! Time)! qui!
nous! permet! de! montrer! que! les! deux! processus! agissent! en! fait! à! des! échelles!
phylogénétiques!différentes.!L’histoire!semble!moduler!la!distribution!géographique!des!
branches! profondes! alors! que! l’environnement! paraît! être! plutôt! important! à! fine!
échelle!phylogénétique.!De!façon!intéressante,!nous!montrons!que!de!tels!résultats!sont!
vrais!pour!les!mammifères,!mais!non!pour!les!oiseaux,!ce!qui!peut!s’expliquer!par!la!plus!
grande!capacité!de!dispersion!de!ces!derniers.!En!résumé,!nous!montrons!à!quel!point!il!
est!important!de!faire!varier!l’échelle!phylogénétique!en!biogéographie!afin!de!séparer!
les!effets!de!différents!processus.!
!
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!
Decomposing'the'global'beta'diversity'of'mammals'and'birds'along'a'phylogenetic'scale'
reveal'the'differential'effects'of'space'and'contemporary'climate'
!
F.'Mazel,'R.'O.'Wüest,'J.'Renaud,'S.'Lavergne'and'W.'Thuiller'
'
Univ.!Grenoble!Alpes,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France.!!
CNRS,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France!
!
!
Introduction.'' might!expect!deep!biogeographical!events!to!have!been!
The! complex! structure! of! past! and! present"day! shaped!by!historical!connectivity!between!landmasses!
geographical! distribution! of! species! and! lineages! has! that! depends! on! climate! configurations! and! plate!
long! fascinated! naturalists! (Humbolt! and! Bonpland! tectonics.!!
1805,! Darwin! 1859,! Wallace! 1876).! Generally,! species! On! the! contrary,! one! could! expect! biogeographical!
distributions!are!considered!to!be!the!outcome!of!three! events! (such! as! long! distance! dispersal)! to! act! at! a!
interrelated! processes:! historical! events! (such! as! recent! phylogenetic! scale! and! environment! or! habitat!
dispersal! or! vicariance,! e.g.! Simpson! 1980;! Sanmartín! type! to! shape! the! distribution! of! higher! lineages.! This!
&! Ronquist! 2004),! environmental! filtering! (e.g.! Root! would! imply! that! an! ancient! niche! divergence!
1988a;! b)! and! biotic! interactions! (e.g.! Pedersen! et+ al.! promoted! the! emergence! of! two! lineages! adapted! to!
2014;! Silvestro! et+ al.! 2015).! Nevertheless,! jointly! different!environment.!Then,!the!diversification!within!
studying! these! processes! has! been! difficult,! notably! each!of!the!climatic!regimes!could!have!been!driven!by!
because! their! importance! vary! among! spatial! and/or! allopatric! diversification! coupled! with! strong! niche!
phylogenetic! scale! (Rosenzweig! 1995,! Lomolino! et! al.! conservatism! (Crisp! and! Cook! 2012).! This! has! been!
2010)! .! In! particular,! different! processes! might! shape! shown! for! example,! for! swallowtail! butterflies! where!
lineage!distribution!at!different!phylogenetic!scales!but! the!two!main!clades!inhabit!different!climatic!regimes!
we! lack! understanding! on! how! deep! time! events! and! (temperate!Vs.!tropical,!Condamine!et+al.!2012).!
contemporary! climate! relate! to! present! day! Understanding! spatial! patterns! of! biodiversity! have!
distributions! (Webb! et! al.! 2002,! Cavender"Bares! et! al.! usually! relied! on! the! magnitude! and! shape! of! the!
2006).!! relationship! between! single' β! diversity! measure! such!
We! might! expect! deep! biogeographical! events! such! as! as! species! or! phylogenetic! turnover! (compositional!
dispersal! or! vicariance! to! act! on! the! distribution! of! and!phylogenetic!β!diversity,!CBD!and!PBD,!Whittaker!
higher! taxonomic! levels! at! a! deep! phylogenetic! scale! 1960;!Graham!&!Fine!2008;!Anderson!et+al.!2011)!and!
(e.g.! orders,! families,! etc.),! while! contemporary! environmental! and! spatial! distances.! While! relatively!
environment! shape! the! distribution! of! genera! and! straightforward! and! easy! to! understand,! the! use! of!
species.! This! view! is! particularly! well! supported! on! such! synthetic! indices! may! in! fact! limit! our!
island! systems! where! adaptive! radiations! have! been! understanding! of! the! processes! shaping! lineages!
observed.! In! a! island! radiation,! populations! of! a! given! distribution.! Indeed,! if! different! processes! act! at!
ancestor! species! reaches! a! newly! created! archipelago! different! phylogenetic! scales,! the! use! of! a! single! index!
from! the! mainland! and! subsequently! diversifies! in! of! turnover! between! assemblages! will! mix! different!
several!lineages.!This!is!the!case!for!example!in!Hawaï! independent! signals! and! possibly! blur! the! overall!
with! the! tetragnatha! spiders! (Gillespie! 2004)! and! pattern.! Moreover,! while! some! studies! have! examined!
silverword!alliance!(Baldwin!and!Sanderson!1998)!but! the!beta"diversity!through!a!relatively!crude!taxonomic!
also! in! less! remote! islands! such! as! the! carribean! with! scale!(i.e.!analysing!beta"diversity!of!species,!genus!and!
the! anoles! lizard! (Losos! 2009)! and! in! south! America! families,!see!for!example!Qian!2009;!Kreft!&!Jetz!2010),!
fossils! records! with! the! so"called! notoungulates! very! few! have! used! the! phylogenetic! information! to!
(Simpson! 1980).! This! means! that! between! mainland! decompose! the! spatial! variation! of! lineages!
and! island! assemblages,! spatial! turnover! of! high! composition.!!
taxonomic! levels! is! the! product! of! dispersal! whereas! To! overcome! these! limits,! we! propose! to! decompose!
that!of!lower!taxonomic!levels!results!from!adaption!to! the!classical!measure!of!phylogenetic!β!diversity!along!
different! environments.! For! mammals! and! birds,! we! the! phylogenetic! scale! (Beta! Diversity! through! time,!
!
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BDTT).! Instead! of! a! single! value! of! turnover,! we! thus! et!al.!2013,!Vilhena!and!Antonelli!2015)!and!have!been!
obtain!a!profile!of!turnover!through!evolutionary!time! suggested! to! be! –at! least! partly"! the! product! of!
(BDTT!profile,!see!Fig.!1!and!Rosauer!et+al.,!2014!for!a! historical! contingencies,! i.e.! vicariance! events! or!
related! approach).! This! BDTT! profile! thus! starts! with! dispersal.!The!positive!significant!relationship!between!
the! CBD! (i.e.! turnover! of! the! tips! of! the! phylogenetic! species!turnover!and!environmental!distances!has!also!
tree)!and!progressively!goes!back!up!in!the!hierarchic! been!found!at!this!scale!(e.g.!Buckley!&!Jetz!2008)!and!
phylogenetic! classification! (see! Fig.! 1).! PBD! then! may! correspond! to! the! signature! of! environmental!
relates!to!the!mean!of!the!BDTT!profile!(Fig!1.C),!i.e.!it! filtering.! Overall,! the! fact! that! space! better! explained!
represents! a! synthetic! measure! of! the! profile,! as! it! is! species!turnover!than!environment!for!the!two!groups!
averaged!over!the!whole!phylogenetic!time!scale.!This! (Fig.! 2)! could! reflect! the! important! effect! of! historical!
new! approach! may! reveal! the! differential! effect! of! events! Vs.! species! differentiation! across! climatic!
space!and!environment.!! gradients.!In!principle,!we!can’t!rule!out!the!possibility!
More! specifically,! we! decomposed! the! Phylogenetic! that! our! spatial! distance! hide! other! environmental!
version!of!the!classical!Simpson!index!(Simpson!1943,! distances!(e.g.!Anderson!et+al.!2011).!!
Leprieur!et!al.!2012,!Holt!et!al.!2013)!to!better!describe! We! then! analysed! turnover! of! higher! lineages!
and! understand! the! relative! importance! of! space! and! using!the!branching!pattern!of!the!phylogenetic!tree!of!
contemporary!environment!in!present!day!structure!of! each! group! (see! principle! in! Fig.! 1).! This! time"
birds! and! mammals! assemblages! worldwide.! We! used! calibrated!branching!pattern!is!somewhat!linked!to!the!
available! species! distributions! coupled! with! classical!taxonomic!rank!assignation!in!genus,!families!
phylogenetic!trees!for!birds!and!mammals!to!ask!three! and! orders! (see! distributions! of! taxonomic! rank! ages!
mains!questions.!! on! the! phylogenetic! scale! in! Fig.! 2! and! for! example!
First,! are! geographical! and! environmental! distances! Qian! 2009;! Kreft! &! Jetz! 2010).! Nevertheless! the!
shaping! bird! and! mammal! distributions! at! the! same! congruence! is! relatively! low! and! we! believe! our!
phylogenetic! time! scale?! Second,! are! these! relative! approach! is! thus! more! transparent! and! less! arbitrary.!
influences!variable!within!each!of!the!two!groups,!i.e.!is! In! fact,! decomposing! lineage! diversity! through!
there! a! good! congruence! among! orders! or! not?! Third,! evolutionary! time! reveals! the! differential! impacts! of!
do!past!geographical!distances!explain!the!turnover!of! space! and! environment! on! lineage! distributions.!
deep! lineages! better! than! present"day! isolation?! We! Across!the!two!groups,!we!found!that!the!pure!spatial!
hypothesise! that! if! vicariance! events! (or! isolation! effect! was! generally! hump"shaped,! although! much!
because! of! geographic! distance)! have! been! the! major! more! for! mammals! than! for! birds,! meaning! that!
drivers! of! range! evolution,! deep! lineages! turnover! geographical! distances! relatively! better! predict! the!
should!be!more!related!to!past!geographical!distances.! turnover!of!deep!lineages!than!the!turnover!of!species!
On! the! contrary! if! long"distance! dispersal! has! been! (Fig.! 2).! These! profile! do! not! not! only! derive! from! the!
predominant! in! the! past,! independently! of! past! observed! species! beta! diversity! and! the! phylogenetic!
geographic! distances,! we! should! not! see! any! effect! of! tree! shape! but! rather! represent! a! non"random! spatial!
past!geographic!information!on!BDTT!profile.!! distribution! of! higher! lineages! in! the! phylogeny!
! (compare!observed!profile!and!null!95%!CI!envelope!in!
Results'and'Discussion' blue!on!Fig.!2).!On!the!contrary,!environmental!effects!
' appeared! to! be! monotically! decreasing! through! time!
Relative+effects+of+space+and+environment+ and! becoming! rapidly! non"significant,! meaning! that!
At! the! scale! of! this! analysis! and! for! both! birds! and! environmental! distance! better! predict! the! turnover! of!
mammals! species,! true! turnover! was! significantly! species!than!deeper!lineages!(Fig!2).!Nevertheless,!this!
positively! related! to! broad! environmental! and! spatial! decreasing! profile! is! not! as! steep! as! one! could! expect!
distances! (Fig.! 2).! The! relationship! between! species! from! the! observed! species! beta! diversity! and! the!
turnover! and! spatial! distance! –the! so! called! distance! structure! of! the! phylogenetic! tree! only,! meaning! that!
decay! relationship"! is! a! well! studied! pattern! in! the! turnover! of! certain! relatively! deep! lineages! is!
(macro)ecology! (Rosenzweig! 1995)! and! has! been! linked! to! broad! environment! gradient! as! well!
already! reported! at! this! spatial! scale! (e.g.! Qian! &! (compare!observed!profile!and!null!95%!CI!envelope!in!
Ricklefs! 2012).! This! significant! relationship! explains! orange!on!Fig.!2).!All!these!results!were!robust!to!tree!
why! species! assemblages! can! be! grouped! in! uncertainties! (compare! multiple! observed! profiles! in!
biogeographic! realm! that! arbour! clear! spatial! Fig.! 2),! to! the! relaxation! of! the! linear! hypothesis!
organisation! (Wallace! 1876,! Kreft! and! Jetz! 2010,! Holt!
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between! faunal! turnover! and! space! or! environment! Overall! we! showed! that! the! pure! spatial! effect! had! an!
and!to!our!stratified!sample!design!(Supp.!Mat.!1).!! important! imprint! on! the! turnover! of! lineages! at! all!
These! relative! trends! could! be! the! result! of! old! phylogenetic! scales! up! to! 65! Ma! for! the! two! clades.!
dispersal! events! followed! by! diversification! across! These! geographic! patterns! can! be! explained! by!
major! climatic! gradients.! There! are! many! examples! of! historical! dispersal! events! between! the! closest!
such! sequences! of! processes,! for! example! lemur! landmasses,! such! as! the! arrivals! of! rodents! (family!
primates! only! occur! in! Madagascar! due! to! an! ancient! Caviomorpha)! in! South! America! via! long! distance!
dispersal! events! and! diversified! within! the! different! dispersal! from! Africa! around! 35! Ma! (Sallam! et! al.!
climatic! regime! of! the! island! (Ganzhorn! et! al.! 2006).! 2009).! But! the! important! question! is! rather! to! which!
Overall! our! findings! demonstrate! that! environment! extent! these! dispersal! events! are! predictable! or! not.!
and!space!do!not!influence!lineage!distributions!at!the! Dispersal! is! generally! thought! to! be! linked! to! (1)!
same! phylogenetic! scale! and! thus! shed! new! lights! on! species! dispersal! abilities! that! are! mediated! by!
the! spatial! structure! of! biodiversity.! Because! this! functional! traits! (Sanmartín! and! Ronquist! 2004,!
structure! is! a! highly! complex! system,! biogeographers! Whitmee! and! Orme! 2013)! and! to! some! measure! of!
and! macro"ecologists! have! to! describe! it! with! some! distance! between! two! regions! (de! Queiroz! 2005,!
synthetic,! tractable! measures! (e.g.! beta"diversity! Gillespie! et! al.! 2012).! As! a! consequence,! we!
indices).! This! simplification! then! allows! to! handle! a! hypothesise!that!ancient!dispersal!probability!between!
relatively! few! number! of! variables! against! which! two! landmasses! should! be! linked! to! (1)! past!
hypotheses!can!be!tested.!Our!approach!lies!somewhat! connectivity!between!the!landmasses!and!(2)!dispersal!
between! studies! that! focus! on! one! single! parameter! abilities!of!the!studied!taxa.!
(i.e.! that! studies! one! single! beta! diversity! values)! and! !
those! that! study! all! lineages! separately! (e.g.! The+imprint+of+tectonics+
Borregaard!et+al.!2014).!Nevertheless!we!assumed!that! We! tested! this! hypothesis! by! reconstructing!
spatial! and! environmental! effects! could! act! differently! the! paleo"coordinates! of! the! studied! grid! cells! and!
along! the! phylogenetic! scale! but! not! among! different! testing! their! ability! to! explain! faunal! turnover! at! deep!
parts! of! the! tree,! thus! neglecting! heterogeneity! within! phylogenetic!scales.!We!used!past!crow"fly!geographic!
the!tree.!! distance! as! a! proxy! of! past! historical! connectivity!
Comparing! BDTT! between! mammals! and! birds! and! between!regions.!Our!hypothesis!is!that!relatively!close!
among!orders!revealed!interesting!trends.!The!fact!that! grid! cells! in! the! past! may! have! been! more! prone! to!
environmental! profiles! were! similar! for! birds! and! dispersal!events!than!distant!grid!cells.!In!this!case,!we!
mammals!is!consistent!with!the!deterministic!nature!of! expect!higher!deep"time!similarities!between!grid!cells!
niche! processes! and! similar! niche! conservatism! relatively!more!connected!in!the!past.!On!the!contrary,!
strength.!On!the!contrary,!deep"time!faunal!similarities! grid!cells!that!have!been!more!isolated!from!each!other!
were! much! better! explain! by! geographical! distances! in! the! past! have! probably! less! experienced! dispersal!
(than! species! similarities)! in! mammals! than! in! birds.! events! and! thus! may! harbor! lower! deep"time! faunal!
This!is!consistent!with!the!higher!dispersal!abilities!of! similarities.!!
birds!that!possibly!erased,!over!evolutionary!time,!the! Historical! proximity! was! significantly! related!
potential!spatial!signal!of!in"situ!of!diversification.!! to! deep! faunal! turnover! in! mammals! but! not! in! birds,!
We! found! that! these! overall! trends! hide! a! diversity! of! supporting! the! hypothesis! that! historical! proximity! is!
response! across! the! different! parts! of! each! of! the! tree! more!important!for!taxa!with!lower!dispersal!abilities,!
(Supp.! Mat.! 2).! Decomposing! the! turnover! within! because!the!high!dispersal!would!erase!the!signal!of!in"
orders! showed! variable! trends,! notably! that! orders! situ! diversification! (Fig! 3! and! Supp! Mat.! 3).! It! is!
with! a! clear! disjunction! patterns! show! clear! BDTT! important! to! note! that! while! our! results! could! be!
patterns! (Supp.! Mat.! 2).! For! example,! the! strength! of! theoretically! explained! by! repeated! vicariance! events,!
the! relationship! between! primate! turnover! and! space! it!seems!in!fact!highly!unlikely.!Indeed,!the!breakup!of!
show!a!clear!increase!from!species!turnover!to!higher! pangea! started! well! before! the! cenozoic! era! so! as!
clades,! a! pattern! that! matches! the! clear! geographical! vicariance! events! could! only! occur! before! the! K/T!
disjunction! of! some! lineages! of! primates! (e.g.! new! vs.! boundary,! i.e.! in! the! Mesozoic,! while! the! data! we!
old! world! monkeys).! Also,! it! appears! that! the! spatial! analyse! here! is! restricted! to! the! Cenozoic.! As! a!
effect! was! more! variable! through! time! than! the! consequence,! we! suggest! that! the! relationship! we!
environmental! one,! a! pattern! that! could! be! explained! found! is! rather! the! product! of! relatively! long"distant!
by!the!somewhat!contingent!nature!of!dispersal.!! dispersal! constrained! by! historical! proximity! between!
!
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landmasses.! It! is! surprising! to! find! such! a! clear! probably! oversimplified! because! dispersal! do! not!
relationship! with! a! relatively! naïve! proxy! of! historical! necessarily!occurs!in!a!straight!line!but!rather!depends!
connectivity.!In!fact,!we!found!that!the!overall!pattern! on! the! geographical! structure! of! habitat! (i.e.!
was! mostly! driven! by! the! particular! case! of! Australia.! connectivity).!For!example,!two!pairs!of!grid!cells!with!
Indeed,! when! this! continent! was! removed! from! the! the! same! geographical! distances! may! in! fact! harbour!
analysis,! the! congruence! between! past! distance! and! very! different! connectivity! if! for! example,! one! pair! is!
deep!faunal!turnover!vanished!(Supp.!Mat.!4).!Australia! separated! by! ocean! while! the! other! pairs! is! separated!
represents!an!important!zoogeographic!realm!because! by! suitable! habitat.! Future! studies! may! try! to! test!
it!contains!a!very!unique!set!of!species!and!thus!show! alternative!measures!of!connectivity,!such!as!least!cost!
high! turnover! with! the! rest! of! the! world! (Kreft! &! Jetz! distances! considering! the! different! barrier! effects! of!
2007;! Holt! et+ al.! 2013! and! see! Supp.! Mat.! 5.1).! In! seas! or! landmasses! with! unfavourable! environmental!
absolute! terms,! the! turnover! of! higher! lineages! is! conditions! (e.g.! deserts,! mountain! chains).! An!
necessarily! lower! than! the! turnover! of! species! due! to! interesting! avenue! would! also! be! to! take! into! account!
the! hierarchical! structure! of! the! phylogenetic! tree.! the! past! distribution! of! climates! to! track! back! the!
Nevertheless,! it! appears! that! Australia! shows! a! potential! ‘corridor’! of! suitable! climate! for! lineages!
relatively! higher! faunal! isolation! of! higher! lineages! trough!time.!!
(Supp.! Matt! ! 5.2"6).! Because! Australia! was! !
geographically! more! isolated! –relatively! to! other! Conclusion+
landmasses! in! the! world"! in! the! past,! it! explains! why! The!importance!of!phylogenetic!scale!decomposition!in!
Australia! drives! the! overall! pattern! of! congruence! the! studies! of! diversity! patterns! have! long! been!
between! BDDT! and! past! distances! we! found.! Except! emphasized! in! the! context! of! lineage! richness! (e.g.!
from!the!particular!case!of!Australia,!we!did!not!find!a! O’Brien!et+al.!1998,!2000;!Qian!&!Ricklefs!2007;!Qian!et+
signature!of!links!between!past!geographical!proximity! al.! 2009;! Terlizzi! et+ al.! 2009;! Kreft! &! Jetz! 2010)! but!
and!turnover!of!deep!lineages.!This!could!be!explained! have!not!been!carried!out!in!the!context!of!a!calibrated!
by!the!real!uncoupling!of!the!two!processes!or!by!two! time"scale! and! faunal! composition! (i.e.! beta! diversity!
main!methodological!limits!of!our!approach!when!it!is! patterns).! Here! we! show! that! such! decomposition!
linked! to! past! connectivity.! First,! our! approach! can’t! reveal! the! differential! effect! of! geographical! and!
directly! disentangle! the! signal! of! recent! and! ancient! environmental!distance!on!faunal!turnovers.!We!found!
dispersal!events.!For!example,!in!the!case!of!mammals,! that! while! environment! better! explain! turnovers! of!
the! Great! American! Biotic! Interchange! brought! only! recent! lineages! (i.e.! species),! geography! better! predict!
recently! new! orders! in! South! America! (i.e.! in! the! last! deep! faunal! turnover! (e.g.! genus! or! families).! This!
15!Ma,!Webb!2006;!Woodburne!2010!but!see!Bacon!et+ could! suggest! that! biogeography! impact! the!
al.! 2015),! for! example! cetartiodactyls! or! carnivoras.! distribution! of! broad! lineages! while! environment!
Thus,!because!of!these!recent!events,!turnover!of!deep! select! for! finer! differences.! We! further! show! that! the!
lineages!(such!as!the!stem!branches!of!these!orders)!is! impact! of! geography! on! the! distribution! of! broad!
reduced! between! North! and! South! America! and! does! lineages! is! shaped! by! species! dispersal! abilities! and!
not! represent! the! turnover! of! lineages! that! were! only! historical!proximity!between!regions.!!
restricted! to! South! America! at! this! given! time! slice.! !
Also,! while! being! isolated! for! most! of! its! history! Acknowledgements'
(Simpson! 1980,! but! see! Bacon! et+ al.! 2015),! South! The! research! leading! to! these! results! had! received!
America! surely! harboured! in! the! past! a! rather! unique! funding!from!the!European!Research!Council!under!the!
set! of! high! taxonomic! categories! (Simpson! 1980),! but! European!Community’s!Seven!Framework!Programme!
the! joint! effect! of! recent! migration! (i.e.! the! great! FP7/2007"2013! Grant! Agreement! no.! 281422!
American! biotic! interchange)! coupled! with! high! (TEEMBIO).! All! authors! belong! to! the! Laboratoire!
extinction! rates! of! native! lineages! (Simpson! 1980)! d’Écologie! Alpine,! which! is! part! of! Labex! OSUG@2020!
removed! the! signal! of! important! deep! lineages! (ANR10!LABX56).!!
turnover.! On! the! contrary,! Australia! did! not! undergo!
secondary!connections!with!other!continents!followed!
by!massive!migration!events,!thus!retaining!its!unique!
deep!lineages.!!
Second,!our!proxy!for!historical!connectivity!is!in!fact!a!
raw! measure! of! past! geographical! proximity.! It! is!
!
"!189!"!
!
1.+Phylogene&c+tree+ 2.+Assemblages+
+++++++++(A)+++++++++(B)+
Evolu&onary+&me+
Past+ Present+
CBDA/B+=+1+
PBDA/B+=+0.56+
3.+Diversity+through+&me+profile+
!
Figure'1.'Theoretical'example'of'the'β'diversity'through'time'(BDTT)'approach.'The!
figure!presents!a!(1)!phylogenetic!tree!associated!with!(2)!two!assemblages!(A!and!B)!and!
(3)!the!corresponding!compositional!β"diversity!(CBD),!phylogenetic!β"diversity!(PBD)!and!
BDTT! measures! between! A! and! B.! The! phylogenetic! tree! (1)! contains! 16! species! whose!
presence!in!assemblage!A!and/or!B!are!depicted!by!a!line!in!front!of!each!tip!(2).!Below!the!
tree! is! depicted! the! BDTT! profile! along! the! same! time! scale! with! CBD! and! PBD! given! for!
information.!!
' '
!
"!190!"!
!
0.6 0.6
R2+of+β8div+against+Space+or+Env.+
0.4 0.4
Explanatory
Variables
Space
0.2 0.2 Envir
0.0 0.0
0 20 40 60 0 20 40 60
Age$of$taxonomic$ranks$
Evolu&onary+&me+scale+(Millions+of+years)+
Species'
(Ma)$
Genus'
Families'
Orders'
0 20 40 60 0 20 40 60
'
Figure'2.'The'relative'effect'of'spatial'and'geographical'distances'on'the'turnover'of'lineages'through'
time.' The! figure! presents,! for! birds! and! mammals! separately,! the! variation! of! the! strength! of! the! Pearson!
correlation! (Y"axis)! between! faunal! turnover! and! geographic! or! environmental! distances! along! the!
phylogenetic! scale! at! which! faunal! turnover! is! defined! (X"axis)! based! on! the! stratified! sample.! Multiple!
profiles! of! correlation! refer! to! alternative! phylogenetic! trees.! Black! line! corresponds! to! a! smoothed! fit.! The!
shaded! area! corresponds! to! the! 95%! confidence! interval! of! a! null! model! that! randomizes! phylogenetic!
relationships! but! keeps! species! composition! constant.! The! distribution! of! stem! ages! of! four! classical!
taxonomic! ranks! (species,! genus,! families! and! orders)! is! given! along! the! time"scale! used! to! define! faunal!
turnover.! *:significant! correlations,! i.e.! for! a! given! slice,! more! than! 90%! of! the! observed! phylogenetic!
decompositions!support!a!significant!relationship!at!the!5%!level.''
' '
!
"!191!"!
Age,distribu7on,of,four,taxonomic,ranks,
'
Species'
!
Genus'
Families'
Orders'
60% 60%
50% 50%
40% 40%
30% 30%
20% 20%
10% 10%
Paleo&geography,(Ma),
!
0% 0%
0%
0%
10%
20%
30%
40%
50%
60%
10%
20%
30%
40%
50%
60%
"!192!"!
Correla.on%between%β3diversity%
%and%(past)%spa.al%distance%
140
120
100
80
60
40
20
0
Low% High% β"diversity+(faunal+turnover)+
along+the+evolu6onary+6me+scale+(Ma)+
Figure'3.'The'historical'imprints'of'past'continental'position'on'BDTT."The"&igure"presents,"for"birds"and"mammals"separately,"the"
variation" of" the" strength" of" the" correlation" between" faunal" turnover" and" geographic" distances" (see" colours" in" the" legend)" along" the"
phylogenetic" scale" at" which" faunal" turnover" is" de&ined" (X>axis)" and" the" date" at" which" geographical" distance" is" computed" (Y>axis)." More"
speci&ically,"for"each"evolutionary"time"slice"where"turnover"is"computed"(X>"axis),"we"rank"past"geographical"distances"according"to"their"
variance"explanation."Ranks"presented"are"the"median"over"phylogenetic"100"trees"with"red"colour"indicating"a"relative"better"&it."Paleo>
geographic"positions"are"depicted"near"the"Y>axis"(based"on"Scotese"maps)."The"distribution"of"stem"ages"of"four"classical"taxonomic"ranks"
(species," genus," families" and" orders)" is" given" along" the" time>scale" used" to" de&ine" faunal" turnover." An" illustration" of" the" method" used" to"
compute"BDTT"is"given"below"the"X>axis."Phylogenetic"trees"depicted"below"the"plots,"as"well"as"the"three"coloured"lines,"are"given"here"for"
illustration" purpose" and" do" not" correspond" to" the" real" mammal" and" bird" trees," nor" any" speci&ic" time" slice" used" for" computations,"
respectively."
!
' The! general! Sørensen! dissimilarity! metric! can! be!
Material'and'Methods' written!as:!
' !
Distribution'data' Eq.1! ! !!"# !="
!!!
!
!!!!!
We!derived!occurrence!data!for!birds!and!mammals!
!
on! worldwide! grid! cells! of! approximately! 200*200!
and!is!decomposed!in!a!‘true!turnover’!component!"
km.! For! mammals,! we! used! the! distribution! maps!
initially!proposed!by!Simpson!(1943)":!!
provided! by! the! Mammal! Red! List! Assessment!
!
(http://www.iucnredlist.org/)! for! 4616! mammals.! !"#!(!,!)
Eq.2! ! !!"# !=" !
For! birds,! winter! ranges! distribution! maps! were! !!!"#!(!,!)
extracted! from! BirdLife! (http://www.birdlife.org/)! !

for! 9993! species.! The! best! resolution! to! use! these! where!a!=!the!number!of!species!shared!by!the!two!
maps! is! still! under! discussion! in! the! literature! grid! cells! and! b! and! c! represent! the! number! of!
(Storch!et!al.!2012,!Jenkins!et!al.!2013)!so!we!used!a! species!unique!to!each!grid!cell.!
resolution! commonly! used! at! global! scale! (e.g.! Safi! The! Sørensen! metric! is! tightly! close! to! the! Jaccard!
et+al.!2011;!Holt!et+al.!2013).!Domestic,!aquatic!and! index! (Jaccard! 1901)! and! both! are! commonly! used!
semi! aquatic! mammals! were! excluded! from! the! in! macro"ecology! (e.g.! Buckley! &! Jetz! 2008;! Qian! &!
analysis.!! Ricklefs! 2012;! Mouillot! et+ al.! 2013).! The!
Stratified'sample' decomposition! of! beta"diversity! metrics! into! their!
Because! of! computational! constrains,! we! simplified! two!distinct!components!have!been!some!matters!of!
some! part! of! our! analysis! by! subsampling! 200! grid! debates! (Baselga! 2010,! 2012,! Podani! et! al.! 2013,!
cells! out! of! 3600.! In! order! to! correctly! sample! the! Mouillot!et!al.!2013,!Leprieur!and!Oikonomou!2014,!
environmental!(summarized!by!the!two!first!axis!of! Legendre! 2014,! Baselga! and! Leprieur! 2015).! We!
a! PCA! on! the! global! worldclim! variables)! and! the! choose! to! use! the! decomposition! proposed! by!
geographical! space! we! used! the! cube! method! Baselga! (2010)! because! its! ‘true! turnover’!
(Deville! 2004)! based! on! PCA! axis! scores! and! component! is! not! mathematically! constrained! by!
geographical! position! of! each! grid! cells! (see! Supp.! difference!in!species!richness!(Baselga!and!Leprieur!
Mat.!6).!! 2015),! a! key! property! not! fulfilled! by! other!
Phylogenies' proposed!frameworks.!
For!mammals,!we!used!the!100!calibrated!and!dated! !
ultrametric!phylogenetic!tree!updated!by!Fritz!et!al.! Decomposition+trough+time+
(2009)! from! Bininda"Emonds! et! al.! (2007).! For! For! a! given! metric! (e.g.! βsor! or! βsim! see! Eq.1"2),!
Birds,!we!used!the!first!100!phylogeny!proposed!by! classical!measures!typically!rely!on!a!single!number!
Jetz!et+al.!(2012).! to!describe!the!turnover!between!two!assemblages.!
! This! number! may! reflect! species! dissimilarities!
β'diversity'metrics' (Baselga! 2010)! or! branch! length! dissimilarities! if! a!
Metrics+ phylogeny! is! integrated! (Leprieur! et+ al.! 2012).!
The! species! beta"diversity! or! dissimilarity! between! Nevertheless,! relying! on! a! single! number! to!
two!assemblages!is!generally!decomposed!into!two! describe! assemblage! dissimilarities! may! be! a!
distinctive! components! (Baselga! 2010).! The! first! problem! if! different! processes! act! at! different!
component!quantifies!the!degree!of!replacement!of! phylogenetic!scale!because!the!use!of!a!single!index!
species! between! two! sites! and! is! often! called! the! will!mix!different!independent!signals!and!possibly!
‘true! turnover’! component! or! ‘spatial! turnover’! blur!the!overall!pattern.!We!thus!propose!to!study!a!
(Gaston! and! Blackburn! 2008,! Baselga! 2010).! This! profile! of! dissimilarity! through! time! (see! Fig.! 1).!
component! is! independent! of! species! richness! More! specifically,! we! trace! back! the! lineages!
difference! between! assemblages! and! is! the! composition!similarities!between!grid!cells!for!each!
component! of! choice! to! delineate! zoogeographic! time! slice! along! the! phylogenetic! tree.! This!
regions! (Kreft! and! Jetz! 2010,! Holt! et! al.! 2013,! decomposition! thus! separates! the! turnover! of!
Mouillot! et! al.! 2013).! Here! we! choose! to! use! to! recent!(e.g.!species)!vs.!deep!(e.g.!genus!or!families)!
decompose!the!classical!Sorensen!metric!(Sørensen! lineages.!!
1948)! using! the! framework! proposed! by! Baselga! !
(2010).!! !
!
"!193!"!
!
Environmental'and'geographical'data' !
For!environment,!we!used!the!Euclidian!distance!on! References'
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effects!of!environment!and!space.!We!used!the!pure!
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(pure!environment!+!shared!affect).!! selection,! or,! The! preservation! of! favored! races! in! the!
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"!196!"!
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"!197!"!
Partie!III.1!–!Chapitre!VI!
!
CHAPITRE'VI'
'
LE''RÉGIME'ALIMENTAIRE'ET'LA'PHYLOGÉNIE'DE'
L’HÔTE'MODULENT'LA'COMPOSITION'DES'
MICROBIOTES'À'DIFFÉRENTES'ÉCHELLES'
PHYLOGÉNÉTIQUES'
'
!
"!198!"!
!
Résumé''
!
Tous! les! mammifères! vivent! en! symbiose! avec! des! communautés!
bactériennes! (microbiotes)! présentent! dans! leur! intestin.! Cependant,! notre!
compréhension!des!processus!responsables!de!l’évolution!du!système!symbiotique!
hôte! :! communauté! reste! limitée.! En! particulier,! l’importance! relative! de! la!
descendance!verticale!(c’est"à"dire!le!long!de!la!phylogénie!de!l’hôte)!et!horizontale!
(c’est"à"dire!entre!hôtes!éloignés!ou!depuis!l’environnement)!est!mal!connue.!Dans!
cette! analyse,! nous! montrons! que! la! phylogénie! et! le! régime! alimentaire! de! l’hôte!
influencent! les! microbiotes! à! différentes! échelles! phylogénétiques! bactériennes! et!
sont!en!fait!largement!indépendants.!La!phylogénie!de!l’hôte!explique!la!répartition!
des! bactéries! à! fine! échelle! phylogénétique! (par! exemple! les! «!espèces!»!
bactériennes)!alors!que!le!régime!alimentaire!de!l’hôte!explique!la!répartition!à!plus!
large!échelle!phylogénétique!(par!exemple!les!«!ordres!»!de!bactéries),!ce!qui!est!en!
accord! avec! un! conservatisme! de! niche! trophique! à! haut! niveau! taxonomique! des!
bactéries.! Par! ailleurs,! nous! montrons! que! la! structure! emboîtée! des! régimes!
alimentaires!de!l’hôte!(les!omnivores!sont!des!carnivores!et!des!herbivores)!résulte!
en!une!structure!emboîtée!des!communautés!de!bactéries!et!pourrait!partiellement!
expliquer!les!dynamiques!macroévolutives!du!régime!alimentaire!des!mammifères.!
Finalement,! le! signal! phylogénétique! (dans! l’arbre! des! hôtes)! des! compositions!
bactériennes! observées! (aussi! appelé! «!phylosymbiose!»)! peut! s’expliquer! par! un!
nombre! important! de! co"spéciations! entre! hôte! et! bactéries! dénotant! une!
descendance! verticale! d’une! part! importante! de! la! communauté.! En! définitive,! nos!
résultats!permettent!de!réconcilier!l’effet!de!la!phylogénie!et!du!régime!alimentaire!
de!l’hôte!en!les!décomposant!le!long!d’une!échelle!phylogénétique!bactérienne.!!
!
Note"sur"la"participation"
!
Cet!article!est!le!fruit!d’un!travail!commun!avec!mon!ami!et!collègue!Mathieu!
Groussin,!du!MIT!(Boston,!USA).!Cette!collaboration!a!été!initiée!lors!de!mon!voyage!
en! Amérique! du! Nord! en! 2014! et! mon! implication! est! très! forte! (co"leadership! de!
l’article).!!
!
!
"!199!"!
!
Phylogenetic'decomposition'of'mammalian'gut'microbiota'reveals'the'evolution'
of'community'symbiosis'
!
Groussin.!M.1*,!Mazel!F.2,3*,!Sanders!J.4,!Smillie!C.1,!Lavergne!S.!2,3,!Thuiller!W.!2,3!&!Alm!E.1!
'
1'Department!of!Biological!Engineering,!Massachusetts!Institute!of!Technology,!Cambridge,!MA,!USA'
2!Univ.!Grenoble!Alpes,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France.!!
3!CNRS,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France!
4!Department!of!Organismic!and!Evolutionary!Biology,!Harvard!University,!16!Divinity!Avenue!room!
3085,!Cambridge,!Massachusetts!02138,!USA'
'
All' mammals' live' in' mutualistic' symbiosis' with' complex' bacterial' communities' (microbiota)'
present' in' their' gut.' Yet,' our' understanding' of' the' processes' responsible' for' the' evolution' of'
host:community' symbiotic' systems' is' limited,' obscuring' our' knowledge' on' gut' microbiota'
assembly.'Notably,'how'vertical'descent'along'host'phylogeny'and'horizontal'descent'due'to'host'
dietary'shifts'relatively'shape'gut'microbiota'composition'is'unknown.'Here,'we'show'that'host'
phylogeny' and' host' diet' drive' community' assembly' at' different' temporal' scales' of' bacterial'
evolution' and' are' independent' processes.' Host' phylogeny' discriminates' bacterial' lineages' at'
recent'time'scales,'consistent'with'intimate'hostVmicrobe'interactions,'while'host'diet'separates'
out'more'ancient'lineages'owing'to'ecological'conservatism'of'high'ranking'bacterial'clades.'We'
show' that' the' nested' structure' of' diets' results' in' nested' gut' microbiota' compositions,' possibly'
related'to'macroecological'observations'of'dietary'shifts'in'mammals.'We'further'highlight'that'
at' the' time' scale' at' which' host' phylogeny' exerts' its' strongest' influence,' extant' mammalian' gut'
microbiota' compositions' retained' an' ancient' signal' of' host' diversification.' Finally,' we' reveal' a'
strong' and' global' pattern' of' coVspeciation' between' hosts' and' gut' bacteria,' indicative' of' a'
communityVscale' vertical' inheritance' of' this' complex' community' symbiosis.' Together,' our'
results' shed' light' on' the' underlying' complexity' of' processes' driving' the' evolution' of'
mammal:microbiota'symbiotic'systems'and'reconcile'previous,'seemingly'inconsistent'empirical'
observations'on'the'relative'contribution'of'host'phylogeny'and'diet.'Also,'our'results'open'new'
interesting' avenues' to' study' and' further' understand' the' functional' drivers' of' mammalian'
evolution.'
'
'
The! bacterial! consortium! (microbiota)! living! in! inheritance! (drift)! can! entail! these! vertical!
mammalian! guts! form! complex! and! malleable! patterns! due! to! passive! mother"to"infant!
ectosymbiotic!communities!with!their!host!(1,!2).! transmission! and! allopatric! host! speciations.!
They! are! engaged! in! mutualistic! interactions,! Alternatively,! selection! can! also! lead! to!
benefiting! from! resources! provided! by! the! host,! phylosymbiosis! if! a! host! trait! that! is! conserved!
while! having! positive! impacts! on! the! along! the! host! phylogeny! (e.g.! immune! genes)!
physiological! state! and! fitness! of! the! host! (3,! 4).! selects! for! a! particular! microbiota! composition!
The! evolution! of! 1:1! symbiotic! relationships! (10,! 11).! Horizontal! transmission,! however,! may!
between! a! host! and! a! single! symbiont! has! been! occur! if! a! selective! trait! decoupled! from! host!
extensively! studied! (5"7).! However,! little! is! phylogeny! (e.g.! diet! in! Mammals)! promotes! the!
known! about! the! mechanisms! involved! in! the! acquisition!of!particular!bacterial!symbionts!from!
long"term!evolution!of!host:community!symbiotic! the! environment! or! from! distantly"related! hosts!
relationships.! In! particular,! we! are! unaware! of! (12,! 13).! Depending! on! the! magnitude! of! this!
the! long"term! relative! influence! of! vertical! vs.! horizontal! selective! force! and! the! amount! of!
horizontal! descent! in! driving! the! composition! of! bacteria!involved,!the!phylosymbiosis!signal!may!
gut!microbiota.! be! erased! rapidly,! making! gut! microbiota!
! compositional! similarities! related! to! differences!
To!ultimately!understand!the!nature!and! in!trait!values!rather!than!phylogenetic!distances.!
the!magnitude!of!the!evolutionary!forces!shaping! !
these! communities! that! symbiotically! evolve! Here,!we!consider!both!host!evolutionary!
along! the! tree! of! Mammals,! it! is! essential! to! history! (summarized! by! host! phylogeny)! and!
analyze!them!in!a!phylogenetic!context.!If!vertical! host!diet!(as!captured!by!food!items)!as!the!main!
transmission!of!symbionts!occurs,!it!should!result! factors! shaping! guts! microbiota! vertically! and!
in!microbiota!compositions!that!recapitulate!host! horizontally,! respectively! (1).! Several! attempts!
phylogeny! (i.e.! ‘phylosymbiosis’! (8,! 9)).! Neutral! have!been!made!to!determine!which!of!these!two!
!
"!200!"!
!
factors! exerts! a! stronger! influence,! often! we! observe! a! striking! difference! of! bacterial!
concluding! in! favor! of! diet! (1,! 12,! 14),! although! temporal/phylogenetic! scale! at! which! host!
the!topic!remains!debated!(8).!Furthermore,!both! phylogeny! and! diet! shape! gut! microbiota.! Host!
confirming!(1,!15)!and!disproving!(12,!16)!results! phylogeny! governs! community! assembly! at!
about! phylosymbiosis! have! been! reported! at! the! recent! bacterial! phylogenetic! scales,! while! host!
scale! of! mammals,! questioning! the! long"term! diet! mostly! determines! the! composition! of! more!
evolutionary! importance! of! host! phylogeny! in! ancient! lineages! (Fig.! 1).! The! recent"scale!
driving! gut! microbiota! composition! and! discrimination! of! bacterial! lineages! by! host!
obscuring! our! understanding! of! the! evolution! of! phylogeny! is! consistent! in! time! with! a! model! of!
host:community!symbiotic!systems.!! co"evolution! between! host"specific! and! bacteria"
! specific! markers.! It! promoted! the! emergence! of!
We! argue! that! the! problem! over! the! intimate! interactions,! such! as! the! interplay! with!
relative! effects! of! host! phylogeny! and! diet! has! components! of! the! innate! and! adaptive! immune!
been!misidentified!and!that!part!of!the!confusion! system!(17)!or!the!physical!interactions!with!host!
arises! from! the! fact! the! selective! pressures! can! mucopolysaccharides! permitted! by! the! bacterial!
operate! at! different! temporal! scales! of! bacterial! CCF!complex!to!mediate!gut!colonization!(18).!We!
evolution.! For! example,! sister! bacterial! lineages! cannot! reject,! though,! the! potential! selection! of!
might! be! functionally! redundant! and! distribute! recent! bacterial! lineages! by! small! differences! in!
randomly! with! respect! to! a! given! diet! (e.g.! they! dietary! compounds! that! are! not! captured! by! our!
possess! the! same! essential! enzymes! needed! for! dietary! distance! matrix.! Diet,! on! the! other! hand,!
herbivores! to! digest! cellulose)! but! not! with! is! probably! a! less! stringent! factor! and!
respect!to!host!immune!system!(e.g.!they!harbor! discriminates! between! more! ancient! bacterial!
different! antigens).! Consequently,! understanding! lineages.! This! is! consistent! with! the! ecological!
the! determinants! of! microbiota! assembly! along! conservatism! of! ancient! bacterial! taxa! (19),! with!
host! evolution! first! requires! the! use! of! all! lineages! belonging! to! these! ancient! taxa!
appropriate! metrics! and! analytical! procedures! sharing!sets!of!functional!traits!that!are!involved!
that! are! able! to! partition! the! effects! of! factors! in! the! digestion! of! dietary! compounds! (12).!
possibly!acting!at!different!phylogenetic!scales.!! Consequently,! neutral! assembly! is! more!
! important! with! respect! to! diet! at! recent! time!
Here,! we! fill! this! gap! by! developing! a! scales! of! bacterial! evolution,! owing! to! higher!
new! method! called! BDTT! (for! Beta"Diversity! degrees! of! functional! equivalence! within!
Through! Time,! beta"diversity! measuring! the! community! members.! A! large! number! of! control!
amount! of! lineage! compositional! dissimilarities! experiments!suggest!that!our!analysis!uncovers!a!
between! two! communities).! BDTT! seeks! to! genuine! and! robust! signal! of! scale! disparity!
explicitly! capture! the! relationship! between! between! the! two! factors! and! is! not! affected! by!
temporal! diversification! of! bacteria! and! the! systematic! biases! (see! Supplementary! Results).!
evolution! of! their! hosts! by! performing! a! time! In!particular,!our!results!are!robust!to!topological!
decomposition!of!microbiota!compositions.!From! uncertainties! of! the! bacterial! phylogenetic!
the! leaves! to! the! root,! the! phylogenetic! community! tree.! Importantly,! our! results!
community! tree! of! all! sequences! (e.g.! 16S! rDNA! demonstrate! that! claiming! domination! of! one!
reads)! is! continuously! sliced,! either! by! time! or! process! over! another! is! inaccurate! when! gut!
evolutionary! distance.! For! all! slices,! the! microbiota! is! reduced! to! a! single! dimension.! As!
microbiota! compositions! are! determined! and! the! gut! microbiota! is! a! complex! system,!
correlated!to!host!phylogenetic!or!diet!distances.! correlation! outcomes! with! any! factor! depend! on!
We! analyzed! a! dataset! of! 33! mammalian! gut! the! (phylogenetic)! scale! to! which! the! complex!
microbiotas! (12),! composed! of! 44,444! system!is!defined!and!observed.!!
dereplicated! and! chimera"free! amplicons! of! the! !
16S! rRNA! gene! (V2! region)! (see! Methods).! To! The! time! scale! disparity! of! host! phylogeny! and!
apply! BDTT,! we! reconstructed! and! time! diet! may! emerge! from! two! different! patterns:!
calibrated!the!phylogenetic!community!tree!of!all! recent! bacterial! lineages! correlated! to! host!
sequences! (see! Methods).! Note! that,! here,! times! phylogeny!may!be!nested!in!or!independent!from!
given! in! Millions! of! years! should! not! be! more! ancient! diet"related! bacterial! lineages.! To!
considered!as!accurate!divergence!times!between! distinguish! between! these! two! hypotheses,! we!
bacterial! lineages,! but,! as! evolutionary! distance,! removed! the! diet"related! ancient! lineages! (i.e.!
should! be! considered! as! proxies! of! time! (see! those! significantly! correlated! to! diet! at! the! time!
Methods).!! slice!where!the!diet!correlation!is!maximal!(Supp.!
! Fig.! 17)! from! the! gut! communities! and! re"run!
While! both! host! phylogeny! and! diet! BDTT.! The! correlation! with! host! phylogeny!
strongly! correlate! with! community! composition,! remains! very! strong! at! recent! slices,! close! to! its!
!
"!201!"!
!
previous! level,! demonstrating! that! the! vast! between.! It! further! reveals! ecologically!
majority! of! bacterial! lineages! targeted! by! host! differentiated! clades! adapted! to! specific! dietary!
phylogeny! and! diet! are! independent.! The! niches.! Some! bacterial! lineages! exhibit! niche!
decrease!in!correlation,!even!though!it!is!slight,!is! breadth! encompassing! carnivorous! hosts! only,!
nevertheless! higher! than! expected! by! chance! (p= while! others! have! niches! restricted! to!
value! <! 0.01)! and! we! estimate! that! only! 8%! of! herbivorous! guts.! However,! no! niche!
host! phylogeny"related! recent! lineages! are! differentiation!is!associated!with!the!omnivorous!
nested! within! diet"related! ancient! lineages! (see! diet,!whatever!the!phylogenetic!resolution!of!the!
Supp.! Fig.! 18).! Taken! together! these! results! microbiota.!Taken!together,!these!results!suggest!
strongly! suggest! that! the! vast! majority! of! that! herbivorous! and! carnivorous! guts! contain!
bacterial!lineages!targeted!by!host!phylogeny!and! specialist! diet"related! bacterial! lineages,!
diet!are!independent!and!emphasize!the!progress! contrarily! to! omnivores! which! filter! lineages!
made!in!the!description!and!understanding!of!gut! from! these! more! circumscribed! herbivorous! and!
microbiota! assembly! when! decomposing! carnivorous! collections.! We! can! also! reasonably!
microbiota!compositions!through!time!(BDTT).! speculate! that! the! high! rates! of! transition! into!
! omnivory!from!herbivory!and!carnivory!and!vice!
! After! disentangling! the! relative! effect! of! host! versa!are!in!part!facilitated!by!the!composite!and!
phylogeny! and! diet,! we! can! now! describe! the! flexible! composition! of! omnivorous! gut!
mechanistic! features! responsible! for! the! microbiota.!
evolution! of! the! host:community! symbiosis! '
between! gut! microbiota! and! mammalian! hosts! We!next!investigated!in!more!details!the!
for!each!factor!separately.!! processes!associated!to!host!phylogeny!that!drive!
! the! evolution! of! microbiota! symbiosis.! We! found!
We! first! investigated! whether! that! the! correlation! with! host! phylogeny! at! all!
macroevolutionary! patterns! of! dietary! shift! in! recent! bacterial! scales! is! almost! entirely! driven!
mammals! are! linked! to! microevolutionary! by! true! lineage! turnovers,! contrarily! to! what! we!
patterns! in! the! gut! microbiota.! Transition! rates! found! with! diet.! This! pattern! is! likely! the!
between! trophic! strategies! are! biased,! with! consequence!of!niche!sorting!by!co"adapted!host"
transitions! from! herbivory! or! carnivory! into! related! factors.' It! is! consistent! with! previous!
omnivory! and! vice! versa! occurring! at! much! observations! that' gut! microbiota! are! highly!
higher! rates! than! transitions! between! herbivory! malleable! systems! that! can! undergo! rapid!
and! carnivory,! which! are! very! rare! (20).! To! ask! compositional!turnovers!(2,!22).!But!it!also!raises!
whether! the! nested! structure! of! diets! (i.e.! the! question! of! whether! the! phylosymbiosis!
omnivory! regimes! include! herbivory! and! signal! is! conserved! over! long! evolutionary! time.!
carnivory! regimes)! results! in! a! gut! microbiota! Thus,! a! probabilistic! and! phylogenetic! approach!
with! nested! compositions! we! partitioned! our! to! model! and! quantify! the! dynamics! of! lineage!
slice"specific! beta"diversities! into! true! turnover! turnover! (gain! and! loss! of! bacterial! lineages)!
(resulting! from! lineage! replacement)! and! along! the! mammalian! phylogeny! is! required! to!
nestedness! (resulting! from! non"random! lineage! capture! the! phylosymbiosis! signal.! We!
losses)! components! (see! Methods)! (21).! At! the! reconstructed! bacterial! community! sizes! for! all!
ancient! time! slices! where! beta"diversity! highly! mammalian! ancestors! and! compared! these!
correlates! with! diet,! a! significant! signal! of! estimations! with! a! null! model! where! host!
bacterial! community! nestedness! is! observed! phylogeny! is! disrupted! (see! Methods).! Our!
(Supp.! Fig.! 12"13),! indicating! that! some! gut! approach! departs! from! previous! ad"hoc,!
microbiota!are!subsets!of!others.!We!suggest!that! parsimony! and! distance"based! methods! that!
omnivorous! guts! are! responsible! for! this! provided! conflicted! results! (8,! 9,! 12,! 23).!
community! nestedness.! To! confirm! this! Ancestors! with! a! significantly! higher! number! of!
hypothesis,! we! used! a! subset! of! the! whole! gut! bacterial! lineages! than! randomly! expected!
bacterial! community! containing! only! ancient! denote! clades! containing! hosts! that! have!
lineages! that! correlate! with! diet! and! not! host! conserved!a!signal!for!ancestral!bacterial!lineage!
phylogeny! to! represent! both! hosts! and! bacterial! content! and! so,! for! host! speciations.! We! also!
lineages! on! the! same! ordination! space.! This! measured! the! magnitude! of! this! phylosymbiosis!
technique!(OMI,!see!methods)!separates!bacterial! signal! by! computing! Standard! Effect! Sizes! (SES)!
lineages! along! a! niche! gradient,! here! defined! by! (see! Methods)! and! observed! that! most! of! the!
the! host! diet! (Figure! 2).! It! confirmed! the! clades! harbor! a! significant! and! strong! signal! for!
nestedness! component! of! mammalian! gut! phylosymbiosis.!Unexpectedly,!the!gut!microbiota!
communities,! with! the! first! axis! (representing! of! some! clades! older! than! 80Myr! still! harbor!
most! of! the! variance! (77,6%))! separating! imprints!of!ancient!host!speciation,!a!pattern!only!
carnivores! from! herbivores,! with! omnivores! in" detectable! through! our! phylogenetic! and!
!
"!202!"!
!
probabilistic! approach.! The! degree! of! phylogenetic! tree! (see! Supp.! Fig.! 21).! Both!
compositional! conservation! decreases! linearly! processes! result! in! the! same! patterns! of!
with! time,! consistent! with! a! progressive! erasure! presence/absence.!But!they!can!be!differentiated!
of! the! phylosymbiosis! signal! owing! to! multiple! with! probabilistic! models! of! host! tree/symbiont!
turnovers! over! millions! of! years! of! host! tree! reconciliation,! modeling! co"speciation! and!
evolution.! host"shifts! events! (see! Methods! and! Supp.! Fig.!
! 21).!We!highlight!that!65%!of!OTUs!evolved!with!
Are! gut! bacterial! symbionts! vertically! more! co"speciation! events! than! host"shift! events!
inherited! over! millions! of! years! of! mammalian! (Figure! 4),! this! proportion! being! by! far! higher!
evolution?! Actually,! the! presence/absence! than! randomly! expected! under! a! null! model!
profiles! can! be! generated! by! two! different! controlling! for! the! over"fitting! of! the! host! tree!
processes:! strict! vertical! inheritance! through! co" during! the! search! for! the! most! likely! scenario! of!
speciations! or! host"shifts! among! hosts.! For! evolutionary! events.! These! results! strongly!
instance,! three! closely"related! hosts! can! possess! suggest! that! vertical! inheritance! is! the! main!
a!bacterial!symbiont!in!their!gut!to!the!exception! evolutionary!process!experienced!by!mammalian!
of! other! hosts.! This! lineage! can! evolve! vertically! gut! symbionts,! explaining! the! strong! correlation!
or! being! horizontally! inherited! several! times! in! with!host!phylogeny!at!recent!time!scales!(Figure!
time,! leaving! imprints! in! the! symbiont! 1).
!
'
!
"!203!"!
'
!
'
!
"!204!"!
Figure'1.'Host'phylogeny'and'diet'in5luence'microbiota'composition'at'different'phylogenetic'scale.'A)#Variation#of#the#strength#
of#the#mantel#correlation#(X5axis)#between#microbiota#dissimilarities#(β#diversity)#and#host#phylogenetic#(blue)#or#diet#(red)#distances#
along#the#bacterial#phylogenetic#scale#at#which#dissimilarities#are#de?ined#(Y5axis).#The#colored#dashed#lines#correspond#to#the#upper#
part# of# the# 95%# null# envelope# (see# methods).# B)# Bacterial# correlations# with# host# phylogeny# and# diet# at# the# individual# lineage# level#
according#to#PERMANOVA#tests#(see#methods).#Signi?icant#correlations#are#represented#with#colored#dots#on#the#bacterial#phylogenetic#
community#tree#at#four#time#slices,#from#recent#to#ancient#phylogenetic#scales.#Colors#are#as#in#A).#C)#Pie#charts#presenting#the#%#of#
lineages# correlated# to# either# host# phylogeny# or# diet.# Note# that# the# phylogenetic# scale# is# common# for# the# three# plots,# which# are#
connected#with#the#dashed#black#lines#corresponding#to#the#four#time#slices.#Main#bacterial#lineages#are#depicted#below#the#tree#(Ac.:#
Actinobacteria;#Ve.:#Verrucomicrobia;#Fu.:#Fusobacteria;#Fi.:#Fibrobacteres;#Te.:#Tenericute;#Sp.:#Spirochaetes;#Pr.:#Proteobacteria).##
!
'
!
Figure'2.'Ecological'niche'differentiation'of'bacterial'lineages'according'to'host'
diet.! Mammalian! hosts! and! single! bacterial! lineages! are! represented! in! the! same!
ordination! space.! Black! dots! correspond! to! mammals! and! colored! squares! denote!
bacterial! lineages.! Only! bacterial! lineages! with! a! distribution! across! hosts! that! is!
significantly! correlated! to! diet! and! not! to! host! phylogeny! are! represented.! The!
bacterial! lineages! has! been! defined! at! the! time! slice! where! the! correlation! between!
host!diet!and!microbiota!composition!is!high.!The!breadth!of!a!bacterial!lineage!niche!is!
represented! with! an! ellipse! while! niche! centers! are! colored! according! to! bacterial!
phyla!(see!legend).!Host!names!are!color"coded!according!to!broad!dietary!categories:!
carnivores! (red),! herbivores! (green)! or! omnivore! (brown).! Bacterial! niche! breadths!
that! are! restricted! to! a! particular! diet,! highlighting! ecological! differentiations,! are!
colored!accordingly.! !
!
"!205!"!
!
Phylosymbiosis signal
A B
0 10 50 100
(Standard Effect Size)
Kroo3
AfElphSD3
● HyraxSTL
140
●
Armadillo
BushDog1
Phylosymbiosis signal (Standard Effect Size)

● SpecBr2
● ● PolarBr2
120
● ●BlackBr2
Hyena2
● Lion1 ●
100
●
● ● Horse1
ZebraSTL1
● BlackRhino1 ● ●
●
● VWPig
80 ● ●
● Okapi2
●
● Giraffe2 ● ●
● ● SpgbkW ●
60
● Gazelle3
●
● BigHornSD
●
● Urial2 ●
●
●
40
● ●
● RTLemur
BlackLemur
●
●
Callimicos
● ●
20
Saki ●
Orang1
● ●● Chimp1 ●
●
●
CRBM.05 ●
● ● GorillaSTL
●
0
● ●
● ● ●
● Colobus
BaboonSTL 20 40 60 80 100
Rabbit Age (Myr)
● Squirrel
● Capybara
(Myr)
150 100 50 0
!
Figure' 3.' The' decrease' of' phylosymbiotic' signal' with' time.! A)! Mammalian! host!
calibrated! phylogeny.! Internal! nodes! are! colored! according! to! the! degree! of! the!
phylogenetic!conservatism!of!community!composition!(strength!of!the!phylosymbiotic!
signal,! see! legend).! For! each! node,! the! phylosymbiotic! signal! is! measured! as! the!
deviation! between! the! inferred! ancestral! bacterial! community! size! (i.e.! number! of!
OTUs)! and! a! distribution! of! null! expectations! (see! methods).! A! large! value! indicates!
that! the! inferred! community! size! is! much! larger! than! expected! by! chance.! B)! Linear!
decay! of! the! conservation! of! ancient! community! compositions! in! extant! mammalian!
microbiota.!Each!dot!represents!an!internal!node!of!the!phylogenetic!tree!presented!in!
A).!The!phylosymbiotic!signal!at!a!given!ancestor!(Y"axis)!is!plotted!against!its!age!in!
Myr! (X"axis).! A! linear! regression! is! fitted! to! the! data! (black! line)! but! a! p=value! is! not!
provided!owing!to!the!non"independence!of!the!points.!!
! !
!
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!
p-value < 0.001

0.6
0.5
Observed frequency
0.4
0.3
0.2
0.1
0.0
S>T T>S Null

OTUs
!
!
Figure' 4:' The' vertical' inheritance' of' gut' bacterial' symbionts' in' mammals.' The!
figure! presents! the! observed! frequencies! of! OTUs! that! harbor! more! co"speciation! (S)!
than! host! shifts! (T)! events! (dark! blue! bar)! or! more! host! shifts! than! co"speciation!
events!(yellow!bar).!These!observed!frequencies!are!derived!from!an!explicit!model!of!
co"evolution!between!host!phylogeny!and!each!individual!OTU!phylogeny,!accounting!
for!co"speciation,!host"shift,!intra"host!speciation!and!extinction!events.!The!light!blue!
bar! corresponds! to! the! mean! frequency! of! OTUS! harboring! more! co"speciation! than!
host!shifts!events!(S>T)!under!a!null!model!(see!methods).!The!observed!frequency!of!
OTUs! that! harbor! more! co"speciation! than! host! shifts! events! is! much! higher! than!
expected!under!this!null!model!(p=val<0.001).!'
!
' '
!
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!
References' 14.! R.! N.! Carmody! et+ al.,! Diet! Dominates! Host!
1.! R.!E.!Ley!et+al.,!Evolution!of!mammals!and!their! Genotype! in! Shaping! the! Murine! Gut!
gut!microbes.!Science.!320,!1647–1651!(2008).! Microbiota.! Cell+ Host+ and+ Microbe.! 17,! 72–84!
(2015).!
2.! L.! A.! David! et+al.,! Diet! rapidly! and! reproducibly!
alters!the!human!gut!microbiome.! Nature.!505,! 15.! P.! L.! Oh! et+ al.,! Diversification! of! the! gut!
559–563!(2014).! symbiont! Lactobacillus! reuteri! as! a! result! of!
host"driven! evolution.! The+ ISME+ Journal.! 4,!
3.! L.! V.! Hooper,! J.! I.! Gordon,! Commensal! host" 377–387!(2010).!
bacterial! relationships! in! the! gut.! Science.! 292,!
1115–1118!(2001).! 16.! P.! A.! Vaishampayan! et+ al.,! Comparative!
metagenomics! and! population! dynamics! of!
4.! C.!A.!Lozupone,!J.!I.!Stombaugh,!J.!I.!Gordon,!J.!K.! the! gut! microbiota! in! mother! and! infant.!
Jansson,! R.! Knight,! Diversity,! stability! and! Genome+ Biology+ and+ Evolution.! 2,! 53–66!
resilience!of!the!human!gut!microbiota.!Nature.! (2010).!
489,!220–230!(2012).!
17.! H."J.! Wu,! E.! Wu,! The! role! of! gut! microbiota! in!
5.! N.! A.! Moran,! J.! P.! McCutcheon,! A.! Nakabachi,! immune! homeostasis! and! autoimmunity.! Gut+
Genomics! and! evolution! of! heritable! bacterial! Microbes.!3,!4–14!(2012).!
symbionts.! Annu+ Rev+ Genet.! 42,! 165–190!
(2008).! 18.! S.! M.! Lee! et+ al.,! Bacterial! colonization! factors!
control! specificity! and! stability! of! the! gut!
6.! G.!M.!Bennett,!N.!A.!Moran,!Heritable!symbiosis:! microbiota.!Nature.!501,!426–429!(2013).!
The! advantages! and! perils! of! an! evolutionary!
rabbit! hole.! Proc+ Natl+ Acad+ Sci+ U+ S+ A.! 112,! 19.! L.!Philippot!et+al.,!The!ecological!coherence!of!
10169–10176!(2015).! high!bacterial!taxonomic!ranks.!Nat+Rev+Micro.!
8,!523–529!(2010).!
7.! J.! L.! Sachs,! R.! G.! Skophammer,! J.! U.! Regus,!
Evolutionary! transitions! in! bacterial! symbiosis.! 20.! S.! A.! Price,! S.! S.! B.! Hopkins,! K.! K.! Smith,! V.! L.!
Proc+Natl+Acad+Sci+U+S+A.! 108' Suppl' 2,! 10800– Roth,! Tempo! of! trophic! evolution! and! its!
10807!(2011).! impact! on! mammalian! diversification.! Proc+
Natl+Acad+Sci+U+S+A.!109,!7008–7012!(2012).!
8.! H.! Ochman! et+al.,! Evolutionary! Relationships! of!
Wild! Hominids! Recapitulated! by! Gut! Microbial! 21.! A.! Baselga,! Partitioning! the! turnover! and!
Communities.!Plos+Biol.!8,!e1000546–8!(2010).! nestedness! components! of! beta! diversity.!
Global+ Ecology+ and+ Biogeography.! 19,! 134–
9.! R.! M.! Brucker,! S.! R.! Bordenstein,! The! 143!(2010).!
hologenomic! basis! of! speciation:! gut! bacteria!
cause! hybrid! lethality! in! the! genus! Nasonia.! 22.! L.! A.! David! et+al.,! Host! lifestyle! affects! human!
Science.!341,!667–669!(2013).! microbiota! on! daily! timescales.! Genome+ Biol.!
15,!R89!(2014).!
10.! J.! Schluter,! K.! R.! Foster,! The! evolution! of!
mutualism! in! gut! microbiota! via! host! 23.! R.! M.! Brucker,! S.! R.! Bordenstein,! The! roles! of!
epithelial! selection.! Plos+ Biol.! 10,! e1001424! host! evolutionary! relationships! (genus:!
(2012).! Nasonia)! and! development! in! structuring!
microbial! communities.! Evolution.! 66,! 349–
11.! T.!Hosokawa,!Y.!Kikuchi,!N.!Nikoh,!M.!Shimada,! 362!(2012).!
T.! Fukatsu,! Strict! host"symbiont! cospeciation!
and! reductive! genome! evolution! in! insect! gut!
bacteria.!Plos+Biol.!4,!e337!(2006).!
12.! B.!D.!Muegge!et+al.,!Diet!Drives!Convergence!in!
Gut!Microbiome!Functions!Across!Mammalian!
Phylogeny! and! Within! Humans.! Science.! 332,!
970–974!(2011).!
13.! F.! Delsuc! et+ al.,! Convergence! of! gut!

microbiomes! in! myrmecophagous! mammals.!
Mol+Ecol.!23,!1301–1317!(2013).!
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Partie!III.1!–!Synthèse!
!
SYNTHÈSE'&'DISCUSSION''
DE'LA'SOUSVPARTIE'III.1'
!
"!210!"!
!
'
Dans! cette! sous"partie,! nous! avons! montré! que! dans! des! systèmes! d’études!
radicalement! différents,! la! décomposition! des! similarités! compositionnelles! le! long!
d’une! échelle! phylogénétique! peut! permettre! de! distinguer! les! effets! relatifs! de!
différents! processus! qui! assemblent! les! communautés! de! mammifères! ou! bien! les!
communautés! de! microbes! dans! leur! système! digestif.! Dans! les! deux! cas,! ces! études!
tentent! de! reconstruire! l'histoire! des! assemblages,! mais! à! des! échelles! radicalement!
différentes.!
!
1.'Similarités'entre'les'deux'études'
!!
Nous! montrons! que! l’influence! de! l’espace! et! du! climat! sur! la! répartition!
géographique! des! mammifères! et! des! oiseaux! à! l’échelle! du! globe! varie! le! long! de!
l’échelle! phylogénétique.! En! particulier,! l’espace! agit! de! façon! prépondérante! à! une!
échelle! phylogénétique! intermédiaire,! notamment! chez! les! mammifères,! alors! que!
l’environnement! a! un! effet! majoritaire! à! fine! échelle! phylogénétique,! par! exemple! au!
niveau! des! espèces.! On! peut! interpréter! ces! résultats! en! proposant! que! l’histoire!
(dispersion! intercontinentale,! vicariance)! influence! plutôt! la! distribution! des! clades!
profonds,! alors! que! l’environnement! sélectionne! différentes! espèces! parmi! ces! clades!
profonds.! La! même! approche! méthodologique! permet! de! montrer! que! les! microbiotes!
présents!dans!chacun!des!33!mammifères!étudiés!gagnent!à!être!décrits!–!comme!leurs!
hôtes! –! à! différentes! échelles! évolutives.! Le! régime! alimentaire! de! l’hôte! semble!
impacter!des!clades!bactériens!profonds!alors!que!la!phylogénie!de!l’hôte!joue!plutôt!sur!
des!échelles!évolutives!plus!fines.!De!façon!intrigante,!si!l’on!considère!la!phylogénie!des!
hôtes! comme! une! mesure! de! l’histoire! et! le! régime! alimentaire! comme! une! mesure! de!
l’environnement,!les!résultats!obtenus!dans!les!deux!études!sont!opposés.!!
!
En!fait,!il!apparaît!que!la!phylogénie!de!l’hôte!n’est!pas!forcément!une!mesure!de!
l’histoire,! mais! plutôt! d’un! environnement! dont! nous! n’avons! pas! de! mesure! directe,!
mais! qui! est! conservé! le! long! de! la! phylogénie! de! l’hôte,! par! exemple! le! système!
immunitaire! (Hooper! et+ al.! 2012).! Dans! le! cas! de! la! biogéographie! des! mammifères,!
l’espace! pourrait! aussi! «!cacher!»! des! variables! environnementales! non! mesurées.!
Cependant,! il! est! bien! établi! que! les! évènements! historiques! de! dispersion! et! de!
!
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!
vicariance! ont! joué! un! rôle! fondamental! dans! la! biogéographie! des! mammifères!
(Simpson!1980),!ce!qui!conforte!nos!résultats!dans!ce!cas.!De!plus,!nous!montrons!que!la!
géographie!passée!permet!de!mieux!expliquer!les!compositions!à!large!échelle!évolutive,!
ce! qui! conforte! l’idée! que! l’histoire! (ancienne)! agit! à! des! échelles! phylogénétiques!
profondes.!On!peut!cependant!noter!que!l’histoire!récente!(par!exemple!le!quaternaire,!
et! notamment! ses! oscillations! climatiques)! est! aussi! un! élément! important! de! la!
répartition!des!lignées,!mais!à!une!échelle!phylogénétique!plus!fine!(Hewitt!2000,!2004;!
Lister!2004).!!
!
En! définitive,! nous! montrons! que! l’analyse! des! patrons! à! différentes! échelles!
phylogénétique,!par!exemple!via!l’utilisation!de!notre!méthode,!est!prometteuse.!Nous!le!
faisons! pour! la! première! fois! dans! le! cadre! de! la! diversité! β,! mais! nous! avons! montré!
dans! le! chapitre! II! son! utilité! dans! le! cadre! de! l’analyse! de! la! diversité! α! (voir! aussi!
O’Brien! et+ al.! 1998,! 2000;! Qian! &! Ricklefs! 2007;! Qian! et+ al.! 2009;! Terlizzi! et+ al.! 2009;!
Kreft!&!Jetz!2010).!
'
2.'Limites'et'améliorations'possibles'de'la'méthode'BDTT'
+
2.1."Limites"de"la"méthode"
+
La!méthode!proposée!comprend!cependant!certaines!limites.!En!particulier,!il!ne!
faut! pas! confondre! les! similarités! de! composition! établies! par! exemple! à! 20! millions!
d’années! sur! l’arbre! phylogénétique! et! la! similarité! des! faunes! à! cette! époque! (que! ce!
soit! la! faune! fossile! ou! les! descendants! actuels! de! ces! faunes"là).! Par! exemple,! les!
carnivores! et! les! artiodactyles! sont! aujourd’hui! présents! en! Amérique! du! Sud,! mais! ils!
n’y! sont! arrivés! que! récemment! (3"15! Ma),! lors! du! grand! échange! biotique! entre! les!
deux!continents!américains!(GABI,!Webb!2006;!Woodburne!2010,!mais!voir!Bacon!et+al.!
2015).!Cependant,!lorsque!l’on!calculera,!avec!la!méthode!BDTT,!la!similarité!faunistique!
à!30!Ma!entre!les!deux!continents,!les!branches!menant!aux!carnivores!seront!présentes!
dans!les!deux!régions,!et!la!similarité!sera!totale,!bien!qu’à!cette!époque,!les!carnivores!
n’étaient! pas! présents! au! Sud.! En! définitive,! la! méthode! proposée! ne! reconstruit! en!
aucun!cas!la!présence!passée!des!lignées!dans!l’assemblage.!Ceci!contraste!directement!
avec!les!méthodes!de!biogéographie!historique!classiques!(Ronquist!&!Sanmartín!2011).!
!
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!
Cependant,! notre! approche! possède! certains! avantages,! comme! celle! de! ne! pas! avoir! à!
définir! des! aires! d’endémisme! et! de! pouvoir! prendre! en! compte! explicitement!
l’influence!du!climat!actuel!et!passé.!Cette!approche!pourrait!donc!constituer!un!premier!
pas! vers! le! rapprochement! de! la! biogéographie! historique! et! de! la! biogéographie!
écologique.!
!
2.2."Améliorer"les"mesures"de"connectivité"passée"
!
Nous! utilisons! la! méthode! BDTT! pour! évaluer! l’impact! potentiel! de! la!
configuration! passée! des! continents! sur! les! distributions! actuelles! des! lignées! en!
mesurant! les! distances! euclidiennes! entre! assemblages! tout! au! long! du! cénozoïque!
(Chapitre! V).! Notre! mesure! de! proximité! historique! tente! de! quantifier! un! coût! à! la!
dispersion!et!pourrait!être!améliorée,!notamment!en!prenant!en!compte!la!part!relative!
de!croûte!continentale!et!océanique!dans!le!calcul!des!distances!entre!assemblages.!En!
effet,! ces! deux! types! de! croûtes! terrestres! possèdent! des! altitudes! très! contrastées!:!
alors! que! la! croûte! continentale! (+300! m! d’altitude! en! moyenne)! peut! être! émergée,!
surtout! pendant! les! glaciations! (p.! ex.! la! Manche),! la! croûte! océanique! ("2400! m!
d’altitude! en! moyenne)! est! toujours! immergée! et! représente! donc! une! bonne! mesure!
pour! la! limitation! de! la! dispersion.! Par! exemple,! la! ligne! de! Wallace! correspond! à! un!
plancher!océanique!et!non!à!un!plancher!continental!(Lomolino!et+al.!2010).!Par!ailleurs,!
il! serait! intéressant! d’ajouter! une! dimension! climatique! à! notre! analyse! de! la!
connectivité! passée.! Le! climat! tropical! et! la! forêt! tropicale! dominaient! largement! la!
surface!terrestre!au!début!du!cénozoïque!(voir!par!exemple!Burnham!&!Johnson!(2004)!
pour!une!perspective!sud"américaine)!pour!finalement!se!contracter!petit!à!petit!jusqu’à!
leur! position! actuelle! (Zachos! et+ al.! 2001).! On! peut! imaginer! que! la! niche! de! certains!
clades! a! évolué! vers! des! climats! plus! froids! et! secs,! permettant! la! colonisation! et! la!
radiation!dans!les!zones!tempérées!à!un!temps!t.!Si!ces!évènements!sont!assez!rares!et!
non! réversibles,! c’est"à"dire! si! l’on! observe! un! fort! conservatisme! de! niche,! on! peut!
imaginer! que! les! patrons! actuels! de! composition! auront! gardé! la! trace! d’une! telle!
histoire!et!que!l’on!pourra!la!révéler!en!utilisant!la!méthode!BDTT.!Par!exemple,!si!l’on!
imagine!qu’un!certain!nombre!de!clades!commencent!à!radier!dans!les!zones!tempérées!
à! partir! du! miocène,! on! observera! aujourd’hui! une! faible! similarité! d’espèces! entre! les!
régions! tempérées! et! les! régions! tropicales! (donc! un! bon! pouvoir! explicatif! du! climat!
!
"!213!"!
!
actuel! au! temps! 0! du! BDTT).! Si! l’on! remonte! le! long! de! la! phylogénie,! la! similarité! au!
niveau! du! miocène! (et! au"delà)! sera! alors! mal! expliquée! par! le! climat! actuel! (les! deux!
régions! ont! des! climats! différents,! mais! des! compositions! similaires),! mais!
probablement! mieux! par! le! climat! passé! (les! deux! régions! avaient! alors! des! climats!
similaires!et!des!compositions!similaires).!!
'
3.'La'biogéographie'des'hôtes'peutVelle'expliquer'la'composition'du'microbiote'?'
+
Finalement,! j’ai! appliqué! l’approche! aux! deux! systèmes! de! façon! relativement!
indépendante.! J’entrevois! cependant! d’intéressantes! perspectives! en! croisant! ces!
systèmes!d’études.!Il!serait!par!exemple!possible!de!tester!si!la!biogéographie!des!hôtes!
a!une!influence!sur!la!composition!des!microbiotes.!On!peut!en!effet!supposer!que!des!
hôtes!en!sympatrie*!puissent!partager!davantage!de!lignées!bactériennes!que!des!hôtes!
en! allopatrie*! (à! environnement! égal)! simplement! par! transfert! horizontal! ou! via!
transfert!depuis!l’environnement.!Pour!l’instant,!de!telles!influences!ont!été!montrées!à!
petite!échelle!phylogénétique!de!l’hôte,!notamment!parmi!les!grands!singes!du!bassin!du!
Congo!(Moeller!et+al.!2013)!ou!même!au!sein!de!groupes!d’humains!(Yatsunenko!et+al.!
2012).!Il!serait!alors!intéressant!de!comparer!les!similarités!de!microbiotes!entre!hôtes!
à! leur! proximité! géographique,! pour! notamment! tester! si! l’influence! de! la! géographie!
tient! à! des! échelles! phylogénétiques! (des! hôtes)! larges.! La! proximité! géographique! est!
un! prérequis! pour! le! transfert! horizontal! de! bactérie! entre! hôtes.! Il! apparaît! donc!
logique! qu’une! plus! longue! proximité! géographique! augmente! la! probabilité! de!
transfert.! On! pourrait! tester! cette! hypothèse! en! comparant! le! pouvoir! prédictif! de! la!
proximité!géographique!actuelle!avec!celle!intégrée!sur!des!temps!évolutifs,!en!utilisant!
les! méthodes! classiques! de! la! biogéographie! historique! pour! reconstruire! les! aires!
ancestrales!des!hôtes!et!reconstruire!un!profil!de!proximité!géographique!dans!le!temps.!
Cependant,! il! faut! rester! conscient! que! pour! tester! de! telles! hypothèses,! un! jeu! de!
données!conséquent!est!nécessaire!pour!distinguer!les!effets!de!la!phylogénie,!du!régime!
alimentaire! et! de! la! géographie.! En! fait,! il! faut! des! hôtes! qui! représentent! toutes! les!
combinaisons!de!cas!possibles!(par!exemple,!des!hôtes!proches!phylogénétiquement!et!
en! terme! de! régime! alimentaire,! mais! éloignés! géographiquement)! afin! de! disposer!
d’une! puissance! statistique! adéquate! pour! détecter! les! effets! relatifs! de! chacun! des!
facteurs.
!
"!214!"!
!
'
!
"!215!"!
Partie!III.2!
SOUSVPARTIE'III.2'
LA'GÉOGRAPHIE'DE'LA'CONVERGENCE!
!
!
"!216!"!
!
INTRODUCTION'DE'LA'SOUSVPARTIE'III.2'
'
'
Figure'9.'La'convergence'évolutive'entre'marsupiaux'
et'placentaires.'
Copyright!©!2015!The!Pennsylvania!State!University!
'
!
"!217!"!
'
'
Dans! le! chapitre! précédent,! nous! montrons! qu’il! existe! une! relation! statistique!
forte! entre! le! taux! de! similarité! faunistique! de! deux! assemblages! et! leur! proximité!
environnementale.!Cette!observation!suggère!que!des!espèces!différentes!sont!adaptées!
à!des!niches!climatiques!différentes!et!qu’elles!ne!cohabitent!donc!pas.!Elles!sont!filtrées!
par! l’environnement! de! sorte! que! l‘espèce! A! n’est! pas! retrouvée! dans! le! même! espace!
géographique! et! environnemental! que! l’espèce! B.! Pour! confirmer! cette! hypothèse,! il!
apparaît!important!d’incorporer!une!dimension!fonctionnelle!à!notre!étude.!En!d’autres!
termes,!il!serait!d’autant!plus!convaincant!de!montrer!que!des!espèces!vivantes!dans!des!
environnements! différents! possèdent! des! caractéristiques! fonctionnelles! différentes!
adaptées!à!chacun!de!ces!environnements,!ou!au!contraire,!que!des!espèces!différentes!
vivantes! dans! des! environnements! similaires! possèdent! des! caractéristiques!
fonctionnelles! similaires.! Dans! une! perspective! évolutive,! il! est! intéressant! de! se!
demander!à!quel!point!la!sélection!a!pu,!de!façon!indépendante!dans!plusieurs!lignées,!
façonner!les!caractéristiques!fonctionnelles!des!espèces!en!fonction!de!l’environnement.!
Ce! phénomène! que! l’on! appelle! la! convergence! évolutive! (ou! parallélisme*)! avait! déjà!
été!noté!par!Darwin!:!
!
«+Des+animaux+appartenant+à+deux+lignées+d’ancêtres+très+distincts+peuvent,+en+effet,+s’être+
adaptés+à+des+conditions+semblables,+et+avoir+ainsi+acquis+une+grande+ressemblance+
extérieure+;+mais+ces+ressemblances,+loin+de+révéler+leurs+relations+de+parentés+tendent+
plutôt+à+les+dissimuler.+[…]+Ainsi,+la+forme+du+corps+et+les+membres+en+forme+de+nageoires+
sont+des+caractères+purement+analogues+lorsque+l’on+compare+la+baleine+aux+poissons,+
parce+qu’ils+constituent+dans+les+deux+classes+une+adaptation+spéciale+en+vue+d’un+mode+de+
locomotion+aquatique+»++
+
Darwin,!1859+
!
Dans!cette!sous"partie,!je!présente!deux!études!(chapitre!VII!et!annexe!3.2.1)!qui!
visent!à!détecter!l’effet!de!la!convergence!évolutive!à!différentes!échelles.!!
!
Question+générale+:!La!convergence!est"elle!un!processus!majeur!au!cours!de!l’évolution?!!
!
"!218!"!
!
Les! convergences! morphologiques,! physiologiques,! biochimiques,!
comportementales!et!même!«!microbiotiques!»!(Delsuc!et+al.!2014)!qui!permettent!à!des!
espèces! relativement! éloignées! dans! la! phylogénie! d’occuper! des! niches! écologiques!
similaires!représentent!un!argument!majeur!dans!la!démonstration!de!l’importance!de!
la!sélection!dans!l’évolution!des!espèces.!Il!faut!noter!que!ce!champ!de!recherche!a!été!
révolutionné! par! l’avènement! de! la! phylogénie! moléculaire! (Felsenstein! 2004)! qui! a!
modifié!de!façon!importante!les!classifications!taxonomiques!classiques.!Dans!le!cas!des!
mammifères! par! exemple,! la! phylogénie! moléculaire! a! révélé! des! liens! de! parenté!
insoupçonnés! entre! lignées! et! a! placé! des! taxons! morphologiquement! similaires! dans!
des! groupes! totalement! différents.! C’est! par! exemple! le! cas! de! l’ordre! "! longtemps!
instable! "! des! «!insectivores!»! qui! regroupaient! des! familles! holarctiques,! par! exemple!
les! solénodontidés,! et! des! familles! africaines,! par! exemple! les! tenrécidés.! Ces! deux!
familles! sont! maintenant! placées! dans! des! ordres! distincts! (afrosoricidae! et!
soricomorphea,!respectivement).!En!fait,!la!détection!de!la!convergence!évolutive!va!se!
baser! sur! la! comparaison! des! caractères! fonctionnels! dans! un! cadre! phylogénétique.!
Dans! cette! sous"partie,! on! va! distinguer! deux! échelles! de! convergence! (Lomolino! et+al.!
2010).!
!
!
Annexe+3.2.1+et+Chapitre+VII+:+La+convergence+au+niveau+des+espèces+
La!convergence!au!niveau!des!taxons!est!traditionnellement!étudiée!et!reconnue!
comme!importante!(Lomolino!et+al.!2010).!Elle!correspond!notamment!à!de!nombreuses!
«!règles!écologiques!»!comme!celle!de!Bergmann!(augmentation!de!la!taille!des!espèces!
avec! la! latitude)! ou! encore! celle! d’Allen! (diminution! de! la! taille! des! extrémités! avec! la!
latitude).! En! pratique,! il! s’agit,! pour! un! ensemble! d’espèces,! de! corréler! un! trait!
fonctionnel! à! une! variable! environnementale! en! prenant! en! compte! la! similarité!
phylogénétique!entre!les!espèces.!Dans!ce!chapitre,!je!présente!un!résumé!de!l’article!9!
(texte! entier! en! annexe! 3.2.1)! qui+ améliore! les! techniques! actuelles! de! détection! de!
convergence! en! prenant! en! compte! les! variations! de! taux! d’évolution! au! sein! d’une!
phylogénie.!!
!
!
!
"!219!"!
Chapitre+VII+:+La+convergence+au+niveau+des+assemblages+entiers+d’espèces+
La! convergence! au! niveau! des! assemblages! d’espèces! correspond! à! l’évolution!
dans! des! lignées! phylogénétiques! distinctes! de! «!types! morphologiques!»! similaires!
adaptés! à! des! niches! particulières.! En! somme,! cette! convergence! correspond! à! une!
multitude!de!convergences!au!niveau!d’espèces!qui!cooccurrent!dans!une!région!donnée!
(Lomolino!et+al.!2010).!Il!existe!des!exemples!emblématiques!de!convergence!au!niveau!
des!assemblages,!comme!ceux!des!cyclidés!des!lacs!d’Afrique!de!l’Est.!Dans!ce!chapitre,!
nous!tentons!de!montrer!à!quel!point!ce!phénomène!est!repandu!chez!les!mammifères!à!
l’échelle!du!globe.!!
!
"!220!"!
!
"!221!"!
Partie!III.2!–!Chapitre!VII!
CHAPITRE'VII''
'
LA'CONVERGENCE'ÉVOLUTIVE'
DES'ESPÈCES'ET'DES'ASSEMBLAGES''
DE'MAMMIFÈRES'
!
"!222!"!
' '
!
"!223!"!
Résumé'de'l’annexe'3.2.1'(article'9,'accepté'dans'Ecology)'
'
«+Differences+in+rates+of+evolution,++
and+not+only+divergent+evolution+at+comparable+rates,++
are+among+the+reasons++for+the+great+diversity+of+organisms+on+Earth.+»+
Simspon,+1953+
+
+
Les!méthodes!comparatives!représentent!un!outil!clef!dans!la!compréhension!des!
processus! écologiques! et! évolutifs! et! sont! utilisées! pour! tester! des! hypothèses! sur!
l’évolution!corrélée!des!traits!(Felsenstein!1985;!Harvey!&!Pagel!1991).!De!nombreuses!
méthodes!ont!été!proposées!par!le!passé!pour!permettre!de!relier!des!traits!fonctionnels!
d’espèces!tout!en!prenant!en!compte!leur!proximité!phylogénétique!(Felsenstein!1985,!
Grafen! 1989,! Maddison! 1990,! Lynch! 1991,! Garland! et! al.! 1992,! Martins! and! Hansen!
1997,!Diniz"Filho!et!al.!1998,!Freckleton!et!al.!2002,!Paradis!and!Claude!2002,!Ives!and!
Garland!2010;!voir!l’encadré'5!pour!un!aperçu!de!la!chronologie!des!articles!fondateurs!
de! la! discipline).! Aujourd’hui,! la! méthode! des! moindres! carrés! phylogénétique!
(«!PGLS!»)!semble!être!particulièrement!utilisée.!Dans!sa!forme!originale,!elle!assume!en!
fait! que! les! traits! évoluent! de! façon! brownienne! le! long! de! la! phylogénie,! mais! peut!
théoriquement! incorporer! des! modèles! plus! complexes.! Nous! montrons! dans! cette!
analyse! que! le! PGLS,! dans! sa! forme! actuelle,! peut! faire! de! graves! erreurs! si!
l’hétérogénéité! des! taux! d’évolution! n’est! pas! prise! en! compte! dans! le! modèle.! Nous!
proposons!une!solution!simple!à!ce!problème.!!
!
Note"sur"la"participation"
!
Cet! article! est! le! fruit! d’une! collaboration! avec! Jonathan! T.! Davies! et! Pedro! R!
Peres"Neto,!tout!deux!basés!à!Montréal!(Canada).!Cette!collaboration!a!été!initiée!lors!de!
mes!voyages!en!Amérique!du!Nord!durant!les!étés!2013!et!2014.!
!
!
"!224!"!
"
Harvey)&)Pagel,)91),)) Felsenstein,)04)) O'Meara,$12,$AREES.$
+$revue$ +$revue$ +$revue$
General(review(
1980$ 1990$ 2000$ 2010$
Felsenstein,)85,)Am.)Nat) Mazel)et)al.)15)
Garland)et)al.,)91,)Sys.)Bio) PGLS$(mul'BM,OU)$
+PICs$ +update$PICs$
Rohlf,)01,)Evo.) Revell,)10,)MEE)
Grafen,)89,)PTRSL) MarXns)&)Hansen,) +$PICs$$=$PGLS$ +$PGLS$(λ)$
PICS$+$PGLS$
+Régression$Phylo.$=PGLS$ 97)Am.)Nat.+$GLS$
Freckleton,)02,)Am.)Nat.) Ives$&$Garland$10$Syst.$Biol.$
+$PGLS$(δ,$λ,$κ)$ $+$traits$binaires$
Madison,)90,)Evo.)
Cheverud,)85,)Evo)) +Nouvelle$
Correla3on(between(traits(
!
+$Autocorréla'on$ méthode$$
Others…$
Phylo.$
"!225!"!
Pagel,)99,)Nature)
+$’modèle’$de$transfo.$d’arbre$(δ,$λ,$κ)$
Hansen,)97)Evo.) Butler)&)King.)04) Beaulieu,)Evo.)12) Ingram)&)Malher.)13)

+$modèle$OU$ +update$modèle$OU$ +Mul'$OU$$ +Mul'$OU$fit$
Edwards,)64,$Book$chap.)) O’meara)et)al.)06)/)
+$modèle$BM$ Thomas)et)al.)06) Thomas)et)al.)12)
Traits(Evo.(models(
+Mul'1BM$ +Mul'$BM$$
Encadré( 5.( Chronologie( des( ar3cles( important( dans( le( développement( des( ou3ls( sta3s3ques( pour( l’analyse( des( données(
interspécifique.(Les$ar'cles$sont$groupés$par$sous1disciplines$(en$ligne).$La$frise$ne$prétend$pas$être$une$bibliographie$exhaus've$
mais$permet$simplement$de$donner$un$aperçu$global$de$l’histoire$du$champ$disciplinaire.$
'
Bibliographie'de'l’encadré'5'
Beaulieu,! J.! and! Jhwueng,! D.! 2012.! Modeling! stabilizing! selection:! expanding! the! Ornstein–
Uhlenbeck!model!of!adaptive!evolution.!"!Evolution!(N.!Y).!66:!2369–2383.!
Butler,!M.!A.!and!Kings,!A.!A.!2004.!Phylogenetic!comparative!analysis:!A!modeling!approach!for!
adaptive!evolution.!"!Am.!Nat.!164:!683–695.!
Cheverud,! J.! M.! et! al.! 1985.! The! quantitative! assessment! of! phylogenetic! constraints! in!
comparative!analyses:!sexual!dimorphism!in!body!weight!among!primates.!"!Evolution!(N.!
Y).!39:!1335–1351.!
Edwards,! A.! W.! F.! and! Cavalli"Sforza,! L.! L.! 1964.! Reconstruction! of! evolutionary! trees.! "! In:!
Heywood,!V.!H.!and!McNeill,!J.!(eds),!Phenetic!and!phylogenetic!classification.!pp.!67–76.!
Felsenstein,!J.!1985.!Phylogenies!and!the!comparative!method.!"!Am.!Nat.:!1–15.!
Felsenstein,!J.!2004.!Inferring!Phylogenies.!
Freckleton,! R.! P.! et! al.! 2002.! Phylogenetic! analysis! and! comparative! data:! a! test! and! review! of!
evidence.!"!Am.!Nat.!160:!712–726.!
Garland,! T.! et! al.! 1992.! Procedures! for! the! analysis! of! comparative! data! using! phylogenetically!
independent!contrasts.!"!Syst.!Biol.!41:!18–32.!
Grafen,!A.!1989.!The!phylogenetic!regression.!"!Philos.!Trans.!R.!Soc.!London!B:!119–157.!
Hansen,!T.!F.!1997.!Stabilizing!Selection!and!the!Comparative!Analysis!of!Adaptation.!"!Evolution!
(N.!Y).!51:!1341.!
Harvey,! P.! and! Pagel,! M.! 1991.! the! Comparative! Method! in! Evolutionary! Biology.! "! Oxford!
University!Press.!
Ingram,! T.! and! Mahler,! D.! 2013.! SURFACE:! detecting! convergent! evolution! from! comparative!
data! by! fitting! Ornstein"Uhlenbeck! models! with! stepwise! Akaike! Information! Criterion.! "!
Methods!Ecol.!Evol.!4:!416–425.!
Ives,!A.!and!Garland,!T.!2010.!Phylogenetic!logistic!regression!for!binary!dependent!variables.!"!
Syst.!Biol.!59:!9–26.!
Maddison,!W.!P.!1990.!A!Method!for!Testing!the!Correlated!Evolution!of!Two!Binary!Characters:!
Are!Gains!or!Losses!Concentrated!on!Certain!Branches!of!a!Phylogenetic!Tree?!"!Evolution!
(N.!Y).!44:!223–539–557.!
O’Meara,!B.!2012.!Evolutionary!inferences!from!phylogenies:!a!review!of!methods.!"!Annu.!Rev.!
Ecol.!Evol.!Syst.!43:!267–285.!
O’Meara,! B.! C.! et! al.! 2006.! Testing! for! different! rates! of! continuous! trait! evolution! using!
likelihood.!"!Evolution!(N.!Y).!60:!922–933.!
Pagel,!M.!1999.!Inferring!the!historical!patterns!of!biological!evolution.!"!Nature!401:!877–884.!
Revell,!L.!2010.!Phylogenetic!signal!and!linear!regression!on!species!data.!"!Methods!Ecol.!Evol.!
1:!319–329.!
Rohlf,! F.! J.! 2001.! Comparative! methods! for! the! analysis! of! continuous! variables:! geometric!
interpretations.!"!Evolution!(N.!Y).!55:!2143–2160.!
Thomas,! G.! H.! and! Freckleton,! R.! P.! 2012.! MOTMOT:! models! of! trait! macroevolution! on! trees.!"!
Methods!Ecol.!Evol.!3:!145–151.!
Thomas,! G.! H.! et! al.! 2006.! Comparative! analyses! of! the! influence! of! developmental! mode! on!
phenotypic!diversification!rates!in!shorebirds.!"!Proc.!Biol.!Sci.!273:!1619–24.!
! !
!
"!226!"!
!
Résumé'de'l’article'10'(en'préparation)"
'
Alors! que! l’extraordinaire! diversité! de! la! vie! sur! Terre! a! longtemps! fasciné! les!
biogéographes,! l’importance! relative! de! la! contingence! historique! et! du! déterminisme!
pour! expliquer! son! évolution! reste! débattus.! Le! déterminisme! peut! apparaître! lorsque!
des! lignées! indépendantes! subissant! les! mêmes! contraintes! environnementales!
montrent!des!tendances!évolutives!similaires!et!prédictibles,!comme!c’est!le!cas!avec!les!
convergences.! À! l’échelle! des! mammifères,! les! convergences! entres! placentaires! et!
marsupiaux!servent!souvent!d’exemple!emblématique!mais!n’ont!jamais!été!clairement!
quantifiées.! Dans! cette! analyse,! nous! comparons! les! similarités! fonctionnelles! entre!
espèces!et!entre!assemblages!d’espèces!à!des!attendus!neutres,!c’est"à"dire!produit!par!
la! dérive! génétique! uniquement.! Nous! montrons! qu’il! existe! de! nombreuses!
convergences!au!niveau!des!espèces,!notamment!entre!marsupiaux!et!placentaires.!Par!
ailleurs,! nous! prouvons! que! ces! convergences! sont! transférées! au! niveau! des!
assemblages! entiers! d’espèces,! notamment! entre! l’Australie! et! l’hémisphère! nord,! et!
particulièrement! entre! régions! qui! ont! des! conditions! climatiques! semblables.! Notre!
étude! permet! donc! de! confirmer! quantitativement! des! intuitions! longtemps! restées!
invérifiées.!!
!
"!227!"!
The"global"biogeography"of"non;neutral"trait"evolution"in"mammals"
!
F.!Mazel,!R.!Wüest,!J.!Renaud,!S.!Lavergne!and!W.!Thuiller!
!
Univ.!Grenoble!Alpes,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France.!
CNRS,!Laboratoire!d’Écologie!Alpine!(LECA),!F"38000!Grenoble,!France.!
!
!
Introduction' assemblage! scale! evolutionary! convergence.! In! the!
While! the! extraordinary! diversity! of! life! on! Earth! case! of! mammals,! it! has! been! common! to! use!
has! long! fascinated! biogeographers! (Humbolt! and! species! level! convergence! events! to! suggest! that!
Bonpland! 1805,! Wallace! 1876),! the! relative! placental! and! marsupial! convergences! scale! up! to!
importance! of! historical! contingency! and! entire! assemblages,! for! example! between! Australia!
determinism! in! explaining! its! evolution! remains! and! North! America! (Lomolino! et! al.! 2010).! This!
unresolved! (Simpson! 1944,! Gould! 2002,! Vermeij! expectation!has!never!been!properly!tested.!Instead,!
2006,! Burbrink! et! al.! 2012,! Gillespie! 2013).! arguments! for! assemblage! level! convergence!
Determinism!may!arise!when!independent!lineages! between! Australia! and! North! America! have! been!
experiencing! the! same! environmental! constrain! mostly!graphical!(see!Figure!9!in!the!introduction!of!
show! similar! and! predictable! evolutionary! trends.! this! chapter),! emphazising! remarkable! pairs! of!
In! particular,! evolutionary! theory! predicts! that! highly!convergent!species!(discussed!in!Lomolino!et!
natural! selection! will! drive! the! convergence! of! al.! 2010).! However,! those! examples! does! not!
morphological,! physiological! and/or! behavioural! represent! the! whole! mammalian! fauna! of! the! two!
traits!of!two!unrelated!species!experiencing!similar! continents! but! rather! show! the! most! striking!
environmental! conditions! (Arendt! and! Reznick! examples! of! species! convergence,! and! published!
2008).!This!prediction!have!been!successfully!tested! studies! have! neither! used! quantitative! data! of!
in! recently! isolated! systems! (either! lakes! or! true! functional! trait! of! species,! nor! neutral! expectations!
islands),!with!emblematic!groups!of!species!such!as! of!evolution.!!
cyclid! fishes! (Burbrink! et! al.! 2012),! tetragnatha! !
spiders! (Gillespie! 2004),! anoles! lizards! (Mahler! et! In!this!paper,!we!build!on!the!most!up"to!date!data!
al.! 2013)! or! sticklebacks! (Rundle! et! al.! 2000).! on!functional!traits!and!phylogeny!for!all!mammals!
Species"level! evolutionary! convergence! have! also! of! the! world! (~4600! mammal! species)! to! test! the!
been! documented! at! large! spatial! scales,! for! extent!of!convergence!at!the!assemblage!level.!More!
example! for! fishes! in! the! Pacific! (Ingram! and! Kai! specifically,!we!first!simulate!neutral!trait!evolution!
2014)! or! in! the! Antartic! (Rutschmann! et! al.! 2011),! on! the! worldwide! species"level! phylogeny! and! ask!
salamander!in!North!America!(Kozak!et!al.!2009)!or! whether! observed! functional! distance! between!
desert! rodents! at! a! global! scale! (Mares! 1993).! species! appear! lower! than! expected! under! the!
Nevertheless,! the! extent! at! which! these! neutral! model,! possibly! indicating! deterministic!
evolutionary! trends! are! common! in! nature! and! convergence.! To! scale! up! from! species! to!
contribute! to! the! building! of! species! assemblages! assemblage! level,! we! use! the! IUCN! range! maps!
remain!discussed!(Moen!et!al.!2009,!Lomolino!et!al.! distribution! of! nearly! all! mammals! to! derive!
2010,! Gillespie! 2013).! Unexpectedly,! the! existence! assemblage!composition!worldwide!at!coarse!grain!
of! species"level! convergence! for! entire! and! large! size! (200*200km).! We! then! project! species!
clades! such! as! all! mammals! of! the! world! has! never! assemblages!in!a!multi"dimensional!functional!trait!
been! evaluated! in! a! quantitative! way.! Instead,! it! is! space! (Petchey! and! Gaston! 2006,! Villéger! et! al.!
usually! accepted! that,! for! example,! placental! and! 2008)!and!estimate!the!functional!overlap!between!
marsupial! mammals! harbour! extreme! cases! of! assemblages! using! functional! β! diversity! indices!
species!convergence!(Lomolino!et!al.!2010)!but!this! (Siefert!et!al.!2013).!We!then!take!advantage!of!the!
has! never! been! evaluated! on! entire! species! previously! estimated! neutral! expectations! of!
assemblages! (e.g.! all! species! from! distinct! regions).! species! traits! to! compute! for! each! pair! of!
Indeed,! species"level! convergence! events! are! assemblages,!a!distribution!of!functional!β!diversity!
predicted! to! scale! up! to! convergence! of! entire! expected! under! a! neutral! model! of! trait! evolution.!
assemblages! if! distinct! species! converge! to! similar! We!predict!that!if!evolutionary!convergence!occurs!
ecological!functions!in!distinct!regions!(Ingram!and! at! the! scale! of! species! assemblage,! some! pairs! of!
Kai! 2014).! Some! empirical! work! suggests! that! assemblage! should! show! very! low! functional! β!
assemblage"level!convergence!exist!but!the!amount! diversity! (i.e.! high! similarity)! compared! to! neutral!
of! evidences! remain! scarce.! For! example,! some! phylogenetic! expectations! and! (2)! will! experience!
desert! lizards! (Melville! et! al.! 2006)! and! stream! similar! environmental! conditions! driving!
fishes! (Ibañez! et! al.! 2009)! communities! from! convergent!functional!assemblage!of!species.!!
distantly! related! regions! appear! to! show! !
!
"!228!"!
Results' 2008,!Lomolino!et!al.!2010).!Indeed,!we!found!many!
We! derived! evolutionary! neutral! expectations! for! examples! of! phenotypes! that! have! independently!
mammal!functional!trait!distances!and!showed!that! evolved! in! placentals! and! marsupials! such! as! large!
a! large! number! of! pairs! of! species! harbour! lower! herbivores! (Cetartiodactylae! Vs.! Macropodidae),!
(or,!alternatively!higher)!dissimilarity!that!expected! small! flying,! tree"dwelling! species! (Pteromyni! Vs.!
under! neutral! functional! divergence.! This! suggests! Petaurus)! or! ‘rodent"like’! (Mus! Vs.! Antechinus).!
important! functional! convergences! between! While!our!results!are!not!surprising,!they!represent!
unrelated! species! (or,! alternatively! functional! the! first! attempt! to! qualitatively! test! convergences!
divergences,!see!Fig.!1).!In!particular,!marsupial!and! at! the! scale! of! mammals! with! functional! and!
placental! showed! recurrent! cases! of! convergence! phylogenetic! data! and! an! explicit! neutral! model! of!
toward! some! guilds! such! as! predators,! large! trait!evolution.!
herbivores! or! small! insectivores! (see! Fig.! 1).! Other! We! expected! these! species"level! evolutionary!
cases! of! convergences! occur! within! orders,! for! convergences! to! scale"up! to! entire! assemblages! if!
example!within!Chiroptera!(Supp.!Mat.!2).!! repeated!species!convergence!occurs!in!two!distinct!
We! then! up"scaled! these! neutral! and! observed! assemblages!that!experience!similar!environmental!
species! similarities! to! assemblages! by! deriving! conditions.!In!this!case,!both!assemblages!would!be!
observed! and! neutral! functional! β! diversity.! Lower! independently! built! by! in=situ+ diversification! and!
(/higher)! than! expected! functional! β! diversity! is! multiple! evolutionary! convergence! events! (ISE,!
characterized! by! negative! (/positive)! SES.! Overall,! Moen! et! al.! 2009,! 2013).! Here,! we! found! that,! for!
SES.βsim!values!were!biased!toward!negative!values! mammals! on! a! global! scale,! the! extreme! cases! of!
(median! of! the! all! SES! distribution! is! "0.63)! and! functional! similarities! between! assemblages! often!
significantly! convergent! assemblages! (at! the! 1%! included! one! Australian! assemblage! (Fig! 2D).! As!
threshold)! were! more! that! six! time! more! frequent! Australian! mammals! are! mainly! composed! of!
than! significantly! divergent! assemblages! in! respect! marsupials! (besides! Chiroptera),! we! suggest! that!
to!a!!model!of!pure!neutral!divergence.!Importantly,! evolutionary! convergence! indeed! occurred! at! the!
we! found! that! SES.βsim! was! positively! and! assemblage! level! in! mammals.! Such! convergences!
significantly! related! to! environmental! distances! have!been!already!discovered!for!other!taxa!such!as!
(slope! mean! estimate! 0.16;! 95%! CI:! 0.15"0.17)! desert!lizards!(Melville!et+al.!2006)!or!stream!fishes!
meaning! that! pairs! of! assemblages! experiencing! (Ibañez! et+ al.! 2009).! For! example,! Melville! et+ al.!
similar! environments! tended! to! be! functionally! (2006)! showed! repeated! convergent! evolution!
more! similar! than! expected! under! a! neutral! model! between! one! North! American! and! one! Australian!
of! trait! evolution.! This! trend! appears! to! be! even! assemblage!of!lizards.!In!this!case,!the!two!continent!
more! marked! when! we! only! consider! functionally! are! inhabited! by! two! unrelated! clades! such! as!
similar! assemblages! (see! lower! quantile! regression! migration! between! continent! is! negligible.! As! a!
lines! in! Fig.! 1)! rather! than! functionally! dissimilar! consequence,! lower! functional! dissimilarities! than!
ones! (see! higher! quantile! regression! line! in! Fig.! 1).! expected! under! neutral! evolution! are! likely! the!
We! further! show! that! these! convergent! and! product! of! repeated! evolutionary! convergence!
divergent! pairs! of! assemblages! were! highly! towards! similar! ecological! functions,! which! shaped!
structured!in!space!(Fig.!2).!In!particular,!we!found! functionally! similar! species! assemblages! from! a!
that! convergent! assemblages! disproportionally! distinct!evolutionary!context!!
concerned! those! assemblages! with! very! high! Since! dispersion! of! lineages! between! mammalian!
phylogenetic! beta! diversity! (Fig! 2.C),! notably! assemblages! is! not! negligible,! the! functional!
Australian! versus! northern! temperate! regions! (Fig! similarities! between! assemblages! can! result! from!
2.D).! Divergent! assemblages! appeared! also! two! non"exclusive! processes:! an! in=situ!
geographically!structured!and!associated!temperate! diversification! process! we! just! described! earlier!
and! tropical! assemblages,! in! particular! temperate! (ISE),!but!also!a!process!of!ecologically!conservative!
North! American! and! tropical! South! Asian! dispersion! (ECD,! Moen! et+ al.! 2009,! 2013).! The!
assemblages!(Fig!2.A).!! ecologically! conservative! dispersal! hypothesis!
! postulates! that! (1)! some! lineages! show! less!
Discussion'' similarity! than! expected! under! a! neutral! model! of!
In! this! paper,! we! described! for! the! first! time! the! evolution!because!of!niche!conservatism!(Crisp!and!
evolutionary! convergence! and! divergence! of! Cook! 2012)! and! (2)! important! dispersal! events!
mammalian! species! and! assemblages! at! a! global! allows!it!to!invade!new!assemblages.!In!this!case,!we!
scale.! We! first! assessed! the! degree! of! species! also! expect! that! the! functional! similarity! between!
convergence! using! the! most! up"to! date! data! on! two! invaded! assemblages! will! be! lower! than!
functional! and! phylogenetic! similarities! between! expected! under! a! BM! model! of! evolution.! As! a!
species.! We! observed! important! case! of! consequence,! ECD! processes! may! also! explain! the!
convergence!between!placental!and!marsupial,!as!it! pattern!we!found.!For!example,!at!large!spatial!and!
is! commonly! admitted! (Springer! et! al.! 1997,! Losos! phylogenetic!scales,!Cetartiodactyls!and!Carnivoran!
! "!229!"!
invaded!South!America!(Simpson!1980,!Flynn!1998)! evolutionary! scenarios! shaping! species!

from! North! America,! well! after! acquiring! their! assemblages.! Finally! we! also! found! cases! of! higher!
major! functional! role,! potentially! leading! to! ECD.! than! expected! functional! dissimilarities! between!
Even! at! smaller! spatial! scales,! recent! allopatric! assemblages,!although!to!a!much!lesser!extent!than!
speciation! coupled! with! strong! niche! conservatism! the! reverse.! These! pairs! of! assemblages! appeared!
probably! prevent! species! from! occurring! in! slightly!dissimilar!in!term!of!climates.!Spatially,!they!
secondary! sympatry! due! to! biotic! interactions! mostly! concerned! tropical! versus! temperate!
limiting! local! coexistence! of! functionally! similar! regions,!possibly!indicating!divergent!selection!due!
species! (Pigot! and! Tobias! 2013)! and! lead! to! lower! to!different!climate.!!
functional! turnover! that! one! would! expect! from! a! In!summary!we!show!in!this!paper!that!combining!a!
BM.!As!a!consequence,!it!is!likely!that!the!observed! macro"evolutionary! and! a! macro"ecological!
relationship! between! ecological! convergence! and! approach! lead! to! important! insights! into! the!
environmental!similarity!is!the!product!of!both!ECD! evolutionary!and!ecological!assembly!of!mammalian!
and! ISE.! Nevertheless! we! showed! that! for! extreme! faunas! at! a! global! scale.! Some! future! studies! may!
functional! similarities,! in+ –situ+ diversification! was! want! to! explore! potential! limits! of! our! approach.!
likely! to! be! important! as! in! concerned! the! well" For! example,! we! simulated! here! neutral! evolution!
known! example! of! marsupial! and! placental.! by! using! a! Brownian! model! of! evolution! with! a!
Nevertheless! it! is! true! that! our! analysis! is! not! single!parameter!of!evolutionary!rate.!As!it!is!likely!
designed!to!directly!disentangle!the!relative!role!of! that!heterogeneous!rate!of!trait!evolution!occurs!in!
ISE!and!ECD!because!it!does!not!explicitly!compare! nature!(Simpson!1944),!especially!in!large!datasets!
the!timing!of!colonization/diversification!of!species! (O’Meara!2012),!it!would!be!interesting!to!compare!
and! the! timing! of! functional! evolution! (Moen! et+ al.! this! single"rate! neutral! model! with! a! multi"rate!
2009,! 2013).! Such! analysis! is! beyond! the! scope! of! neutral!model!(Mazel!et!al.!2015).!
this!study!but!may!deserve!future!investigation.!! !
Another! important! result! of! our! study! is! that!
functional! similarities! between! assemblages! were! Acknowledgements'
significantly! related! to! environmental! similarities.!
Ecological! theory! predict! that! niche"based! The! research! leading! to! these! results! had! received!
processes! should! lead! to! functional! similarity! funding!from!the!European!Research!Council!under!
between! assemblages! experiencing! similar! the! European! Community’s! Seven! Framework!
environmental! conditions! while! neutral! theory! Programme! FP7/2007"2013! Grant! Agreement! no.!
(Hubbell!2001)!predict!that!such!similarities!occurs! 281422! (TEEMBIO).! The! authors! of! this! study!
at! random! (Siefert! et+ al.! 2013).! As! a! consequence,! belong! to! the! Laboratoire! d’Écologie! Alpine,! which!
our! results! suggest! that! niche! based! process! may! is!part!of!Labex!OSUG@2020!(ANR10!LABX56).!!
play!an!important!role!in!structuring!the!functional! !
composition! of! mammals! assemblage! at! a! global! !
scale,! either! by! directly! triggering! convergent! trait!
evolution! or! via! environmental! filtering! of! lineages!
experiencing! niche! conservatism.! Note! that! in! this!
analysis,! we! built! a! neutral! model! of! functional!
composition! of! assemblage! worldwide! by!
simulating! traits! evolution! under! a! neutral! model!
(BM).! This! contrast! with! classical! studies! on!
functional! β! diversity! (e.g.! Siefert! et+ al.! 2013)! that!
compared! observed! β! diversity! with! null! and! not!
neutral! expectations! (Gotelli! and! McGill! 2006).! The!
main! difference! is! that! neutral! expectations! derive!
from! analytic! model! of! trait! evolution! while! null!
expectations! derive! from! the! shuffling! of! one!
particular!attribute!of!the!dataset!(for!example,!the!
species!identity!in!the!functional!dendrogram).!The!
use! of! a! neutral! model! as! we! did! here! allows! to!
specifically! emphasize! the! geography! of! (non"
neutral)! trait! evolution! by! merging! classical!
approaches! of! trait! macroevolution! with! a! macro"
ecological! perspective! on! species! assemblages.!
Former!studies!of!species!assemblages!have!mostly!
used! species! shuffling! as! a! null! model,! thus!
hindering! to! highlight! and! contrast! alternative!
! "!230!"!
Marsupials)Vs.)Placental))
−2−10 1 2
1
Devia7ons)of)species))
0 Func7onal)distances)from)
41) )neutral)expecta7ons)(SES))
42)
Examples)of)convergence)(SES<2))
)
Functional distances
viation of Species
)Placentals)/)Marsupials)
)
4)Dama$/)Macropus)(Ar7odactyla)/Diprotodon7a))
4)Ictonyx)/)Dasyurus)(Carnivora)/)Dasyuromorpha))
4)Lepus)/)Lagorchestes)(Lagomorpha)/)Diprotodon7a))
4)Hemiechinus)/)Monodelphis)(Erinaceomorpha)/)Didelphimorphia))
4)Crocidura)/)Sminthopsis)(Soricomorpha)/)Dasyuromorphia))
!
!
Figure'1.'Relationship'between'phylogenetic'and'functional'distances'at'the'scale'of'
mammalian' species.' The!figure!compares!the!phylogenetic!distances!(X"axis,!in!Ma)!and!
the! functional! distance! (Y"axis)! between! all! species! of! mammals! used! in! this! study.! Each!
pair! of! species! is! coloured! according! to! the! deviation! (Standard! Effect! Size)! of! functional!
distance! to! a! neutral! model! of! evolution! (Brownian! motion).! For! placental! vs.! marsupial!
comparison,! we! give! example! of! some! convergent! pairs! of! species! (by! giving! their! genus!
and!order).!
' '
! "!231!"!
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Environemental distance
'
Figure' 2.' Relationship' between' the' functional' and' environmental' dissimilarities' of'
assemblages.!Deviations!of!observed!functional!β!diversity!to!a!neutral!model!of!evolution!
(Standard! Effect! Sizes)! is! plotted! against! environmental! dissimilarities! between!
assemblages! worldwide.! Environmental! dissimilarities! are! Euclidian! distance! between!
assemblages! in! an! environmental! space! of! the! two! first! axes! of! a! PCA! of! all! Worldclim!
variables.!Black!lines!correspond!to!lower!(1%)!and!higher!(99%)!quantile!regression!fits.!
If! the! observed! functional! β! diversity! between! two! assemblages! is! significantly! lower!
(higher)!than!neutral!expectations,!points!are!coloured!in!red!(blue).!!
' '
! "!232!"!
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0.00 0.25 0.50 0.75 0 5 10 15 20

Phylogene&c*Turnover* Geographical*distance*
D*
Convergence
Neutral
Divergence
!
Figure' 3.' Spatial' patterns' of' nonVneutral' functional' dissimilarities' between'
assemblages.!Deviations!of!observed!functional!β!diversity!to!a!neutral!model!of!evolution!
(Standard! Effect! Sizes)! is! plotted! against! phylogenetic! β! diversity! (B)! or! geographical!
distances!(C)!between!assemblages.!The!figure!also!depicts!the!top!1%!highest!and!lowest!
deviations! of! observed! functional! β! diversity! to! neutral! expectations! in! subplot! A! (blue!
lines)!and!D!(red!lines)!respectively.!!
! "!233!"!
Material'and'Method' global! Worldclim! variables.! We! used! the! cube!

' method! (Deville! 2004)! based! on! the! PCA! axes!
Data' scores! and! the! geographic! position! of! each! pixels!
' (see! Supp.! Mat.! 1)! to! select! 200! representative!
Phylogenetic+ and+ functional+ distances+ between+ pixels.!
species+ !
+ SpeciesVlevel'Analysis'
To! derive! the! phylogenetic! distances! between! '
species,! we! used! the! calibrated! and! dated! To! derive! neutral! expectations! of! functional!
ultrametric!phylogenetic!tree!updated!by!Fritz!et!al.! distances!between!species,!we!simulated!100!sets!of!
(2009)! based! on! Bininda"Emonds! et! al.! (2007).! We! traits! values! under! a! neutral! model! of! evolution,!
then! updated! the! tree! by! replacing! the! Carnivora! namely! the! Brownian! Motion! model! (BM;! Edwards!
clade! in! this! phylogeny! with! a! highly! resolved! and! Cavalli"Sforza! 1964).! The! BM! model! explicitly!
supertree! published! more! recently! (Nyakatura! and! simulates! drift! along! the! mammals! phylogenetic!
Bininda"Emonds!2012).! tree! and! is! thus! adequate! to! test! for! convergent!
! evolution!(Melville!et!al.!2006,!Muschick!et!al.!2012,!
To!derive!the!functional!distances!between!species,! Ingram! and! Kai! 2014).! To! calibrate! the! BM! model!
we! used! four! different! types! of! traits! (diet,! body! before! the! simulation,! we! fitted! it! to! each! trait!
mass,! activity! cycle! and! foraging! height)! extracted! independently.! We! then! used! these! fitted!
from!the!online!database!provided!by!Wilman!et!al.! parameters! to! simulate! neutral! traits! values! and! to!
(2014)! which! represents! appropriate! niche! compute,! for! each! pair! of! species,! a! distribution! of!
dimension! within! assemblages! (Belmaker! and! Jetz! neutral!distances.!We!then!assessed!to!which!extent!
2015).!Because!they!ignore!intraspecific!variations,! observed!functional!distances!(see!below)!departed!
we! may! overestimate! niche! overlap! between! from! the! neutral! distribution! by! computing! the!
sympatric! species! but! we! assume! that,! at! the! scale! standard! effect! size! functional! distance,! as!
of! our! study,! intraspecific! variations! remains! traditionally! used! in! the! case! of! null! models! in!
negligible! compared! to! interspecific! variations.! ecology!(Eq.!1):!
Since! we! used! both! continuous! and! discrete! !
variables! we! used! the! Gower! metric! to! compute! !"!. !"#$%&'( =
!"#$%&'(!"# !!"#$ !"#$%&'(!"##
!
distances! between! each! pairs! of! species! using! the! !" !"#$%&'(!"##
function!dist.ktab!of!the!ade4!package!(Pavoine!et!al.! ! ! ! Eq.!1!
2009).! Each! four! category! was! given! equal! weight.! !
For! continuous! variable! (body! mass),! Euclidian! AssemblageVlevel'Analysis'
distance! was! used! while! for! multi"choice! nominal! '
variables,! we! used! the! coefficient! of! Gower! and! β+Diversity+Metric.+
Legendre!(1986).! +
+ To! quantify! the! functional! (and! phylogenetic)!
Distributions+maps+ similarities! between! assemblages! we! used! a!
+ functional! and! phylogenetic! version! of! the! classical!
We! derived! occurrence! data! for! 4616! mammals! Simpson! index.! The! Simpson! index! was! initially!
worldwide! for! 3616! grid! cells! of! approximately! defined!in!term!of!species!similarities!between!two!
200*200! km! using! the! distribution! maps! provided! assemblages!(Eq!2):!
by! the! Mammal! Red! List! Assessment! !
!"#! !,!
(http://www.iucnredlist.org/).! The! best! resolution! !!"# !=" !! ! ! Eq.2!
!!!"#! !,!
to! use! these! maps! is! still! under! discussion! in! the! !
literature! (Storch! et! al.! 2012,! Jenkins! et! al.! 2013).! where!a!=!the!number!of!species!shared!by!the!two!
We!here!used!a!resolution!commonly!used!at!global! grid! cells! and! b! and! c! represent! the! number! of!
scale! (Safi! et! al.! 2011,! Holt! et! al.! 2013).! Domestic,! species! unique! to! each! grid! cell.! It! can! be! easily!
aquatic! and! semi! aquatic! mammals! were! excluded! extended!to!phylogenetic!similarities!by!considering!
from!the!analysis.!! branch!length!instead!of!species!(Bryant!et!al.!2008,!
! Leprieur! et! al.! 2012).! In! this! case,! a! becomes! the!
Stratified+sample+ length!of!branches!shared!by!the!two!grid!cells!and!
+ b! and! c! represent! the! length! of! branches! unique! to!
Because! of! computational! constrains,! we! simplified! each! grid! cell.! In! a! functional! context,! shared!
our!analyses!by!subsampling!200!pixels!out!of!3616.! functional!characteristics!may!be!viewed!in!terms!of!
We! choose! these! pixels! in! order! to! maximise! the! shared! functional! space! (Villéger! et! al.! 2013)! or!
representativeness! of! the! environmental! and! the! shared! functional! dendrogram! branch! lengths!
spatial! space.! The! environmental! space! was! (Petchey! and! Gaston! 2007,! Leprieur! et! al.! 2012).!
summarized! by! the! first! two! axes! of! a! PCA! on! the! Here! we! use! a! functional! dendrogram! to! depict!
! "!234!"!
distance!as!commonly!done!in!the!literature!(Safi!et! set! as! a! random! effect,! fitted! within! a! Bayesian!

al.! 2011,! Thuiller! et! al.! 2014,! Belmaker! and! Jetz! framework!(MCMCglmm,!Hadfield!2010).!Each!MCMC!
2015)! and! because! it! facilitate! comparison! with! chain! was! ran! for! a! total! of! 50,000! generations,!
phylogenetic! similarities.! To! convert! the! functional! retaining! estimated! parameters! every! 25! steps! (we!
distance! into! an! ultrametric! dendrogram,! we! verified! this! yielded! a! low! autocorrelation! between!
applied! a! hierarchical! cluster! algorithm! using! the! estimates),! and! removing! the! first! 25%! sampled!
UPGMA! method! (function! hclust! in! R).! Note! that! parameters!as!a!burnin!period.!
initial! functional! distances! and! (transformed)! '
dendrogram! functional! distances! were! highly! References'
Arendt,! J.! and! Reznick,! D.! 2008.! Convergence! and! parallelism!
correlated! (pearson! mantel! r=0.88,! p=0.001! based!
reconsidered:! what! have! we! learned! about! the! genetics! of!
on!999!permutations).!! adaptation?!"!Trends!Ecol.!Evol.!23:!26–32.!
We! choose! to! use! the! bsim! metric! because! of! two! Baselga,! A.! 2010.! Partitioning! the! turnover! and! nestedness!
reasons.! First,! it! quantifies! the! degree! of! components!of!beta!diversity.!"!Glob.!Ecol.!Biogeogr.!19:!134–
143.!
replacement! of! functional! branch! length! (Gaston!
Belmaker,! J.! and! Jetz,! W.! 2015.! Relative! roles! of! ecological! and!
and! Blackburn! 2008,! Baselga! 2010)! without! being! energetic!constraints,!diversification!rates!and!region!history!
affected! by! the! difference! of! richness! between! on! global! species! richness! gradients! (H! Arita,! Ed.).! "! Ecol.!
assemblages! (Kreft! and! Jetz! 2010,! Holt! et! al.! 2013,! Lett.!18:!563–571.!
Bininda"Emonds,!O.!R.!P.!et!al.!2007.!The!delayed!rise!of!present"
Mouillot!et!al.!2013).!Indeed!it!represents!the!true"
day!mammals.!"!Nature!446:!507–12.!
turnover! component! of! the! widely! used! PhyloSor! Bryant,!J.!A.!et!al.!2008.!Microbes!on!mountainsides:!contrasting!
metric,! the! later! being! a! functional! (phylogenetic)! elevational! patterns! of! bacterial! and! plant! diversity.! "! Proc.!
version!of!the!Sørensen!similarity!metric!(Sørensen! Natl.!Acad.!Sci.!U.!S.!A.!105:!11505–11.!
Burbrink,! F.! T.! et! al.! 2012.! Evidence! for! determinism! in! species!
1948,! Bryant! et! al.! 2008,! Baselga! 2010,! Leprieur! et!
diversification! and! contingency! in! phenotypic! evolution!
al.! 2012).! Second,! it! mainly! quantifies! functional! during!adaptive!radiation.!"!Proc.!Biol.!Sci.!279:!4817–26.!
(resp.! phylogenetic)! turnover! between! functionally! Crisp,! M.! D.! and! Cook,! L.! G.! 2012.! Phylogenetic! niche!
(resp.! phylogenetically)! close! species! in! both! conservatism:! what! are! the! underlying! evolutionary! and!
assemblages! ('terminal'! metric! sensu! Swenson! ecological!causes?!"!New!Phytol.!196:!681–94.!
Deville,!J."C.!2004.!Efficient!balanced!sampling:!The!cube!method.!
2011),! for! example! between! large! herbivores! (or! "!Biometrika!91:!893–912.!
between!close!relatives!in!its!phylogenetic!version).! Edwards,!A.!W.!F.!and!Cavalli"Sforza,!L.!L.!1964.!Reconstruction!of!
This! is! very! important! here! since! we! aim! at! evolutionary!trees.!"!In:!Heywood,!V.!H.!and!McNeill,!J.!(eds),!
Phenetic!and!phylogenetic!classification.!pp.!67–76.!
comparing!similar!functional!types!between!the!two!
Flynn,! J.! 1998.! Recent! advances! in! South! American! mammalian!
assemblages,! and! not! comparing! all! species! of! one! paleontology.!"!Trends!Ecol.!Evol.!13:!449–454.!
assemblage!with!all!species!of!the!other!assemblage,! Fritz,! S.! A.! et! al.! 2009.! Geographical! variation! in! predictors! of!
which! will! be! the! case! if! we! would! have! used! the! mammalian!extinction!risk:!big!is!bad,!but!only!in!the!tropics.!
"!Ecol.!Lett.!12:!538–49.!
COMDIST! (Webb! et! al.! 2008)! or! Pst! metric! (Hardy!
Gaston,! K.! and! Blackburn,! T.! 2008.! Pattern! and! Process! in!
and!Senterre!2007).! Macroecology.!"!Wiley!&!Sons.!
! Gillespie,! R.! 2004.! Community! assembly! through! adaptive!
Observed+and+neutral+β+Diversities.++ radiation!in!Hawaiian!spiders.!"!Science!303:!356–9.!
Gillespie,! R.! G.! 2013.! Adaptive! radiation:! convergence! and! non"
+
equilibrium.!"!Curr.!Biol.!23:!R71–4.!
We! used! βsim! to! compute! observed! functional! and! Gotelli,!N.!and!McGill,!B.!2006.!Null!versus!neutral!models:!what’s!
phylogenetic! turnover! between! assemblages! of! the! the!difference?!"!Ecography!(Cop.).!29:!793–800.!
world.! We! used! our! neutral! trait! expectations! to! Gould,!S.!J.!2002.!The!Structure!of!Evolutionary!Theory.!"!Harvard!
University!Press.!
derive! a! distribution! of! neutral! functional! βsim!
Gower,! J.! C.! and! Legendre,! P.! 1986.! Metric! and! Euclidean!
values!for!each!pair!of!assemblages.!Deviations!from! properties!of!dissimilarity!coefficients.!"!J.!Classif.!3:!5–48.!
these! expectations! were! computed! using! standard! Hadfield,! J.! D.! 2010.! MCMC! Methods! for! Multi"Response!
effect! size! (SES.βsim,! see! Eq.! 1)! and! significance! Generalized! Linear! Mixed! Models:! The! MCMCglmm! R!
assessed! using! the! relative! rank! of! observed! value! Package.!"!J.!Stat.!Softw.!33:!1–22.!
Hardy,! O.! J.! and! Senterre,! B.! 2007.! Characterizing! the!
compared! to! neutral! values! as! we! will! do! under! a! phylogenetic! structure! of! communities! by! an! additive!
null!model.!! partitioning!of!phylogenetic!diversity.!"!J.!Ecol.!95:!493–506.!
! Holt,! B.! G.! et! al.! 2013.! An! Update! of! Wallace’s! Zoogeographic!
Regions!of!the!World.!"!Science!(80".!).!339:!74–78.!
Statistical+ relationships+ between+ assemblage+
Hubbell,! S.! 2001.! The! unified! neutral! theory! of! biodiversity! and!
convergence+and+environment++ biogeography.!"!Princeton!University!Press.!
+ Humbolt,! A.! von! and! Bonpland,! A.! 1805.! Essai! sur! la! géographie!
To!relate!SES.βsim!to!environmental!dissimilarities!we! des!plantes :!accompagné!d’un!tableau!physique!des!régions!
équinoxiales,! fondé! sur! des! mesures! exécutées,! depuis! le!
used! two! approaches.! First,! we! fitted! quantile!
dixième!degré!de!latitude!boréale!jusqu'au!dixième!degré!de!
regressions! using! the! rq! function! of! the! quantreg+ R! latitude! australe,! pendant! les! années! 1799,! 1800,! 1801,.! "!
package.! Because! the! observations! are! not! Levrault!Schoell,!Paris.!
statistically! independent! from! each! other! (they! Ibañez,! C.! et! al.! 2009.! Convergence! of! temperate! and! tropical!
stream!fish!assemblages.!"!Ecography!(Cop.).!32:!658–670.!
corresponds! to! pairs! of! assemblages),! we! also! used!
generalized! linear! mixed! models! with! pairs! of! sites!
! "!235!"!
Ingram,! T.! and! Kai,! Y.! 2014.! The! geography! of! morphological! Petchey,! O.! L.! and! Gaston,! K.! J.! 2007.! Dendrograms! and!
convergence!in!the!radiations!of!Pacific!Sebastes!rockfishes.!"! measuring!functional!diversity.!"!Oikos!116:!1422–1426.!
Am.!Nat.!184:!E115–31.! Pigot,!A.!L.!and!Tobias,!J.!A.!2013.!Species!interactions!constrain!
Jenkins,!C.!N.!et!al.!2013.!Global!patterns!of!terrestrial!vertebrate! geographic! range! expansion! over! evolutionary! time.! "! Ecol.!
diversity!and!conservation.!"!Proc.!Natl.!Acad.!Sci.!U.!S.!A.!110:! Lett.!16:!330–8.!
E2602–2610.! Rundle,!H.!D.!et!al.!2000.!Natural!selection!and!parallel!speciation!
Kozak,! K.! H.! et! al.! 2009.! Can! parallel! diversification! occur! in! in!sympatric!sticklebacks.!"!Science!287:!306–8.!
sympatry?! Repeated! patterns! of! body"size! evolution! in! Rutschmann,! S.! et! al.! 2011.! Parallel! ecological! diversification! in!
coexisting!clades!of!north!american!salamenders.!"!Evolution! Antarctic! notothenioid! fishes! as! evidence! for! adaptive!
(N.!Y).!63:!1769–1784.! radiation.!"!Mol.!Ecol.!20:!4707–21.!
Kreft,! H.! and! Jetz,! W.! 2010.! A! framework! for! delineating! Safi,!K.!et!al.!2011.!Understanding!global!patterns!of!mammalian!
biogeographical! regions! based! on! species! distributions.! "! J.! functional!and!phylogenetic!diversity.!"!Philos.!Trans.!R.!Soc.!
Biogeogr.!37:!2029–2053.! London,!Ser.!B!366:!2536–2544.!
Leprieur,! F.! et! al.! 2012.! Quantifying! phylogenetic! beta! diversity:! Siefert,! A.! et! al.! 2013.! Functional! beta"diversity! patterns! reveal!
distinguishing! between! “true”! turnover! of! lineages! and! deterministic! community! assembly! processes! in! eastern!
phylogenetic!diversity!gradients.!"!PLoS!One!7:!e42760.! North!American!trees.!"!Glob.!Ecol.!Biogeogr.!22:!682–691.!
Lomolino,!M.!V.!et!al.!2010.!Biogeography.!"!Sinauer!Associates.! Simpson,! G.! G.! 1944.! Tempo! and! Mode! in! Evolution.! "! Columbia!
Losos,! J.! B.! 2008.! Phylogenetic! niche! conservatism,! phylogenetic! University!Press.!
signal! and! the! relationship! between! phylogenetic! Simpson,! G.! G.! 1980.! Splendid! isolation :! the! curious! history! of!
relatedness! and! ecological! similarity! among! species.! "! Ecol.! South! American! mammals.! "! New! Haven :! Yale! University!
Lett.!11:!995–1003.! Press.!
Mahler,! D.! et! al.! 2013.! Exceptional! convergence! on! the! Sørensen,! T.! 1948.! A! method! of! establishing! groups! of! equal!
macroevolutionary! landscape! in! island! lizard! radiations.! "! amplitude! in! plant! sociology! based! on! similarity! of! species!
Science!(80".!).!341:!292–295.! content! and! its! application! to! analyses! of! the! vegetation! on!
Mares,! M.! A.! 1993.! Desert! rodents,! seed! consumption,! and! Danish!commons.!"!I!kommission!hos!E.!Munksgaard.!
convergence :! evolutionary! shuffling! of! adaptations.! "! Springer,!M.!S.!et!al.!1997.!The!chronicle!of!marsupial!evolution.!"!
Bioscience!43:!372–379.! In:!Givinish,!T.!and!Sytsma,!K.!(eds),!Molecular!Evolution!and!
Mazel,! F.! et! al.! 2015.! Improving! phylogenetic! regression! under! Adaptive! Radiations.! Cambridge! University! Press.,! pp.! 129–
compex!models!of!eviolution.!Ecology.!Accepted! 161.!
Melville,! J.! et! al.! 2006.! Intercontinental! community! convergence! Storch,! D.! et! al.! 2012.! Universal! species"area! and! endemics"area!
of!ecology!and!morphology!in!desert!lizards.!"!Proc.!Biol.!Sci.! relationships!at!continental!scales.!"!Nature!488:!78–81.!
273:!557–63.! Swenson,! N.! G.! 2011.! Phylogenetic! beta! diversity! metrics,! trait!
Moen,! D.! S.! et! al.! 2009.! Community! assembly! through! evolution! and! inferring! the! functional! beta! diversity! of!
evolutionary! diversification! and! dispersal! in! Middle! communities.!"!PLoS!One!6:!e21264.!
American!treefrogs.!"!Evolution!63:!3228–47.! Thuiller,!W.!et!al.!2014.!The!European!functional!tree!of!bird!life!
Moen,! D.! S.! et! al.! 2013.! Evolutionary! conservatism! and! in!the!face!of!global!change.!"!Nat.!Commun.!5:!3118.!
convergence! both! lead! to! striking! similarity! in! ecology,! Vermeij,! G.! J.! 2006.! Historical! contingency! and! the! purported!
morphology! and! performance! across! continents! in! frogs.! "! uniqueness! of! evolutionary! innovations.! "! Proc.! Natl.! Acad.!
Proc.!Biol.!Sci.!280:!20132156.! Sci.!U.!S.!A.!103:!1804–9.!
Mouillot,! D.! et! al.! 2013.! The! challenge! of! delineating! Villéger,!S.!et!al.!2008.!New!multidimensional!functional!diversity!
biogeographical!regions:!nestedness!matters!for!Indo"Pacific! indices!for!a!multifaceted!framework!in!functional!ecology.!"!
coral!reef!fishes!(W!Jetz,!Ed.).!"!J.!Biogeogr.!40:!2228–2237.! Ecology!89:!2290–2301.!
Muschick,! M.! et! al.! 2012.! Convergent! evolution! within! an! Villéger,! S.! et! al.! 2013.! Decomposing! functional! β"diversity!
adaptive!radiation!of!cichlid!fishes.!"!Curr.!Biol.!22:!2362–8.! reveals! that! low! functional! β"diversity! is! driven! by! low!
Nyakatura,! K.! and! Bininda"Emonds,! O.! R.! P.! 2012.! Updating! the! functional! turnover! in! European! fish! assemblages.! "! Glob.!
evolutionary! history! of! Carnivora! (Mammalia):! a! new! Ecol.!Biogeogr.!22:!671–681.!
species"level! supertree! complete! with! divergence! time! Wallace,! A.! 1876.! The! geographical! distribution! of! animals.! "!
estimates.!"!BMC!Biol.!10:!12.! Cambride!Univ.!Press.!
O’Meara,! B.! 2012.! Evolutionary! inferences! from! phylogenies:! a! Webb,! C.! O.! et! al.! 2008.! Phylocom:! software! for! the! analysis! of!
review!of!methods.!"!Annu.!Rev.!Ecol.!Evol.!Syst.!43:!267–285.! phylogenetic! community! structure! and! trait! evolution.! "!
Pavoine,!S.!et!al.!2009.!On!the!challenge!of!treating!various!types! Bioinformatics!24:!2098–2100.!
of! variables:! application! for! improving! the! measurement! of! Wilman,! H.! et! al.! 2014.! EltonTraits! 1.0:! Species"level! foraging!
functional!diversity.!"!Oikos!118:!391–402.! attributes! of! the! world’s! birds! and! mammals.! "! Ecology! 95:!
Petchey,!O.!L.!and!Gaston,!K.!J.!2006.!Functional!diversity:!back!to! 2027–2027.!
basics!and!looking!forward.!"!Ecol.!Lett.!9:!741–758.!
! "!236!"!
Partie!III.2!!
'
'
! "!237!"!
'
DE'LA'SOUSVPARTIE'III.2'
'
'
Dans! cette! dernière! partie,! nous! proposons! de! nouvelles! solutions!
méthodologiques!pour!détecter!la!convergence!au!niveau!des!espèces!(annexe!4).!Nous!
étudions! ensuite! la! convergence! au! niveau! des! assemblages! pour! les! mammifères! à!
travers!le!monde.!!
!
Il! est! important! de! souligner! que! l’analyse! du! chapitre! VII! ne! suit! pas! les!
recommandations! de! l’annexe! 3.2.1! et! qu’il! faudra! donc! veiller! à! vérifier! nos! résultats.!
En! effet,! nous! montrons! dans! l’annexe! 3.2.1! que! l’hétérogénéité! des! taux! d’évolution!
browniens! est! un! processus! important! à! prendre! en! compte! pour! modéliser! de! façon!
fidèle! une! évolution! neutre.! Dans! l’état! actuel! de! l’analyse! des! convergences! de!
mammifères,! nous! ne! prenons! pas! en! compte! cette! possibilité! ce! qui! impacte!
probablement!certaines!de!nos!conclusions.!Je!pense!cependant!que!la!convergence!(au!
niveau!des!espèces!et!au!niveau!des!assemblages)!entre!marsupiaux!et!placentaires!ne!
reflète! pas! cette! variabilité! des! taux! d’évolution.! Il! faudra! cependant! développer! des!
attentes!neutres!relaxant!l’hypothèse!d’homogénéité!des!taux!d’évolution!pour!en!avoir!
le!cœur!net.!
!
! "!238!"!
!
! "!239!"!
Partie!III!–!Synthèse!générale!
DE'LA'PARTIE'III'
! "!240!"!
!
!
La! Partie! III! de! ma! thèse! visait! à! mieux! comprendre! la! distribution! spatiale! des!
mammifères!et!des!oiseaux!à!l’échelle!du!globe!en!tirant!profit!de!l’utilisation!des!indices!
de! diversité! phylogénétique! et! fonctionnelle.! Cette! discussion! s’attache! à! rappeler! les!
principaux!résultats!de!cette!partie!en!les!reliant!à!quelques!perspectives!de!travail.!En!
particulier,!je!discute!l’intérêt!de!l’importance!de!l’échelle!spatiale,!de!la!comparaison!de!
groupes!différents,!et!de!nouvelles!perspectives!de!comparaison!entre!PD!et!FD.!!
!
!
1.'Travailler'à'différentes'échelles'spatiales'
!
Dans! cette! partie! III,! nous! nous! sommes! contentés! de! travailler! à! une! seule!
échelle!spatiale,!mais!il!apparaît!que!l’importance!relative!des!processus!historiques!et!
écologiques!peut!varier!le!long!de!l’échelle!spatiale!(Levin!1992;!Chave!2013).!Ainsi,!on!
pourrait!réanalyser!les!profils!de!BDTT!à!différentes!résolutions!spatiales,!par!exemple,!
en! utilisant! les! grains! d’études! utilisés! dans! le! chapitre! III! (article! 4,! de! 100*100km! à!
1000*1000km).! On! pourrait! par! exemple! s’attendre! à! avoir! un! effet! prédominant! de!
l’histoire!à!vaste!échelle!spatiale!et!un!effet!prédominant!de!l’environnement!à!échelle!
intermédiaire.!!
!
2.'Comparer'la'BDTT'de'groupes'taxonomiques'distincts'
+
2.1."En"biogéographie"à"large"échelle"
+
La! sous"partie! III.1! montre! comment! une! description! de! la! composition! des!
assemblages! à! plusieurs! échelles! phylogénétiques! permet! de! décortiquer! l’influence!
relative! de! différents! processus! majeurs,! notamment! les! processus! de! type! historique!
(dispersion! à! large! échelle,! vicariance)! et! les! processus! écologiques! liés! à! la! niche! des!
espèces.! En! particulier,! nous! montrons! comment! ceux"ci! peuvent! avoir! des! effets!
emboîtés! ou! indépendants! le! long! de! l’échelle! phylogénétique!:! la! biogéographie!
historique! conditionne! la! distribution! des! lignées! à! large! échelle! phylogénétique! alors!
que! les! processus! de! niche! la! conditionnent! à! plus! fines! échelles.! En! définitive,! cette!
! "!241!"!
interprétation! est! en! accord! avec! le! fait! que! l’histoire! conditionne! la! formation! des!
royaumes! (Kreft! &! Jetz! 2010;! Holt! et+ al.! 2013),! et! qu’à! l’intérieur! de! ces! royaumes!
l’environnement! définit! des! biomes! différents! qui! présentent! des! faunes! distinctes,!
adaptées!à!leurs!conditions!environnementales.!En!fait,!nos!résultats!soutiennent!cette!
interprétation! pour! les! mammifères,! mais! pas! pour! les! oiseaux.! Pour! ces! derniers,! il!
apparaît! en! effet! que! les! processus! de! type! historique! sont! moins! importants! à! large!
échelle!phylogénétique.!On!peut!tenter!de!relier!ces!résultats!avec!les!capacités!relatives!
de!dispersion!des!mammifères!et!des!oiseaux.!Il!est!en!effet!possible!que!des!capacités!
supérieures! de! dispersion! conduisent! à! un! effacement! du! signal! de! biogéographie!
historique! dans! les! branches! profondes! de! l’arbre.! En! effet,! des! évènements! de!
colonisation! multiples! vont! potentiellement! homogénéiser! la! distribution! des! lignées!
profondes!et!brouiller!le!signal!de!l’histoire!ancienne!sur!les!patrons!actuels.!De!manière!
générale,!les!oiseaux!semblent!en!effet!dotés!de!meilleures!capacités!de!dispersion!que!
les! mammifères,! ce! qui! permet! d’expliquer! l’absence! de! signal! historique! pour! les!
oiseaux,! mais! pas! pour! les! mammifères.! Par! ailleurs,! l’effet! de! la! proximité! historique!
des! continents! a! laissé! une! empreinte! dans! les! distributions! actuelles! de! mammifères,!
mais!pas!sur!celles!des!oiseaux,!comme!attendu.!En!définitive,!il!est!donc!intéressant!de!
contraster! les! importances! relatives! de! différents! processus! entre! groupes! aux!
caractéristiques!écologiques!différentes.!C’est!par!exemple!ce!que!proposent!Sanmartín!
&!Ronquist!(2004)!en!comparant!l’histoire!biogéographique!des!plantes!et!des!animaux!
dans! l’hémisphère! sud! et! en! montrant! que! la! distribution! des! animaux! est! le! produit!
d’une!vicariance!ancienne!alors!que!celle!des!végétaux!est!davantage!conditionnée!par!
les! multiples! évènements! de! dispersion! récents.! De! telles! comparaisons! représentent!
des!pistes!de!travail!intéressantes!pour!le!futur.!Au!sein!des!mammifères!et!des!oiseaux,!
l’analyse! de! la! variabilité! entre! les! ordres! (Figure! 2! du! matériel! supplémentaire! 3.1.1)!
révèle! d’ores! et! déjà! des! résultats! intéressants! qui! mériteront! d’être! creusés.! En!
particulier,!il!apparaît!intéressant!de!contraster!la!variabilité!de!l’effet!de!l’espace!et!de!
l’environnement!!sur!les!profils!de!BDTT.!On!peut!prédire!que!les!effets!géographiques!
(interprétés! ici! comme! historiques)! seront! davantage! variables! que! les! effets!
environnementaux,! car! ils! dépendent! d’évènements! rares,! difficiles! à! prévoir!
(«!contingent!»)!alors!que!les!processus!de!niches!devraient!être!plus!constants,!car!ils!
sont! déterministes.! Cependant,! on! pourrait! aussi! supposer! que! les! effets! historiques!
entre!les!ordres!dépendent!des!caractéristiques!de!dispersion!de!ces!ordres.!Au"delà!des!
! "!242!"!
mammifères! et! des! oiseaux,! il! existe! quelques! groupes! pour! lesquels! des! données!
géographiques,! phylogénétiques! et! parfois! fonctionnelles! existent! à! l’échelle! du! globe.!
On!pourrait!par!exemple!ajouter!à!notre!analyse!des!groupes!taxonomiques!tels!que!les!
poissons!coralliens!(Mouillot!et+al.!2013)!ou!les!champignons!(Tedersoo!et+al.!2014).!
!
!
2.2."En"microbiologie,"pour"l’étude"des"microbiotes"
!
Nous! montrons! dans! le! chapitre! VI! comment! une! analyse! BDTT! permet! de!
préciser!l’importance!relative!de!la!phylogénie!et!du!régime!alimentaire!de!l’hôte!sur!la!
composition!du!microbiote!intestinal.!Nous!montrons!même!que!ces!conclusions!restent!
valides! dans! les! deux! sous! clades! majoritaires! de! notre! analyse,! c’est"à"dire! les!
Firmicutes! et! les! Bacteroidetes! (voir! les! figures! supplémentaires! 12! et! 13! en! annexe!
3.1.2).!Cependant,!il!serait!intéressant!de!se!demander!si!certains!clades!bactériens!ont!
plutôt! tendance! à! être! liés! au! régime! alimentaire! de! l’hôte,! ou! suivent! plutôt! la!
phylogénie.! Dans! ce! dernier! cas! par! exemple,! il! serait! intéressant! de! regarder! la!
distribution! des! OTUs! à! forte! transmission! verticale! (ou! horizontale)! au! sein! de! la!
phylogénie! des! bactéries,! dans! un! premier! en! temps! en! caractérisant! le! signal!
phylogénétique! du! type! de! transmission! et! ensuite! en! tentant! de! relier! ces! taux! aux!
caractéristiques! fonctionnelles! des! bactéries! (capacité! de! dispersion! par! exemple).! Par!
ailleurs!on!pourrait!tester!si!ces!lignées!qui!co"spécient!beaucoup!avec!l’hôte!(i.e.!celles!
liées!à!la!phylogénie!de!l’hôte)!sont!aussi!celles!pour!lesquelles!il!a!été!montré!une!forte!
héritabilité! en! intraspécifique! (voir! Goodrich! et+ al.,! 2014,! pour! le! cas! humain).! En!
d’autres!termes,!observe"t"on!un!lien!entre!micro!et!macroévolution!dans!ce!cas!?!!
!
!
Par! ailleurs,! nous! avons! limité! notre! étude! au! seul! microbiote! intestinal.!
Cependant,! il! en! existe! d’autres! chez! les! animaux,! comme! ceux! de! la! peau! ou! de! la!
bouche.! Il! serait! donc! intéressant! de! les! inclure! dans! les! futures! analyses! afin! de!
proposer!une!vision!plus!complète!de!l’évolution!de!l’ensemble!de!notre!microbiote.!!
!
!
!
! "!243!"!
3.'Combiner'les'diversités'phylogénétique'et'fonctionnelle'
+
L’utilisation! combinée! des! diversités! phylogénétique! et! fonctionnelle! est!
prometteuse.! Dans! cette! partie,! je! discute! dans! un! premier! temps! l’avènement! des!
données! fonctionnelles! en! microbiologie! et! dans! un! second! temps! je! propose! des!
perspectives!sur!la!façon!d’utiliser!les!deux!facettes!conjointement.!!
+
3.1." Combiner" les" informations" fonctionnelles" et" phylogénétiques" dans" l’étude" des"
microbiotes""
!
Notre! analyse! des! microbiotes! intestinaux! de! mammifères! s’est! basée! sur! la!
composition! phylogénétique! des! assemblages! (en! utilisant! une! phylogénie! des!
séquences! d’ARN! ribosomal! 16S)! et! leur! lien! avec! les! caractéristiques! de! l’hôte.!
Cependant,!tout!comme!l’analyse!biogéographique!de!la!même!sous"partie!(chapitre!VI),!
nous! n’avons! pas! utilisé! de! données! fonctionnelles! qui! pourraient! pourtant! préciser! la!
nature!des!liens!entre!hôtes!et!symbiontes.!Étant!donné!qu’il!reste!difficile!de!cultiver!en!
laboratoire!la!plupart!des!bactéries!du!tractus!intestinal!des!mammifères,!on!ne!peut!pas!
mesurer! directement! les! caractéristiques! fonctionnelles! des! OTUS! bactériens.!
Cependant,!il!est!possible!d’estimer!le!contenu!génique!des!microbiotes!(c’est"à"dire!le!
microbiome*),! notamment! via! le! séquençage! métagénomique! de! nouvelle! génération!
(shotgun).!Même!si!la!présence!d’un!gène!ne!garantit!en!aucun!cas!qu’il!soit!transcrit!en!
ARN,! traduit! en! protéines,! et! donc! qu’il! participe! au! phénotype! de! la! bactérie,! il! s’agit!
d’une! première! approche! intéressante! (Lozupone! et+al.! 2012).! Par! exemple,! Muegge! et+
al.!(2011)!montrent!que!les!microbiotes!des!mammifères!herbivores!et!des!carnivores!
contiennent! des! gènes! très! différents.! En! particulier,! ils! montrent! que! les! herbivores!
possèdent!davantage!d’enzymes!anaboliques!des!acides!aminés!alors!que!les!carnivores!
contiennent! davantage! d’enzymes! cataboliques.! En! d’autres! termes,! les! herbivores!
possèdent! un! microbiote! qui! les! aide! à! construire! des! acides! aminés! à! partir! de!
composés! carbonés! plus! simples! alors! que! les! carnivores! ont! un! microbiote! qui! leur!
permet! plutôt! de! cataboliser! les! acides! aminés! pour! en! retirer! de! l’énergie.! Ceci!
correspond! bien! au! fait! que! le! régime! alimentaire! des! carnivores! est! riche! en! acide!
aminé,! au! contraire! des! herbivores.! Ceci! représente! donc! un! formidable! exemple! de!
coévolution! entre! les! hôtes! et! leur! symbiontes,! qui! n’aurait! pas! pu! être! révélé! par!
! "!244!"!
l’analyse!des!seules!séquences!16S.!De!façon!générale,!il!semble!que!les!fonctions!soient!
généralement!conservées!alors!que!les!lignées!bactériennes!ne!le!sont!pas!(Lozupone!et+
al.!2012).!Il!serait!alors!intéressant!de!se!demander!(1)!à!quel!point!les!fonctions!sont!
généralement! conservées!?! (L’équivalent! du! débat! sur! la! prévalence! du! conservatisme!
de! niche! en! macroévolution),! (2)! sont"elles! conservées! à! différentes! échelles!
phylogénétiques!?! (3)! À! quel! point! ce! conservatisme! varie"t"il! en! fonction! de! l’échelle!
phylogénétique! et! de! la! fonction! considérée!(par! exemple,! la! fonction! ribosomale! est!
forcément!très!largement!conservée)!?!!
!
!
3.2."Expliciter"les"modèles"macro;évolutifs"en"biogéographie"
!
La! sous"partie! III.2! tente! de! croiser! l’information! phylogénétique! et! l’information!
fonctionnelle!pour!mieux!comprendre!l’évolution!des!traits!et!leur!répercussion!sur!les!
patrons! biogéographiques.! En! général,! l‘utilisation! conjointe! de! la! PD! et! de! la! FD!
propose! de! contraster! leurs! valeurs,! mais! sans! faire! directement! appel! à! des! modèles!
d’évolution! explicites! (Safi! et+ al.! 2011;! Weinstein! et+ al.! 2014).! Par! exemple,! Safi! et+ al.!
(2011)!utilisent!un!modèle!additif!généralisé!(GAM)!pour!modéliser!la!relation!entre!la!
PD! (Faith! 1992)! et! la! FD! (Petchey! &! Gaston! 2007)! et! en! déduire! des! résidus! de! FD!
indépendants! de! la! PD.! Il! apparaît! ainsi! que! les! zones! tropicales! possèdent! moins! de!
diversité! fonctionnelle! «!qu’attendu!»! selon! leur! diversité! phylogénétique,! ce! qui! selon!
les!auteurs!pourrait!être!le!résultat!d’une!extinction!plus!importante!ou!d’une!évolution!
plus! rapide! dans! les! régions! tempérées! et! d’une! évolution! plus! lente! dans! les! régions!
tropicales! («!niche! conservatism!»).! Ceci! représente! un! premier! pas! important! dans!
l’analyse! conjointe! des! diversités! phylogénétiques! et! fonctionnelles! à! large! échelle!
spatiale.! Cependant,! je! pense! que! l’on! pourrait! tirer! profit! de! l’utilisation! de! modèles!
d’évolution! développés! en! macroévolution.! En! effet,! de! tels! modèles! permettent! de!
tester! différents! scénarii! d’évolution! avec! des! hypothèses! claires! et! précises! et!
représentent!donc!le!lien!direct!entre!l’espace!fonctionnel!et!l’arbre!phylogénétique.!Par!
exemple! le! modèle! brownien! (Edwards! &! Cavalli"Sforza! 1964)! et! ses! diverses!
extensions!(Pagel!1999;!Eastman!et+al.!2011)!permettent!de!modéliser!l’effet!de!dérive!
seule! et! représentent! donc! des! modèles! de! choix! pour! étudier! les! déviations! à! la!
neutralité.! Le! modèle! d’Ornstein=Uhlenbeck+ (Hansen! 1997)! permet! lui! de! modéliser! la!
! "!245!"!
sélection! stabilisante,! mais! aussi! les! convergences! évolutives! (Ingram! &! Kai! 2014).! En!
utilisant!de!tels!outils,!je!pense!que!l’on!pourrait!relier!de!façon!plus!claire!la!PD!et!la!FD,!
notamment! en! explicitant! une! FD! attendue! en! fonction! d’une! phylogénie,! d’une!
répartition!spatiale!et!d’un!modèle!d’évolution.!Il!me!semble!qu’avec!cette!approche,!on!
peut!aller!plus!loin!dans!la!compréhension!des!processus!sous"jacents,!puisque!l’on!ne!
s’intéresse! pas! uniquement! à! l’éradication! de! «+l’effet! de! la! phylogénie+»,! mais! bien! à!
décrire! explicitement! les! processus! en! jeu! et! les! hypothèses! que! l’on! assume.! En!
macroévolution,! cette! dichotomie! d’approche! se! reflète! notamment! dans! les! méthodes!
utilisées,! qui! peuvent! être! explicites! sur! les! processus! modélisés! (voir! les! différents!
modèles! présentés! plus! haut)! ou! non! (voir! par! exemple! les! techniques! de! vecteur!
propres! phylogénétiques,! Diniz"Filho! et+al.! 1998).! Il! apparaît! que! lorsque! des! modèles!
explicites! sont! disponibles,! leur! utilisation! devrait! être! préférée! (voir! Freckleton! et+al.!
2011! pour! une! critique! des! modèles! non! explicites! en! macroévolution).! C’est!
notamment!ce!que!j’ai!tenté!de!faire!dans!le!chapitre!VII!de!cette!thèse!en!comparant!un!
modèle! neutre! explicite! aux! données! observées! (mais! voir! la! synthèse! du! chapitre! VII!
pour!!une!discussion!plus!détaillée!sur!le!type!de!modèle!neutre!à!utiliser).!+
Dans!certains!cas,!les!modèles!explicites!n’existent!tout!simplement!pas!et!on!se!
cantonne! généralement! à! «!gommer!»! l’effet! de! ces! processus,! qui! sont! alors! souvent!
perçus!comme!«!indésirables!».!Deux!exemples!indépendants!sur!la!considération!de!la!
dispersion!en!biogéographie!appuient!cette!proposition.!!
!
(1)! Le! premier! provient! du! traitement! de! la! dimension! spatiale! en! biogéographie!
écologique.! Dans! ce! domaine,! de! nombreuses! études! tentent! de! relier! des! variables!
écologiques! (présence! ou! abondance! d’espèces,! richesse! spécifique)! aux! variables!
environnementales,! notamment! afin! de! confirmer! l’importance! de! la! niche! écologique.!
La!dimension!spatiale!de!l’analyse!est!souvent!réduite!à!un!«!danger!»!que!l’on!appelle!
l’autocorrélation!spatiale*!(Dormann!et+al.!2007)!qui!peut!systématiquement!biaiser!les!
tests!de!significativité.!Ainsi,!il!s’agit!souvent!de!retirer!cet!effet!spatial,!qui!peut!être!le!
résultat!de!la!dispersion!limitée!ou!des!interactions!biotiques,!mais!pas!de!le!modéliser!
explicitement!(Peres"Neto!&!Legendre!2010;!Dray!et+al.!2012).!
!
(2)! Le! deuxième! provient! du! traitement! de! la! dispersion! en! biogéographie! historique.!
Dans! ce! domaine,! on! retrouve! deux! écoles! de! pensées! dont! les! approches! (Sanmartín!
! "!246!"!
2012)! considèrent! la! dispersion! soit! comme! un! bruit! de! fond! sans! intérêt! (modèles!
«!process"based!»,! Morrone! 2009),! soit! comme! un! processus! à! part! entière! (modèles!
«!event"based!»,!Ronquist!&!Sanmartín!2011).!!
!
En!définitive,!l’utilisation!de!modèles!explicites!n’est!pas!toujours!possible,!car!il!
n’existe! pas! pour! tous! les! systèmes! d’études,! et! notamment! pour! les! plus! complexes.!
Ceci!est!typiquement!le!cas!en!écologie!des!communautés,!où!il!n’existe!pas!de!modèle!
mathématique! explicite! à! comparer! aux! observations! et! les! modèles! nuls! (ou! un! des!
paramètres! des! données! est! randomisé)! sont! davantage! utilisés! (voir! Gotelli! &! McGill!
2006! pour! une! discussion! sur! la! différence! entre! modèles! nuls! et! modèles! neutres).!
Cependant,! des! modèles! explicitement! neutres! commencent! à! émerger,! notamment! le!
modèle!neutre!de!Hubbel!(Hubbell!2001;!Rosindell!et+al.!2011;!mais!voir!aussi!Pigot!&!
Etienne!2014;!O’Dwyer!et+al.!2015)!et!semblent!prometteurs.!
!
! "!247!"!
Partie!III!–!Bibliographie!
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composition?!Diversity+and+Distributions,!15,!450–458.!
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206.!
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Botanical+Garden,!245–257.!
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Taxonomic,! phylogenetic,! and! trait! Beta! diversity! in! South! American! hummingbirds.! The+American+
naturalist,!184,!211–24.!
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Ecology+and+Evolution,!19,!639–644.!
Woodburne,!M.O.!(2010).!The!Great!American!Biotic!Interchange:!Dispersals,!Tectonics,!Climate,!Sea!Level!
and!Holding!Pens.!Journal+of+mammalian+evolution,!17,!245–264.!
Yatsunenko,!T.,!Rey,!F.E.,!Manary,!M.J.,!Trehan,!I.,!Dominguez"Bello,!M.G.,!Contreras,!M.,!Magris,!M.,!Hidalgo,!
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Lozupone,! C.A.,! Lauber,! C.,! Clemente,! J.C.,! Knights,! D.,! Knight,! R.! &! Gordon,! J.I.! (2012).! Human! gut!
microbiome!viewed!across!age!and!geography.!Nature,!486,!222–7.!
Zachos,!J.,!Pagani,!M.,!Sloan,!L.,!Thomas,!E.!&!Billups,!K.!(2001).!Trends,!rhythms,!and!aberrations!in!global!
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!
! "!251!"!
!
! "!252!"!
!
! "!253!"!
Conclusion!générale!de!la!thèse!
CONCLUSION'GÉNÉRALE'
! "!254!"!
1.'Rappel'des'questions'initiales'
!
Dans!cette!thèse,!nous!proposions!d’étudier!les!grands!patrons!biogéographiques!via!la!
description! des! différentes! facettes! de! la! diversité! biologique! (taxonomique,!
fonctionnelle!et!phylogénétique).!En!particulier!:!
!
(1)+les+différentes+facettes+de+diversité+des+mammifères+sont=elles+congruentes+à+l’échelle+du+
globe+?+ En+ d’autres+ termes,+ protéger+ le+ nombre+ d’espèces+ suffit=il+ à+ protéger+ la+ diversité+
fonctionnelle+et+évolutive+?+
+
(2)+ Ces+ différentes+ facettes+ sont=elles+ également+ vulnérables+ aux+ changements+ globaux+ et+
en+particulier+à+la+perte+d’habitat+?+
+
(3)+Ces+différentes+facettes+sont=elles+également+couvertes+par+les+zones+de+protection?+
+
(4)+Que+peuvent+nous+apporter+ces+différentes+facettes+dans+la+compréhension+des+grands+
patrons+de+répartition+du+vivant?+
En+ particulier,+ peut=on+ décomposer+ la+ distribution+ des+ lignées+ sur+ une+ échelle+
phylogénétique+ pour+ mieux+ comprendre+ les+ effets+ relatifs+ de+ l’histoire+ et+ de+ la+ niche+
écologique?+
!
!
2.'Synthèse'
!
La!première!partie!de!ma!thèse,!de!nature!méthodologique,!visait!à!faire!le!tri!des!
différentes!mesures!de!diversité!phylogénétique!et!fonctionnelle!tout!en!les!reliant!à!des!
questions! écologiques! et! évolutives! particulières.! Je! pense! que! nous! avons! proposé! un!
premier! tri! conséquent! de! ces! indices,! mais! il! faut! admettre! plusieurs! limites! à! nos!
travaux.!Tout!d’abord,!plusieurs!indices!ont!été!publiés!pendant!la!rédaction!de!l’étude,!
et! d’autres! le! seront! très! probablement! à! (très)! court! terme,! et! il! faudra! donc!
rapidement!refaire!une!synthèse.!Ensuite,!je!pense!que!la!«!jungle!»!des!indices!n’est!en!
fait! que! la! partie! émergée! d’un! problème! plus! profond.! Cet! «!enfer! vert!»! ne! fait"il! pas!
que! refléter! des! racines! théoriques! encore! incertaines! et! mal! ancrées!?! Ce! manque! de!
! "!255!"!
«!repères!»! théoriques,! couplé! à! l’explosion! des! techniques! de! séquençage! de! l’ADN!
permettant!d’obtenir!des!phylogénies!rapidement!et!à!bas!coût,!provoque,!entre!autres,!
une!prolifération!des!indices!de!diversité!phylogénétique.!Il!apparaît!que!le!défi!majeur!
de! l’écologie! des! communautés! soit! la! production! d’un! cadre! conceptuel! et! théorique!
solide,!à!partir!duquel!on!puisse!d’abord!unifier!les!multiples!théories!écologiques!afin!
de! produire! des! attendus! qui! pourront! être! infirmés! "! ou! non! "! par! les! données!
empiriques,!notamment!la!valeur!des!indices!phylogénétiques!et!fonctionnels!(Vellend,!
2010).!!
!
La! deuxième! partie! de! ma! thèse! utilisait! certains! de! ces! indices! pour! montrer!
qu’à!large!échelle!spatiale,!les!différentes!facettes!de!la!biodiversité!étaient!spatialement!
découplées! et! inégalement! protégées! et! vulnérables.! En! ce! sens,! mon! travail! montre!
qu’une! approche! de! conservation! intégrative! doit! considérer! les! trois! facettes!
indépendamment.!Cet!exercice!était!en!fait!largement!descriptif!et!théorique!et!ne!peut!
donc! pas! être! directement! appliqué! en! conservation.! Cependant,! je! considère! qu’il!
pourrait! participer! à! une! prise! de! recul! permettant! de! percevoir! la! conservation! de! la!
biodiversité! sous! plusieurs! facettes,! et! non! plus! uniquement! avec! le! seul! prisme! de!
l’espèce.!!
!
La!troisième!partie!de!ma!thèse,!relativement!découplée!de!la!seconde!sur!le!plan!
conceptuel,! illustrait! quelques! intérêts! fondamentaux! de! la! décomposition!
phylogénétique! et! du! couplage! entre! phylogénie! et! fonction.! Ces! illustrations!
s’appuyaient! sur! des! cas! concrets,! en! l’occurrence! des! systèmes! d’études! emboîtés!:!
l’ensemble! des! mammifères! peuplant! le! globe! et! les! bactéries! peuplant! l’intestin! de!
certains! de! ces! mammifères.! Au! premier! abord,! il! peut! être! surprenant! d’utiliser! des!
objets! biologiques! si! différents! dans! une! même! thèse.! Je! pense! justement! que! cela!
constitue!sa!force!et!sa!facette!la!plus!intéressante.!D’un!point!de!vue!de!la!connaissance!
pure,! l’étude! des! microbiomes! peut! se! nourrir! –! entre! autres! "! des! concepts!
biogéographiques!et!écologiques.!Ces!disciplines!me!semblent!encore!trop!cloisonnées,!
alors! qu’elles! peuvent! apprendre! l’une! de! l’autre.! Ce! parallèle! est! aussi! vrai! dans! le!
domaine!appliqué!des!deux!disciplines.!Comme!le!fait!justement!remarquer!Lozupone!et+
al.!(2012),!les!microbiomes,!comme!les!macro"écosystèmes,!font!face!à!des!menaces!qui!
mettent! en! péril! leur! fonctionnement.! La! compréhension! de! ces! deux! systèmes! pourra!
! "!256!"!
permettre! à! l’avenir! de! mieux! prédire! les! conséquences! des! menaces! et! surtout! de!
proposer!des!plans!d’action!pour!sauvegarder!la!santé!humaine!et!celle!de!la!biosphère.!
!
!
3.'Perspectives'
!
Dans!un!avenir!proche,!plusieurs!pistes!de!travail!me!semblent!intéressantes.!En!
terme! conceptuels,! j’envisage! d’écrire! (1)! une! revue! synthétique! sur! les! indices!
d’originalité!phylogénétique!et!fonctionnelle!des!espèces!(voir!Partie!I!–Synthèse)!et!(2)!
un! article! d’opinion! sur! les! liens! entre! l’étude! des! microbiotes! et! la! biogéographie!
«!classique!».! En! terme! d’étude! de! cas,! je! vais! continuer! à! travailler! sur! les! deux!
systèmes!d’études!présentés!dans!cette!thèse.!D’une!part,!je!vais!poursuivre!mes!travaux!
sur! les! microbiotes! d’animaux! en! collaboration! avec! M.! Groussin,! en! analysant!
notamment!un!nouveau!jeu!de!données.!J’ai!d’ailleurs!participé!au!choix!des!espèces!de!
mammifères!à!échantillonner!au!Zoo!du!Bronx,!en!essayant!de!sélectionner!un!ensemble!
d’espèces!représentatif!de!la!diversité!des!régimes!alimentaires!et!de!la!phylogénie!des!
mammifères.! Par! ailleurs,! je! compte! continuer! mes! travaux! en! biogéographie!
«!classique!»,! notamment! en! tentant! de! combiner! l’analyse! BDTT! et! les! données!
fonctionnelles.!Je!n’ai!pas!encore!choisi!de!système!d’étude!en!particulier!car!je!crois!que!
ce!qui!importe!le!plus,!c’est!justement!de!comparer!les!systèmes.!
!
!
Bibliographie'de'la'conclusion'
Lozupone,!C.A.,!Stombaugh,!J.I.,!Gordon,!J.I.,!Jansson,!J.K.!&!Knight,!R.!(2012).!Diversity,!
stability!and!resilience!of!the!human!gut!microbiota.!Nature,!489,!220–30.!
Vellend,!M.!(2010).!Conceptual!synthesis!in!community!ecology.!The+Quarterly+review+of+
biology,!85,!183–206.!
! "!257!"!
Glossaire!
GLOSSAIRE'
! "!258!"!
Glossaire!
Allopatrie.!Se!dit!de!deux!clades!se!distribuant!dans!des!zones!géographiques!séparées.!!
!
Autocorrélation' spatiale.' L’autocorrélation!spatiale!reflète!simplement!le!fait!que!des!
localités! proches! spatialement! se! ressemblent! plus! que! des! localités! éloignées,! que! ce!
soit!en!terme!de!variables!écologiques!ou!de!variables!environnementales.!'
!
Convergence' évolutive.!Les!termes!de!parallélisme!et!de!convergence!ont!été!tous!les!
deux! employés! dans! la! littérature! pour! décrire! le! phénomène! de! ressemblance!
fonctionnelle! non! héritée! d’une! même! origine! ancestrale! et! produite! par! la! sélection!
naturelle.! En! fait,! la! distinction! entre!les! deux! termes! apparaît! historiquement! floue! et!
semble! correspondre! à! une! différence! d’échelle! phylogénétique! (Arendt! &! Reznick!
2008).!Dans!cette!thèse,!nous!utiliserons!le!mot!convergence!dans!tous!les!cas!comme!le!
proposent!Arendt!&!Reznick!(2008).!
'
Diversité' phylogénétique.' Dans! cette! thèse,! on! utilisera! le! terme! de! ‘diversité!
phylogénétique’! pour! n’importe! quel! indice! quantifiant! la! structure! phylogénétique!
d’une!communauté,!et!on!ne!limitera!pas!son!usage!au!seul!indice!du!même!nom!(Faith!
1992).!!
'
Diversité' fonctionnelle.' Dans! cette! thèse,! on! utilisera! le! terme! de! ‘diversité!
fonctionnelle’! pour! n’importe! quel! indice! quantifiant! la! structure! fonctionnelle! d’une!
communauté,!et!on!ne!limitera!pas!son!usage!au!seul!indice!du!même!nom!(Petchey!&!
Gaston!2006).'
'
Microbiome.!L’ensemble!des!génomes!du!microbiote.!
'
Microbiote.' La! communauté! de! lignées! commensales,! symbiotiques! et! pathogéniques!
qui!peuplent!le!corps!des!métazoaires!et!métaphytes.!!
!
Niche'écologique.!Ensemble!des!conditions!biotiques!et!abiotiques!permettant!la!survie!
et! la! reproduction! d’une! espèce! (voir! les! concepts! de! niche! fondamentale! et! de! niche!
réalisée)!
'
Parallélisme.'Voir!‘Convergence!évolutive’.!
!
Phénotype.!Ensemble!des!caractères!observables!d’un!individu.!
!
Phylogénie.! Étude! des! relations! de! parenté! entre! êtres! vivants,! souvent! (mais! pas!
toujours)!représentées!par!un!arbre!phylogénétique.!!
!
Sympatrie.!Se!dit!de!deux!clades!se!distribuant!dans!les!mêmes!zones!géographiques.!
!
Trait'fonctionnel.!Caractéristique!morphologique,!physiologique!ou!phénologique!d’un!
individu!qui!a!un!impact!indirect!sur!sa!performance!(sa!fitness).
! "!259!"!
!
! "!260!"!
!
!
Les!mammifères!sont!présents!sur!la!surface!terrestre!depuis!au!moins!le!crétacé!et!ont!
colonisé!l’ensemble!des!continents!et!des!océans.!Mon!travail!s’attache!à!comprendre!la!nature!
et!l’importance!relative!des!processus!qui!ont!pu!conduire!à!la!répartition!géographique!actuelle!
des!mammifères!et!notamment!aux!similarités!faunistiques!entre!régions!du!globe.!En!décrivant!
les! facettes! phylogénétiques! et! fonctionnelles! de! la! biodiversité! des! mammifères,! j’adopte! une!
approche! résolument! intégrative,! à! l’interface! entre! la! biogéographie! historique! et! la!
biogéographie!fonctionnelle.!
À!partir!d’un!travail!de!revue!et!de!synthèse,!la!première!partie!de!la!thèse!me!permet!de!
dégager!un!nombre!limité!de!grandes!lignes!structurelles!décrivant!les!facettes!phylogénétiques!
et!fonctionnelles!de!la!biodiversité.!En!particulier,!je!mets!en!évidence!comment!la!variation!de!
l’échelle!phylogénétique!de!travail!peut!permettre!de!mettre!en!lumière!différents!processus.!
La! seconde! partie! de! ma! thèse! s’attache! à! utiliser! cette! approche! pour! expliquer! la!
répartition!des!mammifères!sur!le!globe.!Nous!montrons!ainsi!que!les!compositions!faunistiques!
à! large! échelle! phylogénétique! (p.! ex.! pour! les! familles)! semblent! expliquées! par! l’isolement!
géographique!des!masses!continentales!au!cours!du!cénozoïque!alors!que!les!compositions!à!fine!
échelle! phylogénétique! (p.! ex.! pour! les! espèces)! sont! davantage! conditionnées! par! les! affinités!
climatiques.! Nous! montrons! ensuite! que! les! régions! ayant! développées! des! faunes!
mammaliennes!indépendantes!présentent!en!fait!des!similarités!fonctionnelles!exceptionnelles,!
résultat!d’une!évolution!convergente.!!
Comprendre! les! déterminants! historiques! et! écologiques! d’une! telle! répartition! ne!
représente! pourtant! qu’un! premier! pas! vers! leur! sauvegarde! face! aux! multiples! menaces!
anthropiques.!La!dernière!partie!de!ma!thèse!entreprend!de!montrer!l’importance!d’une!vision!
intégrative! combinant! les! facettes! phylogénétiques,! fonctionnelles! et! taxonomiques! pour! la!
conservation!de!l’ensemble!des!dimensions!de!la!diversité!mammalienne.!
!
!
! Mammals! inhabit! the! Earth! since! at! least! the! Cretaceous! and! have! colonised! all!
continents! and! oceans.! My! work! aims! at! understanding! the! nature! and! importance! of! the!
different!processes!leading!to!current!geographical!distributions!of!mammals!and!in!particular!
faunal!similarities!between!regions!of!the!globe.!By!describing!the!phylogenetic!and!functional!
facets! of! mammalian! diversity,! I! adopt! an! integrative! approach,! at! the! interface! between!
historical!and!functional!biogeography.!!
! First,! I! review! and! synthesize! most! of! the! published! multifaceted! diversity! metrics! to!
propose! a! limited! number! of! structural! dimensions! that! parsimoniously! describe! the!
phylogenetic! and! functional! structure! of! species! assemblages.! In! particular,! I! point! out! how! a!
multiNphylogenetic!scale!approach!might!improve!our!understanding!of!the!mechanisms!shaping!
diversity!patterns.!
! Second,! I! use! this! approach! to! understand! the! geographical! distribution! of! mammals!
worldwide.! I! show! that! at! large! phylogenetic! scales! (e.g.! families)! distributions! seem! to! be!
driven!by!geographic!isolation!of!the!regions!over!the!course!of!the!Cenozoic!Era,!while!at!small!
phylogenetic! scales! (e.g.! species),! distributions! are! related! to! climatic! affinities.! In! addition,! I!
show! that! those! regions! having! developed! independent! mammalian! faunas! show! exceptional!
functional!similarities!due!to!evolutionary!convergences.!
! Understanding! the! historical! and! ecological! drivers! of! mammal! biodiversity! only!
represents!the!first!step!toward!their!conservation!in!the!face!of!anthropic!threats.!The!last!part!
of!my!thesis!shows!the!importance!of!an!integrative!approach!using!phylogenetic,!functional!and!
taxonomic!facets!to!protect!all!dimensions!of!mammal!diversity.!

Thèse MAZEL Diversité Des Mamifères Et Biogéographie

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Comprendre et protéger la diversité des mammifères :

une approche de biogéographie évolutive et fonctionnelle

To cite this version:

HAL Id: tel-01684747

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est

DOCTEUR DE L’UNIVERSITÉ GRENOBLE ALPES

Thèse dirigée par Wilfried Thuiller

préparée au sein du Laboratoire d’Écologie Alpine

Comprendre et protéger la diversité

Thèse soutenue publiquement le 14 décembre 2015,

Tout! d’abord,! la! dualité! traditionnelle! entre! approche! fonctionnelle! et!

Nombre de Publications 600

Research.Areas ENVIRONMENTAL SCIENCES ECOLOGY

I.'Introduction.!! predict! ecosystem! properties! (Mouquet"et"al.,! 2012),!

Within! each! dimension,! different! phylogenetic! 2013;!Scheiner,!2012;!Swenson,!2011;!Vellend"et"

of! the! possible! pairwise! distances! (Table! 1" (δ!statistic)!and!tree!symmetry!(Ic!statistic)!using!

! correlated! with! the! richness! dimension! (PD),! as!

questions!asked!by!ecologists!using!phylogenies,! be! an! outcome! of! different! ecological! and!

dimensions! that! themselves! align! naturally! with! confusing!inference!and!we!do!not!recommend!it.!

phylogenetic! methods! in! ecology! and!

-0.2 -0.1 0.0 0.1 0.2 0.3

1.1 1.2 1.3 2.1 2.2 2.3 3.1 3.2 3.3

Average inter-set relative to intra-set

Richness Dpw Raos D

-0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4

Effect of species pool size

-0.2 -0.1 0.0 0.1 0.2 0.3 0.4

-0.2 -0.1 0.0 0.1 0.2 0.3

b) With Parametric Indices

mean(ED) MPD = PSV

-0.2 -0.1 0.0 0.1 0.2 0.3

0.299 VPD = 25.4

IX.'Works'Cited.' Through! Hill! Numbers.! Annual" Review" of" Ecology,"

(mean! SR)! of! assemblages! (Fig! 2! and! ! 3"4).! The! show!significant!‘basal’!clustering!(as!indicated!by!a!

MPD! is! more! sensitive! to! deeper! branching!

communauté! résidente! influencent! le! succès! invasif! de! l’espèce! exotique!

L’approche! fonctionnelle! privilégie! plutôt! les! propriétés! fonctionnelles! des!

Mammalian phylogenetic diversity–area relationships at a

INTRODUCTION history in species assemblages (Mouquet et al. 2012). To

the SAR, the PDAR brings unique information about

RE S E A RCH Multifaceted diversity–area relationships

The most recent comparisons of the world-wide distribution

Table 1 The set of diversity indices used in the analysis.

report the percentage of maximal diversity reached in this

Model standardization and comparison Convergence, homoscedasticity and normality

0 50 180 1000 0 50 180 1000

0 40 100 800 0 40 100 800

relationship (FDAR) values and

corresponding predicted species–area

correspond to different biomes, while

each plot, the differences between

for three values of q: 0 (Faithcor index), 1

Positive differences mean that PDAR or

maximum diversity faster than SAR. This difference increased

1A. Maps of the averaged ranks 1B. SAR

2A. Maps of the averaged ranks 2B. PDAR

3A. Maps of the averaged ranks 3B. FDAR

Table 2 The five hottest hotspots of

SR Vs. PD SR Vs. FD PD Vs. FD SR Vs. Int.

Spécia6on) Spécia6on) Duplica6on)