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Evolutionary relationships of marine turtles: A molecular phylogeny based on

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 Molecular Phylogenetics and Evolution 49 (2008) 659–662

Contents lists available at ScienceDirect

Molecular Phylogenetics and Evolution

journal homepage: www.elsevier.com/locate/ympev

Short Communication

Evolutionary relationships of marine turtles: A molecular phylogeny based

on nuclear and mitochondrial genes
Eugenia Naro-Maciel a,b,*,1, Minh Le a,c,1, Nancy N. FitzSimmons d, George Amato b
a
Center for Biodiversity and Conservation, American Museum of Natural History, New York, NY 10024, USA
b
Sackler Institute for Comparative Genomics, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA
c
Department of Herpetology, American Museum of Natural History, New York, NY 10024, USA
d
Institute for Applied Ecology, University of Canberra, Canberra, ACT 2601, Australia

a r t i c l e i n f o

Article history:
Received 5 February 2008
Revised 29 July 2008
Accepted 5 August 2008
Available online 12 August 2008

1. Introduction flatback, Natator depressus, which nests only in Australia (see Bo-
wen et al., 1993; Dutton et al., 1996; Pritchard, 1996). The evolu-
Marine chelonians have inhabited the earth for over 100 million tion of feeding ecology in marine turtles remains puzzling, and
years, since the Cretaceous (Hirayama, 1998) and the fossil record two alternative hypotheses of carnivorous versus herbivorous ori-
reveals that four families were established during this period, two gins have been proposed to account for spongivory in hawksbill
of which have survived into the present (Pritchard, 1996). The turtles (Bowen and Karl, 1996), a rare dietary choice in reptiles
Dermochelyidae contains only the leatherback turtle, Dermochelys and vertebrates (Meylan, 1988). The possibility of an omnivorous
coriacea, while the second family, the Cheloniidae, is commonly ancestor has not been as fully explored. Additionally, full consen-
thought to include six species classified into five genera (Fig. 1). sus has not yet been reached on the taxonomic status of the East-
Early molecular phylogenetic studies supported recognition of ern Pacific (EP) green turtle (Chelonia mydas; see Kamezaki and
the olive ridley, Lepidochelys olivacea, and Kemp’s ridley, L. kempii, Matsui, 1995; Parham and Zug, 1996; Pritchard, 1996). However,
as separate species (Bowen et al., 1991, 1993; Dutton et al., 1996) to date DNA results reveal no species-level or evolutionary distinc-
and removal of the flatback turtle, Natator depressus, from genus tiveness of C. mydas of the EP (Bowen et al., 1992, 1993; Bowen and
Chelonia (Dutton et al., 1996; see also Limpus et al., 1988 and Zan- Karl, 1996; Karl and Bowen, 1999).
gerl et al., 1988). There is general agreement that the leatherback, Although recently there has been intense scientific focus on
Dermochelys coriacea, is the sister-taxon to a clade comprising all the evolutionary relationships among all turtles (see Iverson
other extant sea turtles (e.g., Gaffney and Meylan, 1988; Pritchard, et al., 2007), our understanding of marine turtle phylogeny from
1996), and one phylogenetic hypothesis (Fig. 1a; see Iverson et al., a genetic perspective still remains largely based on mitochondrial
2007) is broadly supported by the most recent research (Bowen DNA studies (Bowen et al., 1993; Dutton et al., 1996; but see Bo-
and Karl, 1996; Dutton et al., 1996; Parham and Fastovsky, 1997). wen and Karl, 1996), despite recognized problems in relying so-
Despite the application of molecular approaches, there are still lely on mtDNA. To address the lingering controversies and to
conflicting hypotheses about the evolutionary relationships of recover a definitive marine turtle phylogeny, we sequenced five
widely distributed but highly threatened marine turtles (Bowen nuclear DNA markers (BDNF, Cmos, R35, Rag1, and Rag2) and
et al., 1993; Dutton et al., 1996), and further study is needed (Bo- two mitochondrial genes (12S and 16S) in the seven widely recog-
wen and Karl, 2007; Iverson et al., 2007). In the past, questions nized marine turtle species, the taxonomically ambiguous Eastern
were raised as to the placement of the geographically restricted Pacific green turtle, and four outgroups. We used comprehensive
phylogenetic methods, improving upon previous work by includ-
ing multiple outgroups and examining both nuclear and mito-
chondrial markers. Using this approach we tested hypotheses
* Corresponding author. Address: Sackler Institute for Comparative Genomics, about the evolutionary relationships of marine turtles, including
American Museum of Natural History, Central Park West at 79th Street, New York,
NY 10024, USA. Fax: +1 212 769 5292.
the placement of the geographically restricted flatback turtle,
E-mail address: [email protected] (E. Naro-Maciel). and the origin of the rare spongivorous dietary habit of hawksbill
1
These authors contributed equally to this work. turtles.

1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved.
doi:10.1016/j.ympev.2008.08.004
660 E. Naro-Maciel et al. / Molecular Phylogenetics and Evolution 49 (2008) 659–662

v3 (Sorenson and Franzosa, 2007). All characters were equally

carnivory
Dermochelys coriacea weighted and unordered. For Bayesian analyses we used the opti-
(Leatherback) mal model determined using Modeltest v3.7 (Posada and Crandall,
herbivory
Chelonia mydas 1998) with parameters estimated by MrBayes v3.1. Analyses were
(Green)
carnivory
conducted with a random starting tree and run for 5  106 gener-
Natator depressus
(Flatback)
ations. Four Markov chains, one cold and three heated (utilizing
spongivory default heating values), were sampled every 1000 generations.
Eretmochelys imbricata Log-likelihood scores of sample points were plotted against the
(Hawksbill)

Caretta caretta
number of generations to detect stationarity of the Markov chains.
(Loggerhead) Trees generated prior to stationarity (21 trees in both combined
carnivory
Lepidochelys olivacea and mixed-model Bayesian analyses) were removed from the final
(Olive ridley)
analyses using the burn-in function. Two independent analyses
Lepidochelys kempii
(Kemp’s ridley) were run simultaneously. The posterior probability values (PP)
for all clades in the final majority rule consensus tree are reported.
Fig. 1. (a) Consensus phylogenetic relationships of marine turtles based on
previous studies (after Iverson et al., 2007); (b) Evolutionary relationships revealed We ran analyses on both combined and partitioned datasets to
in this study. examine the robustness of the tree topology (Nylander et al.,
2004; Brandley et al., 2005). In the partitioned analyses, we divided
the data into fifteen separate partitions, including 12S, 16S, and
2. Materials and methods R35, with the other twelve partitions based on gene codon posi-
tions (first, second, and third) in BDNF, Cmos, Rag1, and Rag2. Opti-
2.1. Taxonomic sampling and laboratory methods mal models of molecular evolution for each partition were selected
using the Akaike information criterion (AIC) in Modeltest and then
We obtained blood or tissue samples from marine turtles nest- assigned to these partitions in MrBayes (Table A2, Supplementary
ing at beaches of the Atlantic and Pacific Oceans (with the excep- Data). Model parameters were calculated independently for each
tion of the Kemp’s ridley turtle sampled from a feeding ground; data partition using the UNLINK command. We consider bootstrap
Table 1), and from four outgroups. We employed the primers listed values P70% potentially strong support (Hillis and Bull, 1993) and
in Table A1 (Supplementary Data) to amplify and sequence two PP values P95% strong support for a clade.
mitochondrial and five nuclear markers using previously described
laboratory methods (Le et al., 2006). We aligned the sequence data 2.3. Time calibration
using the program Sequencher v4.6 (Gene Codes Corporation) or
ClustalX v1.83 (Thompson et al., 1997) with default settings for Divergence times were calculated using a relaxed clock model
complete alignment. (Drummond et al., 2006) as implemented in the computer program
BEAST v1.4.5 (Drummond and Rambaut, 2006). The program
2.2. Phylogenetic analysis BEAUti v1.4.5 was used to set criteria for the analysis. Nodes
corresponding to the most recent common ancestors of three
Data were analyzed using maximum parsimony (MP) as imple- clades: (1) all sea turtle species; (2) Caretta and Lepidochelys; and
mented in PAUP v4.0b10 (Swofford, 2001) and Bayesian analysis (3) Lepidochelys kempii and L. olivacea were constrained respec-
as implemented in MrBayes v3.1 (Huelsenbeck and Ronquist, tively to: (1) 110 million years with a 95% confidence interval from
2001). For maximum parsimony, we conducted heuristic analyses 100 to 120; (2) 16 million years with 95% confidence interval from
with 100 random taxon addition replicates using the tree-bisection 12 to 20; and (3) 5 million years with 95% confidence interval from
and reconnection (TBR) branch swapping algorithm in PAUP, with 4 to 6. These dates are based on reasonably strong fossil evidence
no upper limit set for the maximum number of trees saved. Boot- (Carr, 1942; Hendrickson, 1980; Zangerl, 1980; Dodd and Morgan,
strap support (BP; Felsenstein, 1985) was evaluated using 1000 1992; Hirayama, 1998) and supported by genetic studies
pseudoreplicates and 100 random taxon addition replicates. Bre- ( Lepidochelys, Caretta: Bowen et al., 1991). A GTR model using
mer indices (BI; Bremer, 1994) were determined using TreeRot gamma + invariant sites with four gamma categories was used
along with the assumption of a relaxed molecular clock. As for
the priors, we used all default settings, except for the Tree Prior
Table 1
Sampling locations at nesting beaches in the Atlantic or Pacific Oceans
category that was set to Yule Process as suggested in the BEAST
manual. A UPGMA tree was used as a starting tree. The analysis
Taxon Sample site (n)a
was run for 5  106 generations with a 1000-step thinning. The
Atlantic Pacific posterior sample was examined in Tracer v1.4. Burn-in was set to
Dermochelys coriacea Mayumba, Gabon (1) New South Wales, Australia (1)b 500. The final tree with divergence estimates and their 95% highest
Chelonia mydas Atol das Rocas, Heron Island, Queensland, posterior densities (HPD) was computed in TreeAnnotator v1.4.5.
Brazil (1) Australia (1) BEAST, BEAUti, TreeAnnotator, and Tracer are available from
Trindade Island, —
http://beast.bio.ed.ac.uk.
Brazil (1)
Eastern Pacific — Michoacán, Mexico (2)
Natator depressus — Queensland, Australia (1) 3. Results
Eretmochelys imbricata Puerto Rico, USA (1) Queensland, Australia (1)
Caretta caretta Georgia, USA (1) Mon Repos, Queensland,
The final matrix that was subjected to phylogenetic analyses in-
Australia (1)
Lepidochelys olivacea Ada Foah, Ghana (1)b Northern Territory,
cluded 404 aligned bp of 12S, 579 bp of 16S, 717 bp of BDNF, 602 bp
Australia (1) of Cmos, 984 bp of R35, 2860 bp of Rag1, and 1194 bp of Rag2 for a
Lepidochelys kempii New York, USA (1)c — total of 7340 bp. The GenBank Accession numbers for these se-
a
Sample size is indicated in parentheses.
quences are listed in Table A3 (Supplementary Data). The sea turtle
b
A taxon represented by two individuals due to samples that were degraded or data set included 17 indels. Of these, 14 were 1 bp long and found
difficult to amplify. within 12S, 16S and the R35 intron. The remaining three indels
c
Sample collected at a feeding rather than nesting area. were: (1) a 28 bp insertion in Atlantic and Western Pacific green
 E. Naro-Maciel et al. / Molecular Phylogenetics and Evolution 49 (2008) 659–662 661

turtles within the R35 intron; (2) a 12 bp insertion in the Rag1 gene (Chelonia mydas; BP = 99%, PP = 100%). Although recent research
of Caretta caretta (Atlantic and Pacific); and (3) a 3 bp deletion in consistently grouped the flatback with the Carettini tribe (e.g. Dut-
Rag2 of Eretmochelys imbricata. The nucleotide composition of sites ton et al., 1996; Parham and Fastovsky, 1997), this species was un-
polymorphic in more than one individual in green turtles is shown til recently classified as Chelonia depressa (Garman, 1880; Limpus
in Table A4 (Supplementary Data). et al., 1988; Zangerl et al., 1988), and its sister-taxon relationship
Using Maximum Parsimony (MP) and Bayesian analyses, we with C. mydas is supported by mtDNA control region and ND4 data
recovered the phylogenetic trees shown in Figs. 1b and 2. All of (Dutton et al., 1996; Bowen and Karl, 2007).
the phylogenetic methods used in this study generated trees with By placing the flatback outside the Carettini tribe, the previous
an identical topology and strong levels of support for all nodes. In hypothesis that the hawksbill turtle’s spongivorous dietary habit
the MP cladogram, all nodes received high bootstrap support. MP developed from a carnivorous ancestor (Bowen et al., 1993; Dut-
analyses of nuclear and mitochondrial partitions also indicated ton et al., 1996) becomes less obvious. The hawksbill is now
the same topology (Supplementary Data Figs. A1–A2). Time cali- hypothesized to be a basal and distinct lineage rather than a tax-
bration analysis demonstrated that the Chelonini split from Caret- on embedded within a carnivorous clade. In addition, although
tini about 63 MYA (95% HPD: 35.59 MYA–91.38 MYA), while the dietary preferences of hawksbills are primarily for sponges,
Natator separated from Chelonia about 34 MYA (95% HPD: 14.08 their food can also include items such as plants, algae, and ani-
MYA–60.05 MYA), and Eretmochelys split from Caretta and mals other than sponges that may dominate the diet in certain
Lepidochelys about 29 MYA (95% HPD: 16.52 MYA–44.27 MYA; areas (reviewed by Bjorndal, 1996). Similarly, turtles that are
Supplementary Data Fig. A3). The divergence between Atlantic mainly carnivorous such as the loggerhead, the ridleys, and the
and Indo-Pacific green turtles is estimated at about 7 million years flatback, also consume plants and algae (reviewed by Bjorndal,
(95% HPD: 1.92 MYA–13.47 MYA; Supplementary Data Fig. A3). 1996). Green turtles, which tend to specialize on algae or sea
grass as adults, have carnivorous young (Bjorndal, 1996; Reich
et al., 2007) and adult diets may include animals (Bjorndal,
4. Discussion 1996; Seminoff et al., 2002). Based on our phylogenetic results
and dietary reconstruction, we hypothesize the ancestral state
Our phylogenetic results differ from those recovered in previous of all sea turtles is carnivorous (Fig. 1b). However the reconstruc-
molecular studies by strongly supporting a sister-taxon relation- tion of dietary habits is not unambiguous, as the origins of spong-
ship between the flatback (Natator depressus) and green turtles ivory in Eretmochelys could also be explained by transitions from
omnivory to spongivory, with an omnivorous common ancestor
100/11 to all sea turtles. If hawksbill, green, and leatherback turtles are
100/100
Lepidochelys olivacea
Lepidochelys Pacific nonetheless considered to be specialists over evolutionary time,
100/29 with the bulk of their diet consisting of limited items, then a spe-
100/100 Lepidochelys olivacea
LEPIDOCHELYS ATLANTIC
cialized diet in marine turtles evolved independently three times
Carettini

70/2 Lepidochelys kempii

Lepidochelys kempii (i.e., spongivory in the hawksbill, jellyfish carnivory in the leath-
100/100
erback, and herbivory in the green turtle; Fig. 2).
100/19 Caretta
CARETTAcaretta
PACIFIC
Our results substantiate and extend findings of previous molec-
100/100
Caretta
CARETTAcaretta
ATLANTIC ular studies, which also revealed the sister-taxon relationship of
100/24 the ridleys, the close affiliation between Lepidochelys and the log-
100/100 Eretmochelys
ERETMOCHELYS imbricata
PACIFIC
100/17
gerhead turtle, and the basal position of Dermochelys relative to
100/100
Eretmochelys
ERETMOCHELYS imbricata
ATLANTIC other marine turtles (Bowen et al., 1993; Dutton et al., 1996).
91/3
100/21 100/100 Our study joins past work by indicating the paraphyly of the East-
100/100 Chelonia mydasAG(EP)
CHELONIA MYDAS 36365
ern Pacific green turtle with respect to other green turtles (Bowen
Pacific Atlantic

89/2
100/100 Chelonia mydasAG(EP)
CHELONIA MYDAS 36367 et al., 1992; Bowen and Karl, 1996; Karl and Bowen, 1999), and
Chelonini

100/24
100/100 revealing a deep split between Atlantic and Pacific green turtle lin-
Chelonia mydas
CHELONIA PACIFIC
87/2 eages. Our Bayesian analysis dates this divergence back to about 7
100/100 MYA (95% HPD: 1.92 MYA–13.47 MYA; Supplementary Data
100/33 Chelonia mydas
CHELONIA ATLANTIC 53

100 /100 Fig. A3), predating other vicariant events known to divide marine
99/11 Chelonia mydas
CHELONIA ATLANTIC 2541
100/100
taxa such as the formation of the Isthmus of Panama (about 3–
Natator
NATATORdepressus 3.5 MYA). However, effects of the formation of the Isthmus may
100/60 have been felt prior to the closure itself, and previous estimated
Dermochelys coriacea
DERMOCHELYS PACIFIC
100/100 100/87 divergence times between Atlantic and Pacific green turtles based
100/100
Dermochelys coriacea
DERMOCHELYS ATLANTIC on a molecular clock (Encalada et al., 1996) were consistent with
the formation of the Isthmus, a time period included in the confi-
Macroclemys temminckii
100/39 Macroclemys temminckii dence interval of our current estimate.
100/100
Chelydra serpentina
Chelydra serpentina Of interest, our estimated divergence time of about 7 MYA be-
tween Atlantic and Pacific green turtles follows the closure of the
Pelomedusa subrufa
Pelomedusa subrufa
Tethys Sea (14–18 MYA; Vrielynck et al., 1997; Rögl, 1998), an event
Pelodiscus sinensis
Pelodiscus sinensis that prevented mixing between many tropical marine species of the
0.01
Atlantic and Indo-Pacific (Rosen, 1988). The cooling of southern
ocean temperatures from the mid to late Miocene (from 15–17
Fig. 2. Single tree generated from the MP and Bayesian analyses of combined
mitochondrial and nuclear genes with branch length estimated by the Bayesian MYA to about 6 MYA) is consistent with a split about 7 MYA due to
analyses. For the MP analysis, tree length = 1502, consistency index (CI) = 0.868, and cold temperatures blocking dispersal via southern routes. Indeed,
retention index (RI) = 0.84. Of the 7340 total characters, 1177 were variable the divergence between the green turtle populations in separate
characters and 480 of these were parsimony-informative. The numbers above ocean basins is generally attributed to the biogeographic barrier to
branches are MP bootstrap and Bremer values (Bremer, 1994), and those below the
branches are posterior probability values (PP) from combined and mixed-model
the dispersal of tropical species formed by the relatively cold waters
Bayesian analyses, respectively. The triangle, hexagon, and circle show jellyfish of the southern tips of South Africa and South America. However,
carnivory, spongivory, and herbivory feeding modes, respectively. microsatellites and mtDNA phylogeographic studies suggest
662 E. Naro-Maciel et al. / Molecular Phylogenetics and Evolution 49 (2008) 659–662

relatively recent linkages between green turtles of the Atlantic, In- Mediterranean green turtle Chelonia mydas: a mitochondrial DNA control region
sequence assessment. Mol. Ecol. 5, 473–483.
dian, and Pacific (Roberts et al., 2004; Bourjea et al., 2007), and there
Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the
is general agreement that limited gene flow prevents Atlantic and bootstrap. Evolution 39, 783–791.
Pacific green turtle lineages from being considered separate species. Gaffney, E.S., Meylan, P.A., 1988. A phylogeny of turtles. In: Benton, M.J. (Ed.), The
This phylogenetic study, thus, provides a foundation for more de- Phylogeny and Classification of the Tetrapods, vol. 1. Clarendon Press, Oxford,
pp. 157–219.
tailed research in evolutionary biology, clarifies systematic issues Garman, S., 1880. On certain species of Chelonioidae. Bull. Mus. Comp. Zool. 6,
of these highly threatened species, and significantly contributes to 123–126.
the resolution of the ‘‘turtle tree of life.” Hendrickson, J.R., 1980. The ecological strategies of sea turtles. Amer. Zool. 20,
597–608.
Hillis, D.M., Bull, J.J., 1993. An empirical test of bootstrapping as a method for
Acknowledgments assessing confidence in phylogenetic analysis. Syst. Biol. 42, 182–192.
Hirayama, R., 1998. Oldest known sea turtle. Nature 392, 705–708.
Huelsenbeck, J.P., Ronquist, F., 2001. MrBayes: Bayesian inference of phylogeny.
We are grateful to the Regina Bauer Frankenberg Foundation for Bioinformatics 17, 754–755.
Animal Welfare for supporting the research. We thank the Projeto Iverson, J.B., Brown, R.M., Akre, T.S., Near, T.J., Le, M., Thomson, R.C., Starkey,
TAMAR-IBAMA, the Riverhead Foundation, the Wildlife Conserva- D.E., 2007. In search of the tree of life for turtles. Chel. Res. Monogr. 4,
85–106.
tion Society, Omar Chassin-Noria, Carlos Diez, Peter Dutton, Angela Kamezaki, N., Matsui, M., 1995. Geographic variation in skull morphology of the
Formia, Robin Leroux, Manjula Tiwari, and Ximena Velez-Zuazo for green turtle, Chelonia mydas, with a taxonomic discussion. J. Herpetol. 29, 51–
samples. We also wish to thank Rob DeSalle, Francisca Almeida, Jeff 60.
Karl, S.A., Bowen, B.W., 1999. Evolutionary significant units versus geopolitical
Groth, Anna MacDonald, Sergios Orestes-Kolokotronis, Christopher
taxonomy: molecular systematics of an endangered sea turtle (genus Chelonia).
Raxworthy, Mark Siddall, and Eleanor Sterling for assistance. Cons. Biol. 13, 990–999.
Le, M., Raxworthy, C.J., McCord, W.P., Mertz, L., 2006. A molecular phylogeny of
tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes.
Appendix A. Supplementary data Mol. Phylogenet. Evol. 40, 517–531.
Limpus, C.J., Gyuris, E., Miller, J.D., 1988. Reassessment of the taxonomic status of
Supplementary data associated with this article can be found, in the marine turtle genus Natator McCulloch, 1908, with a redescription of the
genus and species. Trans. R. Soc. South Aust. 112, 1–9.
the online version, at doi:10.1016/j.ympev.2008.08.004. Meylan, A.B., 1988. Spongivory in Hawksbill turtles: a diet of glass. Science 239,
393–395.
Nylander, J.A.A., Ronquist, F., Huelsenbeck, J.P., Nieves-Aldrey, J.L., 2004. Bayesian
References phylogenetic analysis of combined data. Syst. Biol. 53, 47–67.
Parham, J.F., Fastovsky, D.E., 1997. The phylogeny of cheloniid marine turtles
Bjorndal, K.A., 1996. Foraging ecology and nutrition of sea turtles. In: Lutz, P.L., revisited. Chel. Cons. Biol. 2, 548–554.
Musick, J.A. (Eds.), The Biology of Sea Turtles. CRC Press, Florida, pp. 199–232. Parham, J.F., Zug, G.R., 1996. Chelonia agassizii—valid or not? Mar. Tur. News 72, 2–5.
Bourjea, J., Lapègue, S., Gagnevin, L., Broderick, D., Mortimer, J.A., Ciccione, S., Roos, Posada, D., Crandall, K.A., 1998. Modeltest: testing the model of DNA substitution.
D., Taquet, C., Grizel, H., 2007. Phylogeography of the green turtle, Chelonia Bioinformatics 14, 817–818.
mydas, in the Southwest Indian Ocean. Mol. Ecol. 16, 175–186. Pritchard, P.C.H., 1996. Evolution, phylogeny and current status. In: Lutz, P.L.,
Bowen, B.W., Meylan, A.B., Avise, J.C., 1991. Evolutionary distinctiveness of the Musick, J.A. (Eds.), The Biology of Sea Turtles. CRC Press, Florida, pp. 1–28.
endangered Kemp’s ridley sea turtle. Nature 352, 709–711. Reich, K.J., Bjorndal, K.A., Bolten, A.B., 2007. The ‘lost years’ of green turtles: using
Bowen, B.W., Meylan, A.B., Ross, J.P., Limpus, C.J., Balazs, G.H., Avise, J.C., 1992. stable isotopes to study cryptic lifestages. Biol. Lett. 3, 712–714.
Global population structure and natural history of the green turtle (Chelonia Roberts, M.A., Schwartz, T.S., Karl, S.A., 2004. Global population genetic structure
mydas) in terms of matriarchal phylogeny. Evolution 46, 865–881. and male-mediated gene flow in the green sea turtle (Chelonia mydas): analysis
Bowen, B.W., Nelson, W.S., Avise, J.C., 1993. A molecular phylogeny for marine of microsatellite loci. Genetics 166, 1857–1870.
turtles: trait mapping, rate assessment, and conservation relevance. Proc. Natl. Rögl, F., 1998. Palaeogeographic considerations for mediterranean and paratethys
Acad. Sci. USA 90, 5574–5577. seaways (oligocene to miocene). Ann. Naturhist. Mus. Wien 99A, 279–310.
Bowen, B.W., Karl, S.A., 1996. Population genetics, phylogeography, and molecular Rosen, B.R., 1988. Progress, problems and patterns in the biogeography of reef
evolution. In: Lutz, P.L., Musick, J.A. (Eds.), The Biology of Sea Turtles. CRC Press, corals and other tropical marine organisms. Helgol Wiss Meeresunters 42,
Florida, pp. 29–50. 269–301.
Bowen, B.W., Karl, S.A., 2007. Population genetics and phylogeography of sea Seminoff, J.A., Resendiz, A., Nichols, W.J., 2002. Diet of east pacific green turtles
turtles. Mol. Ecol. 16, 4907–4986. (Chelonia mydas) in the Central Gulf of California, Mexico. J. Herpetol. 36, 447–
Brandley, M.C., Schmitz, A., Reeder, T.W., 2005. Partitioned Bayesian analyses, 453.
partition choice, and the phylogenetic relationships of scincid lizards. Syst. Biol. Sorenson, M.D., Franzosa, E.A., 2007. TreeRot Version 3. Boston University, Boston.
54, 373–390. Swofford, D.L., 2001. PAUP: Phylogenetic Analysis Using Parsimony Version 4.0.
Bremer, K., 1994. Branch support and tree stability. Cladistics 10, 295–304. Sinauer Associates, Sunderland, MA.
Carr, A.F., 1942. Notes on sea turtles. Proc. New Engl. Zool. Club 21, 1–16. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., 1997. The
Dodd, C.K., Morgan, G.S., 1992. Fossil sea turtles from the early pliocene bone valley ClustalX windows interface: flexible strategies for multiple sequence alignment
formation, Central Florida. J. Herpetol. 26, 1–8. aided by quality analysis tools. Nucl. Acids Res. 25, 4876–4882.
Drummond, A.J., Ho, S.Y.W., Phillips, M.J., Rambaut, A., 2006. Relaxed phylogenetics Vrielynck, B., Odin, G.S., Dercourt, J., 1997. Miocene palaeogeography of the Tethys
and dating with confidence. PLoS Biol. 4, 699–710. Ocean: potential global correlations in the mediterranean. In: Montanari, A.,
Drummond, A.J., Rambaut, A., 2006. BEAST v1.4. Available from: <http:// Odin, G.S., Coccioni, R. (Eds.), Miocene Stratigraphy: An Integrated Approach.
beast.bio.ed.ac.uk/> (downloaded 1 September 1 2006). Elsevier, Amsterdam, pp. 157–165.
Dutton, P.H., Davis, S.K., Guerra, T., Owens, D., 1996. Molecular phylogeny for Zangerl, R., 1980. Patterns of phylogenetic differentiation in the toxochelyid and
marine turtles based on sequences of the ND4-leucine tRNA and control regions cheloniid sea turtles. Amer. Zool. 20, 585–596.
of mitochondrial DNA. Mol. Phylogenet. Evol. 5, 511–521. Zangerl, R., Hendrickson, L.P., Hendrickson, J.R., 1988. A redistribution of the
Encalada, S.E., Lahanas, P.N., Bjorndal, K.A., Bolten, A.B., Miyamoto, M.M., Bowen, Australian flatback marine turtle Natator depressus. Bishop Mus. Bull. Zool. 1, 1–
B.W., 1996. Phylogeography and population structure of the Atlantic and 69.

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