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Animal Evolution Genomes Fossils and Trees 1st Edition
Maximilian J. Telford Digital Instant Download
Author(s): Maximilian J. Telford, D. T. J. Littlewood
ISBN(s): 9780199570300, 0199570302
Edition: 1
File Details: PDF, 8.18 MB
Year: 2009
Language: english
Animal Evolution
This page intentionally left blank
Animal Evolution
Genomes, Fossils, and Trees
E DI T E D BY

Maximilian J. Telford
University College London

AND

D. T. J. Littlewood
The Natural History Museum, London

1
3
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 Foreword

The subject of animal evolution has been explored however, there were almost as many scenarios
and discussed for a century and a half. As long ago proposed as there were scientists considering the
as the late 19th century, Ernst Haeckel, a renowned question, and as a consequence debate was often
evolutionary biologist and supporter of Darwin, heated, personal, and inconclusive. A comment
drew some beautiful phylogenetic trees depicting made by the Rev. T. R. R. Stebbing at the end of
the possible course of animal evolution. Haeckel’s a 1910 symposium discussing the origin of verte-
trees included many of the major animal groups, brates reveals the lack of progress on just one of
placed on the tips of gnarled and life-like branches, these issues: ‘When we return home and our friends
each drawn complete with bark and twigs. One gleefully enquire, “What then has been decided
could be forgiven for thinking that the framework as to the Origin of Vertebrates?”, so far we seem
of animal evolution was completed long ago. Such to have no reply ready, except that the disputants
a view would be grossly mistaken. The past two agreed on one single point, namely that their oppo-
decades in particular have seen a revolution in our nents were all in the wrong’ [Stebbing, T.R.R (1910)
understanding of animal evolution, and revisiting Discussion on the origin of vertebrates. Proceedings
this topic in 2009 is very timely. As the contents of the Linnean Society of London 122, 9–50].
of this volume will testify, research into animal The fundamental problem plaguing the study
evolution is currently in its most vibrant phase of animal evolution a century ago was that there
ever, with novel conclusions being generated at was no reliable way to test alternative scenarios, no
great pace. objective source of data to evaluate putative hom-
It is interesting to contrast the nature of current ologies or proposed relationships. Every scenario
research, as described here, to the first golden age was consistent with the available data, although
of animal evolutionary biology, the late 19th and certainly some theories were more outlandish
early 20th centuries. Many of the early zoologists, than others! This was the major stumbling block to
including Kowalevsky, Metchnikoff, van Beneden, advance in the study of animal evolution, and it
Lankester, Sedgwick, Jägersten, Goodrich, and persisted through much of the 20th century. The
T. H. Huxley were superb anatomists and embry- problem is now clearly in focus and at least part of
ologists, and their work has left us with a wonder- the solution is at hand. A major component of the
ful and extensive legacy of descriptive data. While solution is based on the application of molecular
invaluable for understanding animal form and biology to animal evolutionary biology, in partner-
function, however, these data ultimately proved of ship with other approaches including develop-
less use for discerning deep animal relationships, mental biology and palaeontology. Of course,
or understanding homologies and evolutionary genetics was first incorporated into evolutionary
transformations. Until very recently, textbooks and thinking in the 1920s to 1940s, when the work of
specialized works alike carried speculative, and Thomas Hunt Morgan, R. A. Fisher, Theodosius
often highly imaginative, scenarios of animal evo- Dobzhansky, J. B. S. Haldane, Sewall Wright,
lution, depicting how various body forms could be Julian Huxley, Ernst Mayr, G. G. Simpson, and
derived from others. For every question discussed, G. Ledyard Stebbins gradually merged Mendelian

v
vi FOREWORD

genetics with Darwinian evolution in a population The second application of molecular biology
context, and convincingly explained microevolu- is closely linked with comparative embryology,
tion through changes in allele frequencies. But it the favoured approach of a century ago. Work on
still remained unclear if large anatomical differ- convenient laboratory species, such as Drosophila,
ences, such as those between animal phyla, could nematodes, and mice, has produced a wealth of
be explained in the same way. Even if they could, data on the identity and function of genes control-
as many argued, these early genetic studies did not ling specific aspects of embryonic development,
reveal what genes were actually involved, what from setting up of embryonic axes (dorsoventral,
anatomical transformations had happened in evo- left–right, anteroposterior), to the establishment of
lution, and hence which of the multiple scenarios tissue layers, the formation of organs, and the dif-
for animal evolution were correct. Until the 1980s, ferentiation of specific cell types. With the discov-
those working on evolutionary genetics had little ery that many (but certainly not all) of these genes
interface with whole-organism biology, including are ancient and present in highly divergent phyla,
embryology and animal diversity. Zoology was a it has now become possible to trace how develop-
divided field. As Frank R. Lillie, former Director mental pathways have changed in evolution, or
of the Woods Hole Marine Biological Laboratory, been deployed in different ways, and relate this to
commented in 1927: ‘There can be no doubt, I think, the evolution of specific structures in animals. As
that the majority of geneticists, and many physi- above, there are technological difficulties and ana-
ologists certainly, hope for and expect a reunion. lytical pitfalls, but the results can be highly persua-
The spectacle of the biological sciences divided sive. Examples in this volume include new insights
permanently into two camps is evidently for them into the diversification of nervous systems, evolu-
too serious a one to be regarded with satisfaction’ tion of larval forms, relationships between body
[Lillie, F.R. (1927) The gene and the ontogenetic axes, evolution of segmentation, and the origin of
process. Science 66, 361]. novel characters.
Lillie’s hoped for reunion is now upon us. In the These applications of molecular biology to
past two decades, molecular genetics has started to zoology may have stimulated the reunion of devel-
have major impacts on the study of animal evolu- opmental and evolutionary zoology, but they are
tion, and in two distinct ways. First, comparison of not taking place in isolation. A holistic understand-
DNA sequences is being used to trace evolutionary ing of animal evolution is promised as insights from
relationships between long-divergent animal phyla, these methods are coupled with deeper knowledge
and thus to reconstruct a fairly true genealogy of of animal anatomy and embryology, based on old
animal life spanning over half a billion years. It is and new data, insights into divergence dates and
not a simple exercise, and one that is fraught with extinct character combinations, informed through
methodological and analytical problems, but enor- palaeontology, and refined understanding of gene
mous progress is being made. It is now clear that functions. A revolution in understanding animal
combining data from many genes simultaneously, evolution is upon us.
sometimes over 100 different genes from each spe-
Peter W. H. Holland
cies, can increase the reliability of phylogenetic
Linacre Professor of Zoology,
inference, as can analysis of rare genome-level
Department of Zoology,
changes, such as inversions and rearrangements
University of Oxford, South Parks Road,
of the DNA. Examples of both approaches are dis-
Oxford OX1 3PS, UK
cussed in this volume. These strategies have greatly
benefited from recent advances in high-throughput
DNA sequencing, a technology that is moving for-
ward apace, and as such we are truly in the middle
of a revolution in animal phylogenetics. Haeckel’s
trees are being updated with confidence.
 Acknowledgements

The basis for this book was as part of the tercenten- The majority of contributions have been consid-
ary celebrations of Linnaeus, for which we organ- erably updated or even significantly changed, and
ized a Discussion Meeting at the Royal Society we are delighted to include two entirely new chap-
and a follow-on meeting at a (now sadly extinct) ters. We would like to thank the authors and the
venue provided by the Novartis Foundation. many reviewers for their considerable efforts.
An issue of Philosophical Transactions of the Royal We thank our editors at OUP, Helen Eaton and
Society B: Biological Sciences (Volume 363, Number Ian Sherman, for their patience and support. We
1496) provided the core chapters and content for are pleased that we have been provided with the
this volume, and we thank OUP for their inter- opportunity to celebrate the bicentenary of the
est in publishing an updated issue as a stand birth of Charles Darwin with the publication of
alone volume. We gratefully acknowledge fund- this volume.
ing from The Royal Society, The Linnean Society Lastly, we dedicate this volume to those who
of London, The Systematics Association, and the inspired us to become zoologists and to our chil-
Novartis Foundation for making the original meet- dren, who demonstrate daily the delights and sur-
ing Evolution of the Animals—a Linnean Tercentenary prises of development, discovery, genotype, and
Celebration (June 2007) possible. phenotype.
Max Telford
Tim Littlewood

vii
This page intentionally left blank
Contents

Foreword v
Peter W. H. Holland
Acknowledgements vii
Contributors xi
Introduction xiii
Maximilian J. Telford and D. Timothy J. Littlewood

Part I: Origins of animals 1

1 The earliest fossil record of the animals and its significance 3

Graham E. Budd

2 The Ediacaran emergence of bilaterians: congruence

between the genetic and the geological fossil records 15
Kevin J. Peterson, James A. Cotton, James G. Gehling, and
Davide Pisani

3 Genomic, phylogenetic, and cell biological insights

into metazoan origins 24
Scott A. Nichols, Mark J. Dayel, and Nicole King

4 The mouth, the anus, and the blastopore—open questions

about questionable openings 33
Andreas Hejnol and Mark Q. Martindale

Part II: The Bilateria 41

5 Origins of metazoan body plans: the larval revolution 43

Rudolf A. Raff

6 Assembling the spiralian tree of life 52

Gonzalo Giribet, Casey W. Dunn, Gregory D. Edgecombe,
Andreas Hejnol, Mark Q. Martindale, and Greg W. Rouse

7 The evolution of nervous system centralization 65

Detlev Arendt, Alexandru S. Denes, Gáspár Jékely, and
Kristin Tessmar-Raible

8 The origins and evolution of the Ecdysozoa 71

Maximilian J. Telford, Sarah J. Bourlat, Andrew Economou,
Daniel Papillon, and Omar Rota-Stabelli

ix
x CONTENTS

9 Deciphering deuterostome phylogeny: molecular,

morphological, and palaeontological perspectives 80
Andrew B. Smith and Billie J. Swalla

10 Molecular genetic insights into deuterostome evolution from

the direct-developing hemichordate Saccoglossus kowalevskii 93
Christopher J. Lowe

Part III: Themes and perspectives 105

11 Invertebrate Problematica: kinds, causes, and solutions 107

Ronald A. Jenner and D. Timothy J. Littlewood

12 Improvement of molecular phylogenetic inference and

the phylogeny of Bilateria 127
Nicolas Lartillot and Hervé Philippe

13 Beyond linear sequence comparisons: the use of

genome-level characters for phylogenetic reconstruction 139
Jeffrey L. Boore and Susan I. Fuerstenberg

14 The animal in the genome: comparative genomics and evolution 148

Richard R. Copley

15 MicroRNAs and metazoan phylogeny: big trees from little genes 157
Erik A. Sperling and Kevin J. Peterson

16 The evolution of developmental gene networks: lessons from

comparative studies on holometabolous insects 171
Andrew D. Peel

17 Conserved developmental processes and the evolution of novel

traits: wounds, embryos, veins, and butterfly eyespots 183
Patrícia Beldade and Suzanne V. Saenko

18 Reassembling animal evolution: a four-dimensional puzzle 191

Maximilian J. Telford and D. Timothy J. Littlewood

References 197
Index 239
 Contributors

Detlev Arendt, Developmental Biology Unit, European Susan I. Fuerstenberg, Genome Project Solutions, 1024
Molecular Biology Laboratory, Heidelberg, 69117, Promenade Street, Hercules, CA 94547, USA
Germany James G. Gehling, South Australian Museum, North
Patrícia Beldade, Evolutionary Biology Group, Institute Terrace, Adelaide, South Australia 5000, Australia and
of Biology, Leiden University, PO Box 9516, 2300 RA Department of Geological Sciences, Queen’s
Leiden, The Netherlands and Instituto Gulbenkian de University, Kingston, Ontario, K7L 3N6, Canada and
Ciência, Oeiras, Portugal Department of Earth Sciences, Monash University,
Jeffrey L. Boore, Genome Project Solutions, 1024 Clayton, Victoria 3168, Australia
Promenade Street, Hercules, CA 94547, USA and Gonzalo Giribet, Department of Organismic and
University of California Berkeley, Department of Evolutionary Biology, & Museum of Comparative
Integrative Biology, 3060 Valley Life Sciences Building, Zoology, Harvard University, 26 Oxford Street,
Berkeley, CA 94720, USA and DOE Joint Genome Cambridge, MA 02138, USA
Institute and Lawrence Berkeley National Laboratory, Andreas Hejnol, Kewalo Marine Laboratory, PBRC,
2800 Mitchell Drive, Walnut Creek, CA 94598, USA University of Hawaii, 41 Ahui Street, Honolulu, HI
Sarah J. Bourlat, Department of Biology, University 96813, USA
College London, Darwin Building, Gower Street, Ronald A. Jenner, Department of Zoology,
London WC1E 6BT, UK The Natural History Museum, Cromwell Road,
Graham E. Budd, Department of Earth Sciences, London SW7 5BD, UK
Palaeobiology, Villavägen 16, Uppsala, Sweden Gáspár Jékely, Developmental Biology Unit, European
SE-752 36 Molecular Biology Laboratory, Heidelberg, 69117,
Richard R. Copley, Wellcome Trust Centre for Human Germany
Genetics, Roosevelt Drive, Oxford OX3 7BN, UK Nicole King, Department of Molecular and Cell
James A. Cotton, School of Biological and Chemical Biology, 142 Life Science Addition #3200, University
Sciences, Queen Mary University of London, Mile of California, Berkeley, CA 94720, USA
End Road, London E1 4NS, UK Nicolas Lartillot, Laboratoire d’Informatique, de
Mark J. Dayel, Department of Molecular and Cell Robotique et de Mathématiques de Montpellier,
Biology, 142 Life Science Addition #3200, University CNRS – Université de Montpellier 2, 161, Rue Ada,
of California, Berkeley, CA 94720, USA 34392 Montpellier Cedex 5, France
Alexandru S. Denes, Developmental Biology Unit, D. Timothy J. Littlewood, Department of Zoology, The
European Molecular Biology Laboratory, Heidelberg, Natural History Museum, Cromwell Road, London
69117, Germany SW7 5BD, UK
Casey W. Dunn, Department of Ecology and Christopher J. Lowe, Department of Organismal
Evolutionary Biology, Brown University, 80 Waterman Biology and Anatomy, University of Chicago,
Street, Providence, RI 02912, USA Chicago, IL 60637, USA
Andrew Economou, Department of Biology, University Mark Q. Martindale, Kewalo Marine Laboratory, PBRC,
College London, Darwin Building, Gower Street, University of Hawaii, 41 Ahui Street, Honolulu, HI
London WC1E 6BT, UK 96813, USA
Gregory D. Edgecombe, Department of Palaeontology, Scott A. Nichols, Department of Molecular and Cell
The Natural History Museum, Cromwell Road, Biology, 142 Life Science Addition #3200, University
London SW7 5BD, UK of California, Berkeley, CA 94720, USA

xi
xii CONTRIBUTORS

Daniel Papillon, Department of Biology, University Greg W. Rouse, Scripps Institution of Oceanography,
College London, Darwin Building, Gower Street, University of California San Diego, 9500 Gilman
London WC1E 6BT, UK Drive #0202, La Jolla, CA 92093, USA
Andrew D. Peel, Institute for Molecular Biology and Suzanne V. Saenko, Evolutionary Biology Group,
Biotechnology, Vassilika Vouton, 711 10 Iraklio, Crete, Institute of Biology, Leiden University, PO Box 9516,
Greece 2300 RA Leiden, The Netherlands
Hervé Philippe, Canadian Institute for Advanced Andrew B. Smith, Department of Palaeontology, The
Research, Département de Biochimie, Université de Natural History Museum, Cromwell Road, London
Montréal, Succursale Centre-Ville, Montréal, Québec SW7 5BD, UK
H3C3J7, Canada Erik A. Sperling, Department of Geology and
Davide Pisani, Laboratory of Evolutionary Biology, The Geophysics, Yale University, PO Box 208109, New
National University of Ireland, Maynooth, County Haven, CT 06520, USA
Kildare, Ireland Billie J. Swalla, Box 351800, 24 Kincaid Hall, Biology
Rudolf A. Raff, Department of Biology, Indiana Department, Un iversity of Washington, Seattle, WA
University, Bloomington, IN 47405, USA and School of 98195–1800, USA
Biological Sciences, University of Sydney, Sydney, Maximilian J. Telford, Department of Biology,
NSW 2006, Australia University College London, Darwin Building, Gower
Omar Rota-Stabelli, Department of Biology, University Street, London WC1E 6BT, UK
College London, Darwin Building, Gower Street, Kristin Tessmar-Raible, Developmental Biology Unit,
London WC1E 6BT, UK European Molecular Biology Laboratory, Heidelberg,
69117, Germany
 Introduction

The year 2009 is an important one for evolutionary The central questions of how animals originated
biologists, encompassing the 200th anniver- and how they diverged and radiated to become the
sary of the publication of Lamarck’s Philosophie diverse forms they are today are of sufficient inter-
Zoologique, the 200th anniversary of Darwin’s est to engage a varied group of scientists using an
birth and the 150th anniversary of the publication equally broad variety of approaches. More import-
of On the Origin of Species; the Darwin bicenten- antly, in spite of the problems so far encountered,
nial comes hot on the heels of the tercentenary of recent history suggests that much can be revealed
the birth of Linnaeus (2007), the original excuse about animal evolution and that the resolution of
for the meeting that assembled the authors of key branching points in the tree of life is indeed
this book. achievable. Our choice of authors, then, was further
While the anniversaries of Linnaeus, Lamarck, guided by the need to sample diversely across taxa,
and Darwin are clearly of particular significance disciplines, and over various scales of perspective
to evolutionary biologists, it is not hard to identify (time, level of biological organization), whilst pro-
other contemporary anniversaries marking the viding an overview of the key elements that make
beginnings of research topics that have had a major up modern studies of animal evolution through an
impact on the content of chapters in this book. The understanding of their genomes, fossils, and inter-
year 2009 sees the 100th anniversary of Walcott’s relationships. In this volume we chose to promote
discovery of the Cambrian fossils of the Burgess dialogue between systematists, palaeontologists,
Shales, the 25th anniversary of the discovery and evolutionary developmental biologists, reflect-
(twice) of the homeobox, and marks 21 years since ing our own interests but also, we believe, an area
the first analysis of metazoan phylogeny using where collaboration is driving a greater under-
small subunit rRNA sequences was published by standing of animal evolution.
Field et al. (1988) and, whilst the great significance Fossils are in a unique position to provide
of a 21st birthday might be questioned, we note additional characters for the resolution of phyloge-
that the original Field et al. publication appeared nies, polarization, and ordering of character trans-
on 12 February—Darwin’s birthday. formations and provide the time and ecological
The passage of time, its punctuation by not- background for the evolution of key novelties.
able events, the significance of individuals, and Graham Budd (Chapter 1) explores the nature and
the passing on of experience and knowledge beginnings of the animal fossil record, and con-
are of course all notable components of evolu- siders in particular the recent findings of fossil
tion itself, with the important additions of selec- embryos and other key forms, the incongruence
tion and diversity. Our selection of authors for between molecular and palaeontological estimates
this volume was by no means random, as we of the time of origin of major clades, and the nature
had crossed paths with them in the past either and significance of events around the Cambrian.
personally (as collaborators or colleagues), or Finally, Graham considers the evidence implicating
through their publications and presentations at oxygen as a potential engine driving the Cambrian
scientific meetings. explosion of animal diversity.

xiii
xiv INTRODUCTION

Employing the latest Bayesian methods for esti- larvae. With the appearance of larval forms, the
mating divergence times from molecular data, forces of evolution had an entirely new set of life
Kevin Peterson and colleagues (Chapter 2) con- forms (developmental stages) to act upon.
sider the vagaries of estimating divergence times Following in the wake of recent new phylog-
from the fossil record. They conclude that available enomic data sets involving hundreds of genes,
data satisfy the notions of a Cambrian explosion Gonzalo Giribet and colleagues (Chapter 6) tackle
of metazoans but indicate that the ecological and the interrelationships of the Lophotrochozoa, or the
evolutionary fuses were set with the emergence of Spiralia as they prefer to call them, and consider
the Bilateria in the Ediacaran. the newest of the new animal phylogenies, whilst
The origins of multicellularity are the focus of highlighting the anomalies, inconsistencies, and
attention of Nicole King’s team, led by Scott Nichols persistent gaps in both gene sampling and mor-
(Chapter 3), with a consideration of last common phological and developmental character coding.
metazoan ancestors by means of a comparison of Studies of individual organ systems provide a
shared features, including patterns of gene expres- particular insight into evolutionary patterns and
sion, particularly in the diploblasts. Finally, they processes. Drawing from elegant comparative
consider the emergence of the eumetazoan epithe- studies, Detlev Arendt and co-authors (Chapter 7)
lium that, arguably, provided the means by which reveal complex similarities between the pattern-
complex specialized organ systems subsequently ing of the central nervous system of a protostome
evolved (Schmidt-Rhaesa, 2007). (the annelid worm Platynereis dumerilii) and that of
The characteristics of the last common ances- the chordates. They conclude that the protostome/
tor of the Bilateria, the so-called ‘Urbilateria’, are deuterostome ancestor already had a centralized
of great current interest and, in addition to the rather than diffuse nervous system patterned in
study of fossils, there are two approaches being this way and suggest that the diffuse nervous sys-
employed to reconstruct this animal. The first is to tem in hemichordates is therefore a derived char-
attribute to Urbilateria the shared characteristics of acteristic.
the protostomes (Lophotrochozoa and Ecdysozoa) Charting the recent emergence of a major new
and the deuterostomes. The second approach is to clade, the Ecdysozoa, and the battles for and
look directly at the extant members of what may against accepting its validity is an exercise in
be an even earlier branch to consider their biol- understanding modern animal evolutionary stud-
ogy as a clue to the nature of bilaterian ancestors. ies. Max Telford and colleagues (Chapter 8) show
Andreas Hejnol and Mark Martindale (Chapter 4) that the Ecdysozoa are here to stay and discuss
draw upon their recent studies of gene expression the new interpretation of morphological characters
in the basally branching acoel Convolutriloba longi- suggested by their interrelationships.
fissura to consider gastrulation and, in particular, One major clade that has persisted since before
the relationships between the openings of the ali- the molecular revolution in phylogenetics is the
mentary canal and the blastopore, details that may Deuterostomia but its membership and their inter-
define major subdivisions of the Bilateria. relationships, particularly the placement of enig-
As Rudy Raff (Chapter 5) reminds us, the origins matic fossils and worms, has provided a vibrant
of bilaterian animal body plans are not only about forum for interdisciplinary studies. With the wealth
adult forms. Understanding animal evolution is as of information from genomes, development, and
much about revealing and explaining the evolu- morphology, this mixture of invertebrates and ver-
tion of ontogenies. Reviewing evidence from gene tebrates has posed a considerable number of prob-
expression of patterning genes, phylogeny, morph- lems for scientists integrating independent data
ology, and palaeontology, Raff argues that many sets, as Andrew Smith and Billie Swalla explain
larval features may have arisen independently, (Chapter 9).
with new features emerging as adult bilaterian- Chris Lowe (Chapter 10) describes studies com-
expressed genes being co-opted for use in pelagic paring development in the chordates with those of
 INTRODUCTION xv

Xenambulacrarian hemichordates. Despite signifi- (Chapter 14) asks where in the genomes do the
cant differences in morphology, the degree of con- phenotypic differences between animal taxa arise?
servation of gene expression patterns is striking, Notwithstanding the paucity of current taxon sam-
and Lowe alludes to the confidence and insight pling that requires us to consider existing model
gleaned from establishing ancestral gene networks laboratory organisms as exemplars of metazoan
as a basis for understanding homology. These at diversity, it seems clear that the more we know
least provide a sound basis for interpreting the about comparative genomics the more we can
diversity of forms that such gene networks have reveal about function across the genome. Copley
given rise to. argues that to understand fully the differences and
The study of animal evolution is beset by prob- similarities between genomes, it is necessary to go
lems in all shapes and forms. From a systematic well beyond catalogues of shared genes. Instead, it
perspective, particular taxa have risen to become is an understanding of the interactive components
problematic in themselves; interpreting their biol- that link genotype with phenotype that will allow
ogy in order to glean statements of homology, genomic studies to contribute to what might be
placing them in a phylogeny, or reconciling their construed as a return to organismal biology in its
biology with their phylogenetic placement. Such modern sense, where entire animals are viewed in
Problematica are the subject of the contribution by a comparative evolutionary context integrating all
Ronald Jenner and Tim Littlewood (Chapter 11), available evidence.
who review the kinds and causes of problematic Meanwhile, somewhat in contrast to the ‘more
taxa amongst the invertebrates, whilst attempting genes’ approach to phylogenetics, Erik Sperling
to formulate some possible solutions for dealing and Kevin Peterson (Chapter 15) show that micro-
with them in time. RNAs, small, ubiquitous, non-coding regulatory
Denser taxon and character (particularly gene) genes, have the power to resolve phylogenies
sampling is widely heralded as the means by which across the animal tree of life and argue that their
more accurate phylogenies can be resolved, yet unique properties make them the new characters
Nicolas Lartillot and Hervé Philippe (Chapter 12) of choice.
explain how the power of phylogenomics can only Andrew Peel (Chapter 16) addresses questions
be harnessed properly by employing improved of the evolution of novelty in the insects, looking
models of molecular evolution. Regardless of at the evolution of long- versus short-germ devel-
method of analysis, their contribution shows that opment in the holometabolous insects. One major
novel relationships require a biological explan- conclusion is that developmental modes are not
ation. Of course, evolutionary signal from molecu- fixed in stone and have evolved both divergently
lar data does not stem uniquely from nucleotides and convergently in the insects. Morphology
and amino acid sequences of individual genes. Jeff and developmental genetic networks can effect-
Boore and Susan Fuerstenberg (Chapter 13) look ively become decoupled; one result of which is
at the prospects for comparing entire genomes, that attributing homology to developmental fea-
from their constituent molecules to the biochem- tures based on common gene expression can be
ical and developmental pathways they control, for misleading.
providing suites of new characters for phylogenetic The diversity of non-model systems is steadily
reconstruction. increasing. Patrícia Beldade and Suzanne Saenko
As evolutionary biologists become more involved (Chapter 17) describe one such system, the butter-
in choosing taxa for genome characterization, or fly Bicyclus anynana, and their approach for study-
even characterizing genomes in their own labora- ing one striking aspect of these butterfl ies, their
tories thanks to second-generation sequencing wing eyespots. The fi nding that evolutionary
technologies, it is clear that the depth of sam- novelties such as wing eyespot development have
pling needed to build and interpret the new ani- involved the redeployment of genes from well-
mal phylogeny is currently thin. Richard Copley understood pathways involved in other diverse
xvi INTRODUCTION

aspects of patterning in fruitflies gives one line and with new technologies comes renewed enthu-
of promise for the inclusion of many more diverse siasm. Each generation has the opportunity to
taxa as model laboratory organisms for evo-devo build on the successes and insights of those gone
research. by and to contribute to further understanding the
In the final chapter we take the opportunity to animal in us all.
consider some of the major steps made in the study
Maximilian J. Telford
of animal evolution, and the remaining hurdles
and D. Timothy J. Littlewood
that have a chance of being overcome in the next
few decades. With new data come new perspectives
PA R T I
Origins of animals
This page intentionally left blank
 CHAPTER 1

The earliest fossil record of the

animals and its significance
Graham E. Budd

The fossil record of the earliest animals has been processes that took place long before? Even if the
enlivened in recent years by a series of spectacular fossil record of that time is accurately recording
discoveries, including embryos, from the Ediacaran the unfolding of events in real time, the question
to the Cambrian, but many issues, not least of dat- of why the events took place then—and what the
ing and interpretation, remain controversial. In potential trigger was—has continued to be prob-
particular, aspects of the taphonomy of the earli- lematic. The Cambrian explosion itself has been
est fossils require careful consideration before pro- much discussed (Gould, 1989; Conway Morris,
nouncements about their affinities. Nevertheless, a 1998a, 2003a; Knoll and Carroll, 1999; Budd and
reasonable case can be now made for the extension Jensen, 2000; Knoll, 2003). Here I want to focus on
of the fossil record of at least basal animals (sponges three issues: the age of the earliest animal fossils,
and perhaps cnidarians) to a period of time signifi- the continuing debate about their affinities, and
cantly before the beginning of the Cambrian. The finally, a critical examination of the most popu-
Cambrian explosion itself still seems to represent lar candidate for ‘triggering’ the explosion; the
the arrival of the bilaterians, and many new fos- concentration of atmospheric oxygen.
sils in recent years have added significant data Geologists as long ago as William Buckland
on the origin of the three major bilaterian clades. (1784–1856) realized that a dramatic step change in
Why animals appear so late in the fossil record is the fossil record occurred at the base of what we
still unclear, but the recent trend to embrace ris- now call the Cambrian. The apparent appearance
ing oxygen levels as being the proximate cause in the fossil record of many animal groups with
remains unproven and may even involve a degree few or no antecedents caused Charles Darwin great
of circularity. trouble—indeed he devoted a substantial chapter
of the Origin to this problem. Further insights were
provided by the remarkable amount of work on
1.1 Introduction
North American faunas by Charles D. Walcott, who
The ‘Cambrian explosion’ is a popular term that proposed that an interval of time, or the ‘Lipalian’,
refers to the period of profound evolutionary and was not represented in the fossil record and/or
environmental change that took place at the open- did not preserve fossils and that the forms ances-
ing of the Phanerozoic some 540 million years ago tral to the Cambrian taxa evolved during this time.
(Ma). Although this set of events is multifaceted, it However, the intense modern interest in the subject
is associated primarily with the origin of animals was probably sparked by the work of Whittington
in the fossil record. For over 150 years, an argu- and colleagues in their redescriptions of the
ment has raged about the reality of this event. Is it Burgess Shale (see below), together with Stephen
a genuine evolutionary event, or merely a sudden Jay Gould’s popular account of this work, Wonderful
manifestation in the fossil record of evolutionary Life, published in 1989. In recent years, the attention

3
4 ANIMAL EVOLUTION

paid to the youngest part of the Precambrian has of how Cambrian taxa should be classified; and
led to the erection of the formal Ediacaran Period (3) various dating problems.
of c. 630–542 Ma (Knoll et al., 2006), an interval that
has been intensely scrutinized for its bearing on
1.2.1 The Doushantuo Formation and its
the origin of the animals.
taphonomy
The processes that convert a living organism into a
1.2 Fossil evidence for the origin of
mineralized or organically preserved fossil are far
animals: the state of play
from being fully understood; nevertheless, at least
The classical fossil evidence for the early evolu- some understanding of them is essential if fossils
tion of animals consists of several sources: trace are to be successfully interpreted (Butterfield et al.,
fossils, the Ediacaran biota from just before the 2007). Nowhere has this been more important than
beginning of the Cambrian (Narbonne, 2005), the the evaluation of the various exceptional faunas
conventional Cambrian fossil record (Bengtson, around the Precambrian/Cambrian boundary. Of
1992), and the Burgess Shale fauna (Briggs et al., particular recent interest has been the Doushantou
1995). In recent years these data sources have been Formation (Fm) of South China. This c. 250-m thick
enriched by further important discoveries, espe- sequence of siliciclastic, phosphatic, and carbonate
cially new Cambrian exceptional faunas such as rocks has yielded exceptionally preserved puta-
the Chengjiang fauna (Hou et al., 2004) and indeed tive examples of algae, acritarchs, and metazoan
very substantial new discoveries from the Burgess embryos and adults including sponges and a bila-
Shale itself (Caron et al., 2006; Conway Morris terian (Chen et al., 2000; Xiao and Knoll 2000; Yin
and Caron, 2007); the Doushantuo fossils from et al., 2001, 2007; Chen and Chi 2005; Dornbos et al.,
the Ediacaran period of the latest Precambrian 2006; P. J. Liu et al., 2006; Tang et al., 2006; Xiao et al.,
(Xiao and Knoll 2000; Xiao et al., 2007a; Yin et al., 2007a). However, nearly all of these fossils have
2007), and more Ediacaran discoveries, such as proved highly controversial. One reason for this is
from Namibia, Newfoundland, and the White Sea clear: the Doushantuo Fm has been dated to well
(Grazhdankin and Seilacher, 2002; Narbonne, 2004). before the beginning of the Cambrian, and thus
Outside the Cambrian, the Silurian Herefordshire these fossils would undoubtedly include the oldest
fauna has also yielded some remarkable fossils animals in the record (but see below).
that have had significant bearing on the origins of The preservation in phosphate of many
various animal clades (e.g. Sutton et al., 2001a, 2002; Doushantuo fossils leads to problems of disen-
Siveter et al., 2007). The volume of data that the fos- tangling primary morphology from subsequent
sil record has brought to bear on the issue of the taphonomic overprints (Bengtson and Budd, 2004;
origin of the animals has thus notably increased Xiao et al., 2000). As a result of such concerns,
in recent years, explaining the exciting dynamism some of the more extravagant claims, such as that
that currently characterizes the field. Nevertheless, the Doushantuo biota includes representatives of
even a casual observer would note that few of these bilaterians and deuterostomes, do not currently
new inputs have been without controversy; with stand up to scrutiny. Nevertheless, and not with-
high-profile publications regularly attracting pub- standing attempts to provide alternative bacterial-
lished responses or critical reviews. The undeni- affinity explanations (Bailey et al., 2007a,b; Xiao
able difficulties surrounding these data can be et al., 2007b), the Doushantuo fossils remain as
attributed to several causes: (1) an often incomplete convincing embryos. Even if the presence of phos-
understanding of the taphonomy (i.e. the complete phatized embryos is accepted though, a significant
set of preservational processes surrounding the amount of disagreement over their precise dating
production of the final fossil), a lack that has often remains, which, in its extreme, would extend the
led to interpretation of ambiguous fossils in a pre- range of animals down to close to the opening
conceived manner; (2) the continuing discussion of the Ediacaran at around 630 Ma, while at the
 E ARLIEST FOSSIL RECORD OF THE ANIMAL S 5

other extreme the Doushantuo fossils may not sig- An additional aid to dating comes in the form
nificantly pre-date the oldest Ediacaran fossils at of chemostratigraphy, especially using GC13, which
around 565 Ma. suggests that the Doushantuo Fm is marked by three
negative GC13 excursions: one at the base, associated
with the so-called ‘cap carbonates’ that directly
1.2.2 Towards a chronology of the latest
overlay the glacial deposits; one in the middle, and
Precambrian
one near the top (Condon et al., 2005). It has often
The later stages of the Precambrian are marked been thought that the excursion towards the top is
by glaciations of global extent that show up in the associated with the Gaskiers glaciation, in which
record as, for example, a series of tillites (lithi- case the age of the Doushantuo Fm would range
fied glacial sedimentary rocks of mixed compos- from about 580–635 Ma. The significance of these
ition that are formed as the result of movement dates is that all of the Doushantuo fossils would
by ice). These glaciations have been suggested pre-date the oldest of the famous Ediacaran fossils
to be evidence for the so-called ‘snowball earth’, such as Dickinsonia etc., and thus would provide an
i.e. intervals of time when the earth was effect- independent record of animal life during a period
ively deep-frozen. The amelioration of conditions of time for which no large-body fossils or trace fos-
after these glaciations has been suggested to be a sils are known. Indeed, the overlying Dengying
key factor in the rise of the animals (Runnegar, Fm does yield Ediacaran-type fossils, which could
2000), although the mechanism for such a direct be said to support this contention. However, some
causality remains largely obscure. The interval recent work has questioned this view, suggesting
of time known informally as the ‘Cryogenian’, that it is the middle GC13 in the Doushantuo Fm
from approximately 850–630 Ma is marked in the that corresponds to the Gaskiers Fm (despite the
Australian record by two distinct ice intervals: the lack of other evidence for glaciation in the type
‘Sturtian’ and the ‘Marinoan’ (Kennedy et al., 1998). area; in the Weng’an section, a definite break in the
These glacial intervals can be correlated with gla- sequence at this point could be correlated with gla-
cial deposits elsewhere in the world, such as in cially related drop in sea-level). This would con-
China (Zhou et al., 2004). In addition, a further strain the age of the upper Doushantuo Fm units
short-lived glacial interval, the ‘Gaskiers’, known to lie within about 551 and 580 Ma (Dornbos et al.,
primarily from Newfoundland (Eyles and Eyles, 2006), and, as it is this interval that is thought to
1989), has been dated to be c. 580 Ma. Correlating yield the animal fossils, these fossils could plaus-
Precambrian glacial intervals worldwide is diffi- ibly be regarded as being of a similar age to the
cult at best, largely because of the lack of accurate Ediacaran assemblages. In order for this model to
biostratigraphical control, and the task is compli- be correct, some of the published radiometric dates
cated by the technical problems associated with for the Doushantuo Fm would have to be incorrect
the various types of absolute radiometric dating. (Barfod et al., 2002), but given the care required to
As a result, a number of minority views exist, such interpret whole-rock radiometric dates, this possi-
as that the Marinoan and Gaskiers glaciations are bility cannot simply be ruled out.
identical (based on dating in Tasmania; Calver More recently, the claim has been made that at
et al., 2004). As far as the dating of the Doushantuo least one of the enigmatic acanthomorphic (i.e.
Fm goes, the glacial rocks below can be dated spinose) acritarchs (see Figure 1.2), which are nor-
to close to 635 Ma, and the base of the overlying mally assigned to protist groups such as the green
Dengying Fm, has been dated to 551 Ma (Condon algae and dinoflagellates, are actually the hulls
et al., 2005). A complicating factor is that the well- of diapause animal eggs (Yin et al., 2004, 2007).
preserved fossils of the Doushantuo Fm are known Although the fossil in question, Tianzhushania, is
not from its type locality but from the Weng’an known to contain embryos only in the upper part
locality, which consists of a much shorter (c. 40 m of the Doushantuo Fm, it ranges down to very
thick) section made up largely of two phosphoritic close to the base, and thus to 630 Ma or so. The
units (Dornbos et al., 2006). claim would be that the oldest animal fossils of
6 ANIMAL EVOLUTION

the Doushantuo Fm, dating back to just after the Ordovician

Nantuo glaciation (i.e. the Chinese glacial deposits 490
(part)
normally correlated with the Marinoan) are of this Upper
age, a time that pre-dates the first Ediacaran fossils 500 Cambrian
Middle
by some 60 million years, as well as the more con- Cambrian
510 Burgess shale
servative molecular clock estimates for the diver- preservation
gence of the bilaterians. 520
8 Lower
Despite the obvious uncertainties, the most
Cambrian
reasonable interpretation of the data is thus that 530
4
embryo-forming animals of some sort had evolved 1 6
540
by just after Marinoan time; that sponges and
7
presumed other animals had started to emerge 550 3
by 580 Ma at the latest; and that the Ediacaran
560 5
biotas are likely to be a little younger than the E
Doushantuo embryos. The upshot of the new data 570
is that much more convincing evidence exists in
the fossil record for an origin of the animals con- 580 D

Ediacaran
“Formative Gaskiers glaciation
siderably before the Cambrian than it did 10 years interval”
590
ago (Budd and Jensen, 2000), with an inferred
documented fossil origin of the entire clade being 600 2
datable to just after 635 Ma—a significant result C
(see Figure 1.1 for summary). 610
If animals had already evolved at this time, why
620
is it that the rest of the record does not correlate
with it—why are there no macro body fossils and 630
no (generally accepted) trace fossils? The answer B
Marinoan glaciation
to this question, which on the face of it seems to 640
directly contradict predictions (Budd and Jensen,
650
2000) that no animals existed significantly before
the first good trace fossils at around 555 Ma, may 660
hinge on what sorts of organisms these embryos A
represent. Given their relatively unusual develop-
Figure 1.1 Provisional timescale for events around
ment, with large numbers of cell divisions taking the Precambrian/Cambrian boundary: 1, range of large,
place without any sign of gastrulation or epithe- acanthomorphic ‘Ediacaran’ acritarchs; a genus that contains
lial formation, it has been suggested that they are metazoan-like embryos is found from close to the bottom of their
from stem-group metazoans; i.e. from organisms range just above the Marinoan glaciation rocks; 2, possible range
of Doushantuo embryos and cnidarian-like fossils according to
more basal than any living animals including
Barfod et al. (2002); 3, possible range of the same according
sponges (Hagadorn et al., 2006). Given that such to Condon et al. (2005), which if correct is uncertain,but the
an organism, lacking muscles and other features former is favoured here; 4, the ‘Ediacaran’ biota; 5, trace fossils;
of the more derived bilaterians, would be unlikely 6, Cloudina and Namacalathus; 7, classical small shell fossils. The
readily to form either body or trace fossils, such an letters correspond to key dated points in metazoan evolution in
Peterson and Butterfield (2005) based on minimum evolution:
assignment is consistent with the hypothesis that
A, origin of crown-group Metazoa; B, total-group Eumetazoa;
bilaterians emerged later, close to the Precambrian– C, Crown-group Eumetazoa; D, crown-group Bilateria (here
Cambrian boundary. equivalent to Protostomia plus Deuterostomia); E, crown-group
What is perhaps more surprising is the gen- Protostomia. The ‘formative interval’ during which distinctive
eral lack of convincing sponge spicules from the bilaterian features were assembled according to this dating is
marked by arrows.
Precambrian (Gehling and Rigby, 1996; Brasier
 E ARLIEST FOSSIL RECORD OF THE ANIMAL S 7

Many workers (Smith, 1984; Runnegar, 1996; Budd

and Jensen, 2000) have seen the apparently more
bizarre forms as lying in the stem groups of the
extant phyla, thus providing a critical basis for
understanding the origin of animals as we see them
today. A corollary of this view is that the modern
phyla, strictly considered, often do not emerge until
some time after the classical Cambrian explosion,
with the major radiation associated with the begin-
ning of the succeeding Ordovician period being at
least as important for the emergence of modern
body plans. Conversely, other writers have seen this
definition of the phyla to be overly legalistic (Knoll,
Figure 1.2 The Ediacaran acanthomorphic acritarch Tanarium
pluriprotensum from the Tanana Formation, in the Giles 1 drillcore, 2003; Valentine, 2004; Briggs and Fortey, 2005). Part
Officer Basin, Australia (×75). At least some Precambrian of the disagreement is a relatively uninteresting
acanthomorphic acritarchs may be the eggs of animals. Courtesy of one over terminology (i.e. when does a fossil qual-
S. Willman. ify to be straightforwardly called an ‘echinoderm’
for example), but this surface dispute conceals a
more important issue, which is over the actual tim-
ing of the establishment of the extant body plans.
et al., 1997; Li et al., 1998); given that living sponges The difficulty partly arises because it is often hard
may be paraphyletic, stem-group metazoans to say with confidence when the ‘crown node’ that
should be spiculate, and spicules should thus be subtends the crown group has been attained.
present very early on. If this absence is genuine Although a crown group can be defined empir-
as opposed to taphonomic (Pisera, 2006), then the ically by the results of a cladistic analysis and
suggestion would be that crown-group metazoans supported by the synapomorphies at its base, the
did not evolve until close to the beginning of the practical issues involved in placing any particu-
Cambrian. Finally, the suggestion that mineralized lar fossil within or outside it can be difficult to
sponge spicules are convergent within sponges resolve. In order to identify membership of the
and thus need not characterize basal metazoans at crown group, it is necessary not only to show that
all (Sperling et al., 2007) is one other obvious way the fossil in question possesses the set of plesio-
around this impasse. In summary there seems to morphic features associated with its crown group
be no good reason as yet to place the radiation of (i.e. it lies within at least the total group), but also
the bilaterians significantly before the first decent that it possesses at least one apomorphy of one of
trace fossils at around 555 Ma or so; although the clades included within it. This task is compli-
evidence for the presence of metazoans of some cated by the phylogeny of the ingroups often being
sort considerably before this point seems to be uncertain (with a good example being provided by
hardening. the molluscs), and by the possibility of apomor-
phic character states for an in-group of the phylum
actually being plesiomorphic, but lost in the sister
1.2.3 The status of Cambrian fossils
group to the group that now possesses them (Budd
The years in which the various exceptionally pre- and Jensen, 2000). Such a possibility is locally
served fossils from the Cambrian were viewed as unparsimonious, but may not be globally so. The
representing a plethora of body plans essentially net result of these two effects is that although a
unrelated to the extant phyla have now passed, taxon may look rather similar to a crown-group
closing a tradition that dates back many decades member of its phylum, its crown-group status can-
(Nursall, 1959). Nevertheless, the significance of not be confirmed. For example, there are several
Cambrian taxa continues to be hotly debated. Cambrian taxa such as Ottoia that closely resemble
8 ANIMAL EVOLUTION

crown-group priapulids, but nevertheless lie near itself. A far from inclusive list might include the
the top of the stem group (Wills, 1998; Dong et al., arthropods, molluscs, priapulids, and brachiopods:
2004). As a result, the formal origin of the crown Cambrian life is different, but not alien. Therefore,
group is pushed much later, probably to the although the recognition that crown groups in gen-
Carboniferous. It nevertheless seems fairly clear eral evolve late allowing some body-plan evolution
that the basic features of the priapulids had been to be ‘smeared upwards’ into the Palaeozoic (Budd
attained early on in their history, and the formal and Jensen, 2000), the latest Proterozoic and earliest
origin of the crown group, although strictly accur- Cambrian were still highly significant periods dur-
ate for determining the point at which the modern- ing which the classical features of the phyla as we
day body plan appeared (at least as measured by see them today were partly, or even largely, assem-
the fossil record), is a trivial event compared with bled. These include the origins of segmentation, the
the evolution of the basic form that took place in coelom, blood-vascular and nervous systems, and
the Cambrian (Fortey et al., 1996). nephridia. A major unsolved question of course
As a result of this potentially misleading appli- is whether or not these features evolved once, at
cation of the stem-group/crown-group distinc- the base of the bilaterians, and were then subse-
tion, the alternative idea of extending the phylum quently lost as the early bilaterians radiated into
concept phylogenetically backwards to incorpor- niches where they were functionally pointless (e.g.
ate formal members of the upper stem group is in the meiofauna) or whether they evolved inde-
favoured by several writers. While this proposal pendently several times under strong convergent
has its merits, it has obvious drawbacks too: for pressure (Conway Morris, 2003a,b), often using a
example, how unlike the modern phylum does similar developmental toolkit to do so. This ques-
a stem-group member need to be before being tion would be resolvable by a much more precise
excluded from the group and other problems asso- phylogeny than is currently available and must be
ciated with the erection of subjective paraphyletic regarded as a major aim of the investigation of the
groups? Although the formal stem-group concept origins of the animals.
is of course paraphyletic, it at least has the advan-
tage of being objectively so, with the arbitrary but
1.2.4 Recent advances in basal animal
empirical datum point being survivorship to the
palaeontology
modern day.
Despite the objections to the idea then, the use Study of the fossil record of the oldest animals has
of the stem-group/crown-group distinction has been enlivened by the molecular evidence that the
the advantages of providing a fixed and objective extant sponges are paraphyletic, with the Calcarea
measure that is comparable across phyla for when being more closely related to the Eumetazoa than
the modern clade can be formally recognized in the the other sponges (Cavalier Smith et al., 1996;
fossil record; and it does not seem that any alterna- Borchiellini et al., 2001; Peterson and Butterfield,
tive proposals, which may rely on a subjective or 2005). Such a finding gives hope of understand-
even misleading assessment of what an ‘important’ ing the vexed issue of what sort of organism
character for a particular clade is, offer much of an the eumetazoans (i.e. cnidarians plus bilateri-
advance. ans) evolved from. Indeed, the notable discovery
Although I wish to continue to defend the use of (Botting and Butterfield 2005) that the Burgess
the stem-group/crown-group distinction as being Shale sponge Eiffelia (Figure 1.3a) possesses both
of phylogenetic and historical importance, the rea- hexaradiate spicules (characteristic of calcareans)
sons for its rejection are certainly worth serious and tetraradiate spicules (characteristic of hex-
consideration. It is clear that by Burgess Shale time actinellids), suggests that the fossil record may
in the Middle Cambrian (i.e. about 507 Ma) most allow at least some insights into the earliest tran-
extant clades had appeared, and many of them sitions in animal evolution; insights that comple-
had members that were, at least in a broad sense, ment those, not uncontroversially, already attained
recognizable as being similar to the crown group for other basal groups such as the ctenophores
 E ARLIEST FOSSIL RECORD OF THE ANIMAL S 9

(a) (b)

Figure 1.3 Basal metazoan fossils. (a) Eiffelia globosa from the Middle Cambrian Burgess Shale (ROM 57023; ×5.0) (Botting and
Butterfield 2005). As well as the prominent hexaradiate spicules typical of calcarean sponges, rows of smaller, hexactinellid-like tetraradiate
spicules are also visible (arrowed). Courtesy of N. J. Butterfield. (b) A section of Sinocyclocyclicus guizhouensis from the Ediacaran Doushantuo
Formation (Xiao et al. 2000; Liu et al. 2008) (×130). This small, branching tabulate fossil has been interpreted as being a potential stem-
group cnidarian. Courtesy of Shuhai Xiao.

(Conway Morris and Collins, 1996; Shu et al., 2006; (Zhang and Reitner, 2006), and Newfoundland
Chen et al., 2007). (Narbonne, 2004), has added information about
Conversely, the early record of cnidarians their morphology, and has led to claims that some
remains uncertain. Whilst some of the Ediacaran of these taxa can now be accommodated in the stem
taxa, especially the fronds and disc-shaped fos- or crown of groups such as the ctenophores (Dzik,
sils, have classically been interpreted as cnidar- 2002; Shu et al., 2006; Zhang and Reitner, 2006), the
ians, the interpretation of these remains in doubt, ever-present problem of taphonomy, particularly
partly because of profound differences in growth acute in the ediacarans, means that any claims
patterns (Antcliffe and Brasier, 2007). On the other for certain affinities must be treated with a great
hand, the Doushantuo Fm has once again gener- deal of caution. Nevertheless, given the potentially
ated material of interest, especially the branching pivotal morphology, molecular development, and
tabulate form Sinocyclocyclicus (Xiao et al., 2000), phylogenetic position of the ctenophores (Yamada
material that, although potentially algal, does dis- et al., 2007), the developing leitmotif of ctenophore-
play a set of characters that are compatible with like morphologies in the late Ediacaran might just
cnidarian affinities (Figure 1.3b). Thus, sponges, be pointing towards substantial advances in the
cnidarians, and potentially ctenophores are all area of understanding stem-group eumetazoans
known from Precambrian strata. These findings, and bilaterians in the not too distant future.
and the continuing general lack of convincing evi- As for the bilaterians themselves, new data con-
dence for bilaterians until just before the beginning tinue to be generated from the major Cambrian
of the Cambrian, all suggest that ‘radiate’ animals lagerstätten such as new collections of Burgess Shale
were radiating during the Ediacaran, and that the material, including a remarkable reassessment of
Cambrian explosion itself represents the radiation the previously highly problematic Odontogriphus as
of bilaterians (Benton and Donoghue, 2007). a stem-group mollusc (Caron et al., 2006) and other
The status of the classical Ediacaran fossils, such taxa claimed as stem-group lophotrochozoans,
as Spriggina, Dickinsonia, etc., remains highly uncer- such as the ‘halwaxiids’ (Conway Morris and
tain. While new well-preserved material from, for Caron, 2007). It should also be noted that advances
example, Namibia (Dzik, 2002), the White Sea area in photographic techniques (Bengtson, 2000) have
10 ANIMAL EVOLUTION

also greatly increased the ease with which data 1.3 What caused the Cambrian
from Burgess Shale fossils can be extracted. explosion?
Persistent claims are made that members of the
Ediacaran biota should be considered to be bilateri- The age-old question of why animals evolved
ans, especially the clearly complex Kimberella from when they did, and not, for example, 500 million
the White Sea area (Fedonkin and Waggoner, 1997), years before, continues to trouble researchers. In
a claim that has been revitalized by the discovery one sense, the question is trivial, in the same way
of the molluscan affinities of the rather similar that the question of ‘why did the First World War
Odontogriphus from the Burgess Shale (Butterfield, take place in the 20th, rather than the 16th cen-
2006; Caron et al., 2006). tury?’ is. Clearly, whenever this event took place,
The conventional record, too, continues to the same question could be asked, and the general
provide provocative material, including recent answer of ‘many other things had to happen first’
evidence that the highly enigmatic but very wide- is not as vacuous as it at first appears. Nevertheless,
spread tommotiids from the Lower Cambrian a serious point remains: is there a set of conditions
are lophophorate relatives (Holmer et al., 2002, that had to be in place in order to release animal
2008; Skovsted et al., 2008). Thus, the fossil record evolution? When David Nicol reviewed the ques-
is providing important new data that might go tion 40 years ago (Nicol, 1966) he listed some of the
some way to help resolving one of the most vexed hypotheses that had been put forward up to that
problems in animal phylogeny, the relationships point, some of which now seem quaint, for example
between the protostomes. The Chengjiang fauna the view that life evolved on land and only reached
has also provided material (controversially) rele- the sea, and thus could become readily fossilizable,
vant to the origins of the deuterostomes, with in the Cambrian, or that animals adopted a more
the vetulicolans being claimed as a new deuter- sluggish mode of life to which hard parts were
ostome phylum, as well as several craniates and appropriate—the exact opposite of the more nor-
even vertebrates that significantly extend their mal ‘arms race’ view of the development of hard
record back in time (Chen et al., 1995,1999; Shu parts prevalent today (Vermeij, 1993; Bengtson,
et al., 1996b, 1999, 2001b, 2003a,b). The fi nal major 2002). In all of these ideas a more or less constant
group of bilaterians, the ecdysozoans, although factor has been the level of oxygen.
widely accepted, remains controversial in terms
of in-group relationships (Budd, 2002; Waloszek 1.3.1 Did oxygen fuel an explosion?
et al., 2005a, 2008). The arthropods are now largely
accepted to have arisen via a rather heteroge- Without any doubt, the most popular candidate for
neous group of lobopods, although the exact root causing—or allowing—the Cambrian explosion is
is far from agreed on (Budd, 1996; Zhang and a rise in oxygen levels at the end of the Proterozoic
Briggs, 2007). In addition to the arthropods, the (Nursall, 1959). In one sense, this is an excellent
cycloneuralians have come under some scrutiny, choice of causal agent, as no-one will ever know
especially since the description of stem-group exactly what oxygen levels were like during that
scalidophoran embryos from the Lower Cambrian period of time. Nevertheless, the perennial debate
(Budd, 2001a; Dong et al., 2004; Donoghue et al., about oxygen levels in the Proterozoic has been
2006a; Maas et al., 2007). Nevertheless, the intri- sharpened recently by intense interest in the subject,
guing question of what sort of animal the last which has led to many more data and a clearer pic-
common ancestor of the ecdysozoans was like ture of the rise of oxygen levels in the atmosphere.
(Budd, 2001b) remains currently unanswered, at The oxygen debate is not, in this context, simply
least from the fossil record, although the suspi- about what levels of oxygen pertained at various
cion that the earliest lobopods such as Aysheaia times in the Proterozoic, interesting and intract-
(Whittington, 1978) are more or less priapulids on able though that question has proved (Lambert
legs is not one that is easily shaken off (Dzik and and Donnelly, 1991; Runnegar, 1991; Canfield and
Krumbiegel, 1989). Teske, 1996; Thomas, 1997; Canfield et al., 2007). It is
 E ARLIEST FOSSIL RECORD OF THE ANIMAL S 11

narrowly focused on the following two questions: modified in a similar way, although the roles of the
(1) when did oxygen levels first permanently rise two respective end products, hydroxyproline and
high enough to permit the evolution of any sort hydroxylysine, are very different.
of metazoan? and (2) did low oxygen levels limit Although post-translational modification of pro-
the fossilization potential of early metazoans? The teins and indeed their component amino acids is
second question has widely been considered to common (for example, removing the methionine
have a positive answer, and to provide the explan- start codon; acetylation or phosphorylation), the
ation for why animal fossils do not appear in the specific hydroxylation of proline raises the question
record until just before the Cambrian, despite some of why hydroxyproline is not included in the pri-
evidence that they evolved hundreds of millions of mary code. The obvious answer is that this amino
years before this. It is also worth stating at the out- acid was not used by organisms when the genetic
set that the whole oxygen level debate has recently code first originated. The reason is clear, because
been rejuvenated and enriched by the realization the complex—but well understood—biosynthetic
that oxygen is merely one component in a multifac- pathway by which hydroxyproline is formed
torial geochemical setting. In order to understand involves free oxygen. Simplistically, as life certainly
oxygen levels, one must consider other elements evolved under very low-oxygen conditions, it was
as well, such as sulphur (Shen et al., 2002; Canfield not possible to synthesize hydroxyproline at this
et al., 2007), as well as temperature and salinity time. It was only when oxygen levels had risen to
(Knauth, 2005). Further, oxygen availability is also a certain level that hydroxyproline synthesis was
of importance: oxygen levels in the atmosphere, possible. The strategy for identifying the rise in
deep oceans, and shelves may all have significantly oxygen levels, then, is to identify where hydroxy-
different values (Canfield, 1998; Holland, 2006). proline synthesis evolved in the history of life. To
put it another way, when oxygen levels were lower
than this critical value, hydroxyproline synthesis
1.3.2 Why is oxygen important?
would have been impossible, and thus any clades
Simply put, oxygen plays a critical role in animals that now synthesize hydroxyproline could not
for two reasons. The first is that it is necessary for have existed. As usual, this simple picture needs
certain important biosynthetic pathways; and the some careful qualification. How do we know when
second is that it is used in energy production, i.e. hydroxyproline appeared phylogenetically, and
in aerobic respiration. If it is the limiting factor in could it have arisen more than once? Did hydroxy-
either of these roles, then low oxygen levels might proline synthesis require free oxygen when it first
have impeded animal evolution. These two cases arose? What is the present day phylogenetic distri-
can be called the biosynthetic argument and the bution of hydroxproline?
physiological argument, respectively. It should be noted that hydroxyproline has long
been considered of interest in the debate about
The biosynthetic argument: oxygen as a structural animal origins because of its critical importance
necessity in one of the most important of all animal pro-
The most famous argument for the importance of teins, collagen, although this is not the only bio-
oxygen in animal evolution was put forward by chemical pathway requiring oxygen (Catling et al.,
Towe (1970). It relies on a quirk of the genetic code 2005). Collagen is an unusual protein because it
that has interesting evolutionary consequences. The is made of repeating units of a few amino acids,
genetic code allows the assembly of 20 amino acids including hydroxyproline. The hydroxyproline is
into first polypeptides and then proteins. However, produced in situ by modification of proline after
some important amino acids are synthesized after the basic protein structure has already formed. It
this translation of the code. The classical example seems that this process needs free oxygen levels
is the formation of one of these, hydroxyproline, to be about 1% of present-day atmospheric levels
from the encoded proline (technically proline is an (PAL). The process also requires ascorbic acid (i.e.
imino acid). Lysine is also, on a much smaller scale, vitamin C); collagen defects are the reason behind
12 ANIMAL EVOLUTION

the symptoms of scurvy. Towe’s reasonable argu- and extensin synthesis grew out of a common bio-
ment, therefore was that animals, all of which chemical pathway that also utilized hydroxypro-
produce collagen, could not have evolved before line and hydroxylysine, and that this pathway may
oxygen reached 1% PAL (Towe, 1970). This value, be shared by fungi. A simple survey thus suggests
which can be called the Towe limit, sets an abso- that these multicellular eukaryotes share hydroxy-
lute limit to the conditions in which animals could proline synthesis, and indeed synthesis of a shared
have evolved, and provides the basic mechanism family of structural proteins.
by which animal evolution could have been con- The above suggests that the multicellular
trolled by oxygen. However, although the focus has eukaryotes arose in an environment that allowed
largely been on animals, the scope of this enquiry the hydroxylation of proline and lysine, and was
must be broadened, because animals are not the thus above the Towe limit, a view supported by
only organisms to produce either hydroxyproline modelling of the atmosphere (Canfield, 1998;
or, indeed, collagen. Holland, 2006). More controversially, the ‘fungi
first’ model of eukaryote relationships (Martin
The phylogeny of hydroxyproline and collagen et al., 2003) suggests that hydroxyproline synthesis
synthesis; primitive or convergent? was a basal eukaryotic feature. If true, the import-
Collagen itself has long been thought of as one of ant result would be that there would be no level
the (few) classical synapomorphies that uniquely of atmospheric oxygen that would permit eukary-
unite metazoans (Conway Morris, 1998b). As a otic evolution in general but not animal evolution
result, its discovery in fungi (Celerin et al., 1996) in particular; they share the same requirements.
came as a considerable surprise. The fungal colla- If one is searching for a general mechanism for
gen is considerably different from any of the many delaying animal evolution after the appearance of
types known from animals, and may have arisen eukaryotes then this appears not to be it. On these
by convergence. Nevertheless, this discovery sup- grounds alone, oxygen levels must have been at
plies intriguing evidence for an animal–fungus least 1% of PAL ever since the origin of the eukary-
sister-group relationship, one that has gained otes, which is almost certainly over a billion years
some support in recent years (Wainwright et al., ago (Butterfield et al., 1990).
1993). The exciting discovery of several collagen-
domain-encoding genes in the recently published
1.3.3 Oxygen requirements, size and shape
genome of the choanoflagellate Monosiga brevicollis
(King et al., 2008; cf. Ruiz-Trillo et al., 2008) adds fur- One of the first efforts at relating oxygen levels to
ther critical information for tracing the evolution the rise of animals was made by Nursall (1959), who
of structural proteins that have until recently been argued that large animals, with their concomitant
thought to be metazoan autapomorphies. complex ecologies, were simply not possible in a
Although plants do not synthesize collagen, they low-oxygen environment. Not until oxygen levels
do produce various proteins such as extensins and had risen above a certain level would large ani-
pherophorins that are an important component of mals be able to evolve, especially equidimensional
the cell wall; i.e. they are structural proteins simi- animals such as brachiopods. For many people
lar in function and form to collagen, and are found (Runnegar,1982c; Knoll, 2003; Shen et al., 2008) this
in both the algae and higher plants (Sommer- is the best reason for why the Cambrian explosion
Knudsen et al., 1998; Hallmann, 2006). Further, happened when it did. But does this argument
in such molecules, hydroxyproline and hydroxy- hold water?
lysine are produced in a very similar way as in Most animals are able to generate energy using
collagen—by in situ post-translational modification either aerobic or anaerobic metabolic pathways;
of proline and lysine—and in both animals and with glycolytic anaerobic respiration generating
plants the enzyme prolyl 4-hydroxylase is used for about two ATP molecules, and aerobic respiration
the former. The overall similarity in synthetic path- (citric acid cycle plus oxidative phosphorylation)
way, structure, and function suggests that collagen about 36. Although the citric acid cycle does not
 E ARLIEST FOSSIL RECORD OF THE ANIMAL S 13

directly rely on free oxygen, it does not take place the same amount of oxygen; as might be expected,
under anaerobic conditions. As there is no free oxy- mode of life is a critical variable too. Organisms
gen to act as the final electron acceptor, the inter- that swim generally need more oxygen than those
mediates all along the oxidative phyosphorylation that walk, dig, or just open their valves. Floating
chain remain in a reduced state. As a result, the in the water column requires least energy of all,
chain stops functioning; and the build up of end of course (Pörtner, 2002). For some of the more
products means (via Le Chatelier’s principle) that ‘athletic’ extant organisms, such as squid, it seems
the citric acid cycle halts. However, glycolysis can that swimming takes place close to their func-
still occur, leading to a build-up of pyruvate and a tional and environmental limits. They manage to
small amount of ATP (two or three molecules). achieve this ‘life on the edge’ by living in a very
So much for the basic biochemistry, the broad out- stable environment, i.e. the open ocean. Although
line of which is extremely well known. What is less they use both aerobic and anaerobic respiratory
well known, however, is the presence of a variety pathways, they maximize aerobic respiration and
of anaerobic respiratory pathways in metazoans. eventually tire during anaerobic activity, as levels
Some metazoans, for example, are able to ferment of free ATP drop.
as well as produce lactic acid (from glycolysis) or For other organisms, though, a very different pic-
opines, formed by condensing pyruvic acid with ture emerges. Sipunculans, for example, that typic-
an amino acid. Simply because the yield of ATP ally spend their time slowly digging in low-oxygen
from glycolysis is so low, some invertebrates also mud, produce identical metabolites whether they
have pathways that avoid glycolysis. For example, work under oxygen-rich conditions or artificially
some invertebrates use a fumarate electron trans- induced oxygen-deficient ones, suggesting, with
port system that increases the yield of ATP to other evidence, that almost all muscular activity of
up to eight molecules (Fenchel and Finlay, 1995; any significance takes place anaerobically (Pörtner,
McMullin et al., 2000; Tielens et al., 2002), includ- 2002). In other words, low oxygen levels hardly
ing some parasites such as the nematode Ascaris, affect such organisms because almost everything
but also free-living invertebrates such as the mus- they do requires them to switch to anaerobic res-
sels Mytilus and Geukensia and the polychaete piration in any case. Only resting respiration is
Arenicola. Whilst most of the sources of electrons performed aerobically, i.e. mitochondria are fuelled
in these various anaerobic pathways are organic, by oxygen when the organism is not actually doing
it is also now known that these invertebrates can anything. As might be expected, such organisms
switch to sulphide oxidation in hypoxic conditions, have an extreme tolerance to anaerobic respiration,
a presumed remnant of eukaryotic diversification and do not seem to tire while performing their con-
in a high-sulphide Proterozoic ocean (Theissen stant but low-energy functions. Such modes of life
et al., 2003; contra Anbar and Knoll, 2002). Thus, may provide important clues to how early animal
respiratory mechanisms, and the mitochondria life functioned in the early Cambrian.
that generate them, are surprisingly diverse: as Despite the arguments above, a powerful case
they do not fall into obvious well-defined clades, it has recently been put forward that high oxygen
is likely that they have been convergently derived levels are indeed necessary to sustain a complex
(Tielens et al., 2002). ecology, based partly on the ability of organisms
The presence of diverse, mitochondrial based to produce a large body size and generate enough
anaerobic respiratory pathways, even in meta- energy to sustain complex food chains (Catling
zoans, is significant because it suggests that at et al., 2005). While their calculations do not seem
least some metazoans can (and could have) func- to take into account the possibility of fumarate-
tion well even under low-oxygen conditions, pro- based anaerobic pathways that would generate
ducing more energy than from mere glycolysis, more ATP than glycolysis, their points must be
thus somewhat undermining the claim that ris- well taken, especially given the demonstrable
ing oxygen levels were a pre-requisite for animal effect on body size and mineralization that low-
evolution. Furthermore, not all organisms require oxygen environments have on organisms today
14 ANIMAL EVOLUTION

(Rhoads and Morse, 1971). However, to return to misleading to identify these milestones as stand-
the two questions asked at the beginning of the alone ‘key innovations’, embedded as they are in
section, the real question is not whether or not, for a nexus of other morphological and ecological
example, hard parts could be formed under low- changes (e.g. Budd, 1998). Thus although the
oxygen conditions, but rather if any sort of animals undoubtedly important suite of geological changes
could evolve in such a regime that would gener- that took place during the close of the Proterozoic
ate a fossil record? Given that minute trace fossils and opening of the Phanerozoic form the essential
and indeed body fossils, as in the Doushantuo Fm, backdrop against which the Cambrian explosion
can be preserved in the record, it seems that the must be viewed, it still seems reasonable to regard
answer must be yes. them as scenery rather than the major players in
Although animals can obviously persist in, and the Cambrian drama.
have distinctive adaptations for, low-oxygen envir-
onments, there can similarly be little doubt that
1.4 Conclusions
high oxygen levels (perhaps 10% PAL) are really
necessary for modern food chains and large ani- Although the dating of the early animal fossils
mals to flourish. Determining when this level remains problematic, a reasonable case for stem-
was first permanently achieved in the atmosphere group animals existing shortly after the Marinoan
must remain an important goal for studies of the glaciation at around 630 Ma can be made.
late Precambrian and the influence of environment Nevertheless, evidence for mobile bilaterians does
on animal evolution. Thus there are considerable not appear in the record until around 555 Ma, just
uncertainties about Proterozoic oxygen levels and before the beginning of the Cambrian; a time that
the physiological requirements of early animals; is no longer wildly inconsistent with some molecu-
after all, recent animals living in low-oxygen lar clock estimates (e.g. Aris-Brosou and Yang,
environments usually possess distinct adaptations 2003; Peterson et al.
that it would be reasonable to suppose were also
possessed by early animals. As a result, the current
1.5 Acknowledgements
fashion for rising oxygen levels being the primary
engine for the Cambrian explosion may not be as Discussions with many colleagues including Simon
well founded as is sometimes assumed. A perfectly Conway Morris, Nick Butterfield, Sören Jensen, and
reasonable alternative is that the Cambrian explo- Sebastian Willman are gratefully acknowledged,
sion is an ecological event (Butterfield, 1997; Budd as are the providers of images as detailed in the
and Jensen, 2000; Marshall, 2006), consisting largely figure captions. This work was supported by the
of a cascade of knock-on effects that emerged from Swedish Research Council (VR) and the Swedish
multicellularity and mobility; although it would be Royal Academy of Sciences (KVA).
 CHAPTER 2

The Ediacaran emergence of

bilaterians: congruence between
the genetic and the geological
fossil records
Kevin J. Peterson, James A. Cotton, James G. Gehling, and
Davide Pisani

Unravelling the timing of the metazoan radiation (Darwin, 1859), it has long been argued that this
is crucial for elucidating the macroevolutionary same geological record, because of its incom-
processes associated with the Cambrian explosion. pleteness, might be misleading when considering
Because estimates of metazoan divergence times metazoan origins (Runnegar, 1982b). As Runnegar
derived from molecular clocks range from quite recognized, a second ‘fossil record’, the genetic
shallow (Ediacaran) to very deep (Mesoproterozoic), record written in the DNA of all living organisms
it has been difficult to ascertain whether there (Runnegar, 1986), could be used to test hypotheses
is concordance or quite dramatic discordance about the completeness of the geological record
between the genetic and geological fossil records. (Peterson et al., 2007), and initial attempts at using
Here, using a range of molecular clock methods, a molecular clock strongly suggested that meta-
we show that the major pulse of metazoan diver- zoans had a deep and cryptic Precambrian history
gence times was during the Ediacaran, consistent (Runnegar, 1982a, 1986; Wray et al., 1996; reviewed
with a synoptic reading of the Ediacaran macro- recently by Conway Morris, 2006). Nonetheless,
biota. These estimates are robust to changes in pri- several palaeontologists have cogently argued
ors, and are returned with or without the inclusion that the fossil record provides positive evidence
of a palaeontologically derived maximal calibra- for the absence of early Neoproterozoic and
tion point. The two historical records of life both Mesoproterozoic animals, casting doubt on the
suggest, therefore, that although the cradle of the veracity of these molecular clock estimates (Budd
Metazoa lies in the Cryogenian, and despite the and Jensen, 2000, 2003; Jensen et al., 2005; Conway
explosion of ecology that occurs in the Cambrian, it Morris, 2006; Butterfield, 2007). Comparisons
is the emergence of bilaterian taxa in the Ediacaran between the genetic and geological fossil records
that sets the tempo and mode of macroevolution of early animal evolution, as currently understood,
for the remainder of geological time. therefore suggest that either the geological record
is woefully incomplete or there is something ser-
iously awry with our reading of the genetic record
2.1 Introduction
(Bromham, 2006).
Accurately and precisely elucidating the times of To explore the apparent incongruity between the
origin of the metazoan phyla is central to unrav- known fossil record and the very deep estimates
elling the causality and biological significance of metazoan diversification suggested by molecu-
of the Cambrian explosion. Despite the fact that lar clocks, Peterson and colleagues (Peterson et al.,
the Cambrian explosion is geologically obvious 2004; Peterson and Butterfield, 2005) assembled the

15
16 ANIMAL EVOLUTION

largest novel data set yet, showing that the two maximum proposes an absolute value for the oldest
records were remarkably concordant: metazoans possible date of divergence, whereas a ‘soft’ max-
originated at some time during the Cryogenian, imum treats a divergence as having some chance
and bilaterians arose during the Ediacaran. Part of being older than a particular date, depending on
of the reason for the prior discrepancy concerned a probability distribution used to describe the cali-
the use of vertebrate divergence times. Peterson bration point (Hedges and Kumar, 2004; Yang and
et al. (2004) discovered that there was an approxi- Rannala, 2006; Benton and Donoghue, 2007).
mately two-fold rate reduction across the verte- Most modern molecular clock methods (e.g.
brate protein-coding genome as compared with Sanderson, 1997, 2002; Thorne et al., 1998; Drummond
the three invertebrate lineages examined (echino- et al., 2006) allow one to constrain, as well as fix,
derms, molluscs, and insects), consistent with total the age of a calibration point, so that every fossil
genome comparisons between vertebrates and dip- divergence can be defined using a minimum and a
teran insects (Zdobnov et al., 2002). However, some maximum. This is a significant improvement over
studies using invertebrate calibrations have also older molecular clock approaches (e.g. Kumar and
inferred divergence times consistent with a cryp- Hedges, 1998) because it allows the integration of
tic Precambrian history of the Metazoa (Pisani palaeontological uncertainty in the estimation of
et al., 2004; Regier et al., 2005), suggesting that the divergence times. However, most existing molecu-
two-fold rate reduction across the vertebrate gen- lar clock software including r8s (Sanderson, 2004)
ome is only one of many factors influencing the and Multidivtime (Thorne and Kishino, 2002), do
estimation of divergence times (Linder et al., 2005; not distinguish between hard and soft maxima,
Peterson and Butterfield, 2005). instead treating all maxima as hard. The difficulty
In addition, Peterson et al.’s (2004) estimates and here is that divergence times estimated with uncer-
explanations were called into question by several tain maxima treated as if they were hard can only
workers, notably Blair and Hedges (2005) who give minimum estimates for the true divergence
argued that Peterson et al. (2004) used palaeon- time, as the soft maxima might significantly under-
tologically derived calibration points as maxima estimate the true age of the calibration points.
as opposed to minima, which generated spuri- Nonetheless, Drummond et al. (2006) have now
ously shallow estimates for metazoan divergences. implemented Bayesian relaxed molecular clock
Although false, as Peterson et al. (2004) stated methods (in the software package BEAST) where
explicitly (see also Peterson and Butterfield, 2005), soft maxima can be properly modelled using a
this criticism highlights an important issue sur- probability distribution, and can thus be older than
rounding the use of molecular clocks, namely the their proposed fossil date.
proper way to incorporate calibration points into Here, we set out to explore the diversification of
molecular clock analyses (Benton and Donoghue, animal phyla in the Neoproterozoic using alter-
2007). Recent experimental analyses have shown native relaxed molecular clock approaches while
the importance of numerous, well-constrained testing the stability of our results to the choice of
calibration points for returning accurate and pre- different priors and to the deletion of palaeontolog-
cise estimates of divergence times, and thus high- ically derived maxima, and modelling soft maxima
lighting the need to pay particular attention to this using the most appropriate probability distribu-
aspect of molecular dating (Roger and Hug, 2006; tion. We find that although deleting or relaxing
Hug and Roger, 2007). Nonetheless, difficulties maxima tends to push divergence times toward the
arise when incorporating fossils into a molecu- past (as expected), all estimates are largely congru-
lar clock analysis: unlike the establishment of a ent between algorithms. We conclude that a synop-
minimal divergence time for any two taxa, which tic reading of both the geological and genetic fossil
is simply the first appearance of either one of the records demonstrates that the Ediacaran was the
taxa, estimating the maximum divergence time is time of major diversification of most higher-level
much more difficult (Benton and Donoghue, 2007). animal taxa and set the stage for Phanerozoic-like
Two types of maxima have been proposed: a ‘hard’ macroecology and macroevolution.
 T H E ED I AC A R A N EM ERG EN CE O F B I L AT ER I A NS 17

2.2 Materials and methods demosponges is the first appearance of demos-

ponge-specific biomarkers (McCaffrey et al., 1994;
2.2.1 Molecular characters Love et al., 2006; see Peterson et al., 2007 for dis-
All taxa are taken from Sperling et al., (2007) where cussion) sometime after the Sturtian, c. 657 Ma
a concatenated alignment of seven different house- (Kendall et al., 2006). Finally, the maximum for the
keeping genes, for a total of 2059 amino acid pos- origin of crown-group Eumetazoa, which was only
itions and 44 representative species (see Peterson used in the BEAST analyses, is argued to be 635 Ma
et al., 2004, and Peterson and Butterfield, 2005), was based on palaeoecological observations (Peterson
analysed using Bayesian methods (MrBayes 3.1.2; and Butterfield, 2005).
Ronquist and Huelsenbeck, 2003). See Sperling Newly incorporated minima include the first
et al., (2007) for further details. appearance of arthropod traces 525 Ma (Budd
and Jensen, 2003) as a minimum for the diver-
gence between insects and the priapulids, the first
2.2.2 Molecular clock calibration appearance of medusozoans 500 Ma (Hagadorn
et al., 2002) as a minimum for the origin of the
Calibration points were taken from Peterson et al.,
crown-group Cnidaria, and the first appearance of
(2004) except for the minimum estimate for crown-
vertebrates 520 Ma as the minimum for the origin
group Eleutherozoa, which was adjusted from 475
of crown-group chordates (Benton and Donoghue,
to 480 million years ago (Ma) in light of the dis-
2007).
covery of a slightly older asterozoan (Blake and
Guensberg, 2005), and the minimum and max-
imum for crown-group Diptera was taken from 2.2.3 Molecular estimates of divergence times
Benton and Donoghue (2007). Several new maxima
Molecular estimates of divergence times were
and minima were incorporated into this analysis.
obtained using the Bayesian methods of Thorne
First, the maximum for the origin of crown-group
et al., (1998), as implemented in Multidivtime
echinoderms was set at 520 Ma, the first appear-
(Thorne and Kishino, 2002), and Drummond
ance of stereom in the fossil record. Because ster-
et al., (2006) as implemented in BEAST version
eom is a highly distinctive skeletal material, and
1.4.2 (Drummond and Rambaut, 2006). All diver-
its presence in numerous stem-group taxa (Smith,
gence times were calculated assuming the tree
2005) demonstrates that stereom is a total-group
topology of Figure 2.1, which was derived from
echinoderm character, it must have evolved before
MrBayes (see above and Sperling et al., 2007). For
the origin of the crown group. Second, this same
the Multidivtime analyses, branch lengths were
time point also sets the minimum for Ambulacraria
estimated using the Estbranches program from
(Echinodermata + Hemichordata), as echinoderms
the Multidivtime package, under the WAG model.
appear before hemichordates in the rock record
For BEAST analyses, starting branch lengths
(Budd and Jensen, 2003). Third, because ambulac-
were assigned arbitrarily to match the constraints
rarians are characterized by the possession of four
imposed by the calibrations.
to six coeloms in each animal (Peterson et al., 2000;
For the Multidivtime analyses a prior age for the
Smith et al., 2004), and because coeloms cannot
root node (in our case the Fungi–Metazoa split)
pre-date the first appearance of bilaterian traces
must be specified. We assumed a 1000 Ma prior
(Budd and Jensen, 2000, 2003), the first appearance
for this node (Knoll, 1992; Douzery et al., 2004)
of traces sets the maximum age for crown-group
and then tested whether this choice affected our
Ambulacraria at approximately 555 Ma (Martin
results by performing analyses in which this age
et al., 2000; Jensen et al., 2005). Fourth, the max-
was changed to 100 Ma (standard deviation (SD) =
imum for the origin of Gastropoda + Bivalvia is
500 Ma), 1500 Ma (SD = 500 Ma), and 2000 Ma (SD
the first appearance of skeletons in the fossil record,
= 750 Ma). Other priors used in Multidivtime ana-
about 542 Ma (Amthor et al., 2003; Bengtson, 1994).
lyses include the mean and standard deviation of
Fifth, the maximum for the origin of crown-group
the prior distribution at the root node, and ‘Minab’
18 ANIMAL EVOLUTION

Cryogenian
Ediacaran
Cambrian

1100 1000 900 800 700 600 500 400 300 200 100 0

73 Ciona
Branchiostoma
100 Dendraster
31 100
Encope
98
100
Eucidaris D
Asteria
100
Antedon
100 Saccoglossus
Ptychodera
100 M. edulis
100 M. californianus
82
68 Modiolus
100 Nucula
100 Haliotis
100 Crepidula
100 Capitella S
100 Nereis
100
Chaetopterus
100 Amphiporus
100 Lineus
82
Cerebratulus
69
Stylochus
99 100 Lestes
100 Enallagma
100 100 100 Drosophila E
Anopheles
Priapulus
99 59 Obelia
100 Metridium C
Nematostella
Oscarella O
100
100 Scypha
Leucosolenia
100 Microciona
100 Suberites
65 Halichondria
100 Ephydatia Sp
100 Trochospongilla
100
Amphimedon
100 Chondrilla
100 Darwinella
Dysidea
Saccharomyces

1100 1000 900 800 700 600 500 400 300 200 100 0

Figure 2.1 The timing of the metazoan radiation according to the molecular clock. The figure shows the phylogenetic tree for 41 metazoan
taxa rooted on the yeast Saccharomyces cerevisiae as determined by Bayesian phylogenetic analysis (see text). The deuterostomes are shown
in box D, spiralian protostomes in box S, ecdysozoan protostomes in box E, cnidarians in box C, the homoscleromorph Oscarella in box O,
calcisponges in box C, and demosponges in box Sp. The nodes of the tree are positioned according to the optimum as determined from the
Bayesian autocorrelated method of Thorne et al. (1998), as implemented in the software package Multidivtime (Thorne and Kishino, 2002)
using a root prior of 1000 Ma (SD 500 Ma). The 95% highest-probability-density (HPD) credibility intervals are shown in brackets. The white
circles are the estimates for clades with internal calibration points as determined by the Bayesian algorithm BEAST (Drummond et al., 2006)
using uniform priors and an exponential rate distribution. Black Xs are the estimates using exponential priors and the same rate distribution.
Note that much of the metazoan diversification occurs during the Ediacaran, which lies between the Cryogenian and the Cambrian.

(parameter for the beta prior on proportional node parameter had on the results were assessed. The
depth). The mean and standard deviation of the Minab parameter affects the distribution of the
prior distribution of the rate at the root node were nodes through time—Minab values greater than 1
set to 0.039, as estimated from the data following will cause the nodes to repel each other, while
the procedure outlined in the Multidivtime man- values less than 1 will cause the nodes to attract
ual, and the effects that 100-fold changes to this each other. This parameter was set to 1 for our
 T H E ED I AC A R A N EM ERG EN CE O F B I L AT ER I A NS 19

analyses, but we assessed how changing the Minab example, all but one node (Stylochus + Nemertea)
parameter from 0.6 to 1.4 affected our results. have posterior probability values above 80%, and
BEAST implements uncorrelated relaxed clock both Lophotrochozoa and Ecdysozoa, as well as
methods, which assume an overall distribution of Annelida + Mollusca, have clade credibility values
rates across branches but do not assume that the of 100%. In addition, we find strong support for the
rates on adjacent branches are autocorrelated. We node Homoscleromorpha + Eumetazoa, which
used both the exponential and lognormal rate dis- indicates that there are at least three independent
tributions with two different calibration schemes: extant sponge lineages (Sperling et al., 2007).
one with hard maxima, in which most calibrations Using this topology as a constraint tree, diver-
were treated as uniform priors on clade ages, and a gence times were estimated using the Bayesian
second with only soft maxima, in which all calibra- autocorrelated method of Thorne et al. (1998), as
tions were treated as exponential priors, with 95% of implemented in the software package Multidivtime
their density lying between the uniform maximum (Thorne and Kishino, 2002). These Bayesian esti-
and minimum. In both schemes, the maximum at mates are robust to changes in the age of the root
635 Ma was treated as an exponential prior, with prior as the estimates are essentially the same
90% of its density lying below 635 Ma, giving a 10% whether the age is 100 Ma (SD 500 Ma) or 2000
prior chance that this calibration point is incorrect. Ma (SD 750 Ma) (Table 2.1), suggesting that the age
All other priors and operators were kept at default of the root prior is not biasing the analyses. Also,
settings, except that all operators that alter the tree changing the value of Minab, or the mean rate
topology were disabled. of evolution of the root node, did not change our
Ninety-five per cent highest-probability-density results (not shown). Running the analyses without
(HPD) credibility intervals are automatically calcu- data confirmed that our results were not domi-
lated by Multidivtime, and were calculated using nated by our choice of priors (not shown). Because
the program Tracer for the BEAST analyses. To test of the suggestion that fungi diverged from animals
whether our priors dominated the posterior distri- c. 1000 Ma (Knoll, 1992; Douzery et al., 2004), was
bution, all our BEAST and Multidivtime analyses confirmed by all our analyses that did not assume
were also performed without data and the results a particular age for the root node, and in our
obtained in these runs were compared with those Bayesian analyses performed assuming different
obtained when the actual data were analysed. prior root ages (100, 1500, and 2000 Ma) we used
the values derived from the 1000 Ma (SD = 500 Ma)
2.3 Results prior in Figure 2.1.
The removal of the deeper calibration point,
Molecular divergence times were estimated namely the maximum age of 657 Ma for the ori-
using the topology shown in Figure 2.1. Support gin of crown-group demosponges, resulted in
for Cnidaria and Deuterostomia was low (67% increasing the estimate for the age of crown-group
and 33%, respectively), probably because of long- Metazoa by c. 18% (from 766 Ma to 904 Ma; Table 2.1).
branch artefacts (Pisani, 2004) associated with Nonetheless, the age for both crown-group
Ciona and Obelia in particular (indeed the value for Protostomia and crown-group Deuterostomia
Deuterostomia goes to > 90% with the removal of increased by only c. 4–5%, suggesting that the
Ciona), but given the clear monophyly of the phyla results derived with the use of this maximum are
Chordata and Cnidaria, constraining these nodes generally robust. Given its position in the tree, the
should not generate spurious molecular divergence geological depth of the divergence, and the unique
estimates. Most of the other nodes were strongly nature of the evidence (biomarkers), this maximum
supported, including Calcispongia + Eumetazoa, is most likely adding both accuracy and precision
and Eumetazoa, supporting the results of Peterson to the clock estimates.
and Butterfield (2005), and contra the conclusions We next explored these same divergence
of Rokas and colleagues (Rokas et al., 2005; see also times using the models implemented in BEAST
Baurain et al., 2007). Indeed, within Protostomia, for (Drummond et al., 2006). In general, the estimates
20 ANIMAL EVOLUTION

Table 2.1 Optima (maxima, minima) in millions of years derived from Multidivtime (M) and BEAST (B) analyses for five key metazoan
divergences

Method Metazoa Eumetazoa Bilateria Protostomia Deuterostomia

M-10001 766 (803, 731) 676 (709, 645) 643 (671, 617) 619 (648, 594) 601 (625, 579)
M-1002 760 (798, 725) 672 (706, 642) 641 (669, 615) 618 (645, 592) 600 (624, 578)
M-20003 774 (812, 739) 679 (712, 648) 645 (674, 619) 622 (649, 595) 602 (626, 580)
M-1000-D4 904 (997, 825) 743 (798, 694) 686 (727, 649) 653 (689, 619) 624 (655, 596)
B-UCEX Uniform5 815 (1621, 625) 676 (849, 579) 652 (764, 570) 620 (692, 556) 572 (614, 537)
B-UCEX Exp6 1067 (2358, 612) 707 (985, 581) 669 (870, 566) 638 (784, 556) 582 (695, 529)
B-UCLN Uniform7 891 (995, 640) 739 (822, 607) 699 (768, 588) 660 (715, 572) 640 (706, 559)
B-UCLN Exp8 953 (1093, 821) 779 (869, 694) 733 (808, 663) 688 (751, 629) 677 (746, 607)

1
Age of the root prior is 1000 Ma (SD 500 Ma).
2
Age of the root prior is 100 Ma (SD 500 Ma).
3
Age of the root prior is 2000 Ma (SD 750 Ma).
4
Age of the root prior is 1000 Ma (SD 500 Ma) and estimates are derived without considering the demosponge maximum of 657 Ma.
5
Estimates derived using an exponential rate distribution and uniform priors.
6
Estimates derived using an exponential rate distribution and exponential priors.
7
Estimates derived using a lognormal rate distribution and uniform priors.
8
Estimates derived using a lognormal rate distribution and exponential priors.

derived from BEAST using an exponential rate do these molecular estimates compare with the
distribution and uniform priors (white circles known geological record? Macroscopic fossils
in Figure 2.1) are similar to those derived from of the Ediacara biota span the upper half of the
Multidivtime (Table 2.1). The analyses that use Ediacaran Period, from 575–542 Ma (Grotzinger
exponential priors are somewhat deeper than those et al., 1995; Martin et al., 2000; Bowring et al., 2003;
that use uniform priors (black Xs in Figure 2.1), Condon et al., 2005). Because most of these fos-
and those using a lognormal rate distribution are sils occur as soft-bodied impressions in relatively
deeper than those derived from an exponential coarse-grained siliciclastic sedimentary rocks, a
rate distribution (Table 2.1), presumably because comprehensive array of palaeobiological inter-
the exponential distribution on rates is leading to pretations of the Ediacara biota has been put
greater autocorrelation between rates. Analyses forth. Nonetheless, a few taxa stand out as poten-
without data again confirmed that the priors were tial candidates for affinities within the Metazoa.
not dominating the data (results not shown). One taxon in particular, Kimberella, has generated
much discussion as a possible triploblastic meta-
zoan. It compares well in external form to mol-
2.4 Discussion
luscs (Fedonkin and Waggoner, 1997) and in a few
2.4.1 Concordance between the genetic and cases an everted proboscis is preserved (Gehling
geological fossil records et al., 2005) that is inferred to contain a radula-like
organ given the association between specimens of
Here we have shown, using a variety of analyses
Kimberella (Figure 2.2a, asterisk, and Plate 1) and
and appropriately testing for biases that may have
aligned sets of paired scratch marks (Figure 2.2a,
been introduced by the use of palaeontologically
arrows) (Gehling et al., 2005). These finds sug-
derived maxima, that the genetic fossil record
gest that Kimberella was preserved in place while
strongly supports the notion that the diversificat-
grazing on substrate microbial mats (Seilacher,
ion of metazoans in general, and bilaterian meta-
1999; Gehling et al., 2005). Given that we estimated
zoans in particular, occurred during the Ediacaran
the divergence between annelids and molluscs to
Period, 635–542 Ma (Knoll et al., 2004, 2006). How
 T H E ED I AC A R A N EM ERG EN CE O F B I L AT ER I A NS 21

(a) (e)

(d)

(b) (c)

Figure 2.2 Putative ediacaran metazoans: (a) natural cast on bed base of Kimberella resting trace (asterisk) and Radulichnus radular
feeding trace fans (arrows) (scale bar 1 cm); (b) Dickinsonia costata (scale bar 2 cm); (c) Marywadea ovata (scale bar 10 mm); (d) Spriggina
floundersi (scale bar 10 mm); (e) Parvancorina minchami (scale bar 1 cm). See also Plate 1.

be c. 570 Ma (Figure 2.1), it is possible, if not prob- Skania (Lin et al., 2006). Spriggina (Figure 2.2c) also
able, that Kimberella is allied somehow with mod- preserves large numbers of appendage-like struc-
ern molluscs. tures, and still others like Marywadea (Figure 2.2d)
What about other higher-level clades? Our esti- show apparent cephalic branching structures
mates suggest that arthropods diverged from that resemble digestive caecae in arthropods.
priapulids c. 575 Ma, suggesting that stem-group Importantly (see below), all of these taxa were
panarthropods (Nielsen 2001) should be present in no larger than 10 cm in maximum dimension
Upper Ediacaran rocks. Interestingly, several taxa (Gehling, 1999; Fedonkin, 2003) (see Figure 2.2), and
compare favourably with a panarthropod interpret- appear simultaneously with the first demonstrable
ation. For example, large specimens of Parvancorina trace fossils (Jensen et al., 2005). The absence of
show lateral structures originating on either side arthropod scratch marks (Seilacher, 1999), though,
of the medial ridge that might be characterised as is not too worrisome given that such traces would
appendages (Figure 2.2b). In fact, in external form, demand the presence of sclerotized appendages
Parvancorina bears a striking resemblance to the to cut through the ubiquitously present microbial
unmineralized, kite-shaped Cambrian arthropod mats, a character not necessitated by the presence
22 ANIMAL EVOLUTION

of stem-group panarthropods, or even deeply analyses, which is supported by the fact that their
nested stem-group arthropods, in Ediacaran-aged estimate for the origin of a mineralized, coelom-
sediments. ate taxon like crown-group Echinodermata pre-
Indeed, the distinct possibility remains that cedes their appearance in the fossil record by some
this fauna preserves numerous stem-group forms 200 million years.
ranging from basal triploblasts up through basal Of course, neither the genetic nor the geological
ecdysozoans, spiralians, and possibly even deu- fossil record has a monopoly on historical accur-
terostomes. Given the enigmatic nature of some acy, and as much as molecular evolutionists need
very prominent taxa like Dickinsonia (Figure 2.2e), to keep in mind the relevant palaeontological data,
a taxon that appears capable of some form of lim- palaeontologists need to keep in mind estimates
ited motility (Gehling et al., 2005), a position for derived from molecular clocks (Donoghue and
Dickinsonia within total-group Eumetazoa is not Benton, 2007). For example, Budd and Jensen (2000,
out of the question. In fact, mobile but saprophytic 2003) argued that bilaterians could not have had
feeding without the use of a gut would be com- an extensive Precambrian history, as suggested
pelling evidence that some form of ectomesoderm by almost all molecular clocks, as the trace fossil
pre-dates the advent of endoderm. record, and the inferred morphology of these ani-
mals, is not consistent with an origin much before
555 Ma. They observed that possession of coelom(s)
2.4.2 Discordance between the genetic and
and a blood-vascular system (BVS) are inconsist-
geological fossil records
ent with a meiofaunal origin, as tiny organisms
Of course, many others have addressed these ques- would have had no need for a transport system like
tions using a similar approach, and it is worth com- the BVS, and are only consistent with a size large
paring our results not only against the fossil record enough to be detected in the geological record. In
but also with other molecular clock estimates as general, we agree with their arguments, and use
well. They compares well with some molecular ana- their insights to set a maximum age for crown-
lyses, notably Aris-Brosou and Yang (2002, 2003), group Ambulacraria (see above).
Peterson et al. (2004), and Peterson and Butterfield However, the same argument cannot be
(2005), all of whom argued that the last com- extended to many other parts of the bilaterian
mon ancestor of protostomes and deuterostomes tree. Contra Budd and Jensen (2000), there is no
evolved not more than 635 Ma. However, Blair evidence for homology of coeloms either between
and Hedges (2005) have recently argued for much protostomes and deuterostomes or even within
deeper divergences, based on a series of penal- both protostomes and deuterostomes. Because
ized likelihood (Sanderson, 2002) analyses using the coelom is, by defi nition, just a mesodermally
r8s (Sanderson, 2004) in which every calibration lined cavity (Ruppert, 1991a; Nielsen, 2001) the
point was treated as a minimum. They suggested possession of the space itself cannot be used
that the divergence between ambulacrarian and as an argument for homology. Instead, topo-
chordate deuterostomes was 896 Ma (with the 95% logical similarity must be used, and when it is, it
confidence interval spanning from 832 to 1022 Ma). strongly suggests homology, for example, within
They further argued that the divergence between Ambulacraria (Peterson et al., 2000; Smith et al.,
hemichordates and echinoderms was 876 Ma (725, 2004), but not homology between any other higher
1074 Ma), and the origin of crown-group echino- taxa (Nielsen, 2001; Ruppert, 1991a). Thus, outside
derms was 730 Ma. Finally, they estimated that the of Ambulacraria, the trace fossil record cannot be
divergence between starfish and sea urchins was used to set a maximum for most bilaterian diver-
580 Ma. Unfortunately, their results are most likely gences. In fact, the small size of many putative
spurious because, as Sanderson (2004) pointed out, Ediacaran bilaterians (Figure 2.2), and the fact
r8s cannot converge on a unique solution if only that acoel flatworms are now recognized as the
minima are used to calibrate penalized likelihood sister group to the remaining bilaterians (Baguñà
 T H E ED I AC A R A N EM ERG EN CE O F B I L AT ER I A NS 23

and Riutort, 2004; Peterson et al., 2005; Sempere 2.5 Conclusions

et al., 2007), is consistent with an argument that
small size and absence of a coelom are primitive Both the genetic and geological fossil records, each
for Bilateria. This then removes the fi nal obstacle with their own inherent biases and artefacts, are
to a pre-555 Ma origin for Bilateria, which is con- largely congruent with one another, and for his-
sistent with both the appearance of many differ- torical disciplines congruence of independent data
ent bilaterian lineages in the Ediacaran (Figure sets is the strongest argument one can make for
2.2) and the molecular clock (Figure 2.1). historical accuracy (Pisani et al., 2007). Our ana-
But despite the presence of many different lyses suggest that while the cradle of metazoan life
stem-group taxa, the Ediacaran is still a transi- occurred in the Cryogenian, and the explosion of
tional ecology, with these organisms confi ned to metazoan ecology occurred in the Cambrian, it is
a two-dimensional mat-world. This stands in dra- the emergence of bilaterians in the Ediacaran that
matic contrast to the Early Cambrian where the established the ecological and evolutionary rules
multitiered food webs that typify the Phanerozoic that have largely governed earth’s macrobiota for
were established with the eumetazoan invasion the remainder of geological time.
of both the pelagos and the infaunal benthos
(Butterfield, 1997, 2001; Vannier and Chen, 2000, 2.6 Acknowledgements
2005; Dzik, 2005; Peterson et al., 2005; Vannier
et al., 2007). Hence, although the Ediacaran is an KJP was supported by the National Science
apparent quantum leap in ecological complexity Foundation; JAC was supported by an Irish Research
as compared with the ‘boring billions’ that char- Council for Science, Engineering and Technology
acterize earth before the Ediacaran, it is still rela- Post-doctoral Fellowship; JGG is supported by the
tively simple when compared with the Cambrian. Australian Research Council Discovery Project
The Cambrian was yet another quantum leap in (DG0453393), the ARC Linkage Project LP0774959
organismal and ecological evolution, and which including the South Australian Museum and Beach
thus stands as the transition interval between the Petroleum Pty Ltd, and the SA Museum Waterhouse
‘Precambrian’ and the Phanerozoic (Butterfield, Club. We would like to thank P. Donoghue
2007). Whether it was triggered by the introduc- (University of Bristol) for his usual perspicacity,
tion of eumetazoans, as argued by Peterson and two anonymous reviewers for their helpful com-
Butterfield (2005), by the introduction of mobile, ments on an earlier version of this chapter, and T.
macrophagous triploblasts, as is suggested by our Littlewood (Natural History Museum, London) and
analyses reported here (Figure 2.1), or by some M. Telford (University College London) for inviting
other factor or combination of factors, remains to us to contribute to this volume. Finally, KJP would
be more fully studied through continued explor- like to thank all of the students who have come
ation of the relevant rock sections throughout the through the lab and contributed data to this pro-
world, and continued improvements in molecular ject, and the South Australian Museum for a very
clock methods. enlightening visit.
 CHAPTER 3

Genomic, phylogenetic, and cell

biological insights into metazoan
origins
Scott A. Nichols, Mark J. Dayel, and Nicole King

Over 600 million years ago (Ma), the first Metazoan origins required at least two innov-
multicellular metazoans evolved from their single- ations: the evolution of simple colonies of equipotent
celled ancestors. Although not recorded in the fos- cells followed by the organization and integration
sil record, the earliest events in metazoan evolution of cell function and behaviour within an ‘individ-
can be inferred by integrating findings from phylo- ualized’ organism (Pfeiffer and Bonhoeffer, 2003;
genetics, genomics, and cell biology. Comparisons King, 2004; Michod, 2007). Both of these phenom-
of choanoflagellates (microeukaryote relatives ena required regulated cell signalling, adhesion,
of metazoans) with sponges (the earliest known and differentiation mechanisms, the origins of
metazoans) reveal genetic innovations associated which directly address fundamental questions
with metazoan origins. Among these are the evolu- about the evolution of multicellularity.
tion of the gene families required for cell adhesion Metazoan multicellularity evolved independ-
and cell signalling, the presence of which catalysed ently from that of all other macroscopic lineages.
the evolution of multicellularity and the functions In fact, although unicellular life predominates in
of which have since been elaborated to regulate all considerations of total biomass and biodiversity,
cell differentiation, developmental patterning, at least 16 separate transitions to multicellularity
morphogenesis, and the functional integration of have occurred during the history of eukaryotic life
tissues. The most ancient tissues—differentiated (King, 2004). The imprint of these separate origins
epithelia—are found in sponges and evolved before can be seen at the level of phylogenetics, compara-
the origin and diversification of modern phyla. tive genomics, and comparative cell biology. In
the following discussion, we review how insights
from choanoflagellates and sponges have begun to
3.1 Introduction
illuminate some of the earliest events in metazoan
Metazoans are one of evolution’s most dramatic history, the origin of multicellularity, and the dif-
experiments with multicellularity, and yet we ferentiation of epithelial tissues.
know surprisingly little about their origins. The
fossil record provides no insight into the biology of
3.2 Phylogenetics: are there any
the unicellular ancestors of metazoans. Indeed, the
‘living models’ of early metazoan
relatively abrupt appearance of fossils attributable
ancestors?
to modern metazoan phyla over the c. 80 million
year span of the Cambrian radiation obscures the 3.2.1 The case for choanoflagellates
sequence of metazoan phylogenesis. Nonetheless,
Choanoflagellates and sponges have classically
by merging phylogenetics and comparative gen-
been thought to straddle the evolutionary divide
omics with comparative cell biology, we can infer
between metazoans and their unicellular ances-
some of the earliest events in metazoan evolution.
tors. Choanoflagellates, a group of heterotrophic

24
 O R I G I N S O F M U LT I CEL LU L A R I T Y 25

microeukaryotes, originally captured the atten- fi rmly established that sponges are metazoans,
tion of cell biologists for their striking similar- that metazoans are monophyletic, and that cho-
ity to the ‘feeding cells’ (choanocytes) of sponges anoflagellates are sister to metazoans (Burger
(James-Clark, 1866; Saville-Kent, 1880–82; see et al., 2003; Medina et al., 2003; Steenkamp et al.,
Figure 3.1). This resemblance was fi rst noted 2006; Moreira et al., 2007; King et al., 2008; Ruiz-
by Henry James-Clark in 1866, prompting one Trillo et al., 2008; see Figure 3.2). Furthermore,
of two interpretations: either that sponges and mitochondrial genome data and species-rich
choanoflagellates are derived from an ancestral phylogenetic analyses demonstrate that choano-
species that used choanoflagellate-like cells to flagellates are not derived from metazoans, but
capture bacterial prey, or that these cell types instead represent a distinct lineage that evolved
are only superficially similar and have evolved before the origin and diversification of metazoans
independently. Subsequent molecular phylogen- (Lavrov et al., 2005; Steenkamp et al., 2006; Rokas
etic analyses and comparative genomic data have et al., 2005; Jimenez-Guri et al., 2007).

(a) (b)

5 µm 5 µm

(c) (d)

2 µm 4 cm

Figure 3.1 Similarities between choanoflagellates and sponge choanocytes. Choanoflagellates are heterotrophic microeukaryotes
that use an apical flagellum to swim and to generate water flow, thus trapping bacterial prey on an actin-filled microvillar collar. Some
choanoflagellates, like the species of Proterospongia shown here, have both unicellular (a) and colonial (b) life-history stages. The
ultrastructural and functional characteristics of choanoflagellates are conserved in the feeding cells of sponges, choanocytes (c, adapted from
Leys and Eerkes-Medrano, 2006), despite vast differences in overall organismal morphology (d). Arrows indicate flagellum and braces indicate
the collar of individual cells.
26 ANIMAL EVOLUTION

3.2.2 The case for sponges

Bilateria
Arguments in support of sponges as useful ‘liv-

Metazoa
Ctenophora
Cnidaria
ing models’ of the last common metazoan ances-
tor (LCMA) stem from their cytological similarities
Trichoplax
with choanoflagellates, their phylogenetic position,
Sponges
and the antiquity of their fossil record. Of these
Choanoflagellates arguments the evolutionary link between cho-
Filasterea anoflagellates and sponge choanocytes is perhaps
the most compelling. The strength of this argu-
Ichthyosporea
ment lies in its proven predictive power; it was the
Fungi hypothesized homology of sponge choanocytes
with choanoflagellates that first suggested an evo-
Dictyostelium
lutionary relationship between choanoflagellates
and metazoans (to the exclusion of countless other
Figure 3.2 Phylogenetic relationships among metazoans and
their close relatives. The preponderance of available evidence eukaryotes). As discussed above, this predicted
supports sponges as the earliest branching metazoan lineage and relationship has since been independently borne
choanoflagellates as the closest living relatives of the Metazoa. out in phylogenetic analyses.
As such, comparisons with these lineages can uniquely inform us In addition to the observation that the sponge
about the nature of the last common metazoan ancestor (white
body plan is organized around the most ancient
circle) and the last unicellular ancestor of Metazoa (black circle).
Other close unicellular relatives of Metazoa, such as Filasterea and metazoan cell type, a preponderance of phylogen-
Ichthyosporea are poorly understood, but ongoing genome projects etic analyses based upon both morphological and
for members of these lineages promise to feature prominently in molecular data sets place sponges as the ‘earliest
future studies of metazoan origins. branching’ metazoans (i.e. all other metazoans are
more closely related to each other than to sponges:
Collins, 1998; Borchiellini et al., 2001; Medina et al.,
Increasing numbers of molecular phylogen- 2001, 2003; Eernisse and Peterson, 2004; Peterson
etic analyses of diverse microeukaryotes have and Butterfield, 2005; da Silva et al., 2007; Jimenez-
recently revealed a collection of taxa (including Guri et al., 2007; Sperling et al., 2007; Ruiz-Trillo
Filasterea, Ministeria, Capsaspora owczarzaki, and et al., 2008). With this perspective, we can begin
Ichthyosporea) in the internode between meta- to reconcile the ‘primitive’ nature of the modern
zoans and fungi (Ruiz-Trillo et al., 2004, 2008; sponge body plan with the fact that they, like most
Steenkamp et al., 2006; Shalchian-Tabrizi et al., metazoans, are the product of at least 600 million
2008). Choanoflagellates remain the closest years of independent evolution. Chance, key inno-
known relatives of Metazoa, and the cell morph- vations, or (more likely) both, resulted in drastic-
ology of these other diverse microeukaryotes ally different evolutionary outcomes in sponges
does not provide an obvious link to choanoflag- compared with other metazoans. Only after other
ellates and metazoans. Nonetheless, molecular metazoans diverged from sponges did traits such
phylogenetic analyses reveal that metazoans as nerves, muscles, tissues, and a digestive gut
count diverse single-celled and colony-forming arise.
lineages, in addition to choanoflagellates, among The fossil record is consistent with the hypoth-
their close relatives (Medina et al., 2001; Ruiz- esis that the sponge body plan has remained nearly
Trillo et al., 2004, 2007, 2008; Steenkamp et al. unchanged since the late Neoproterozoic (reviewed
2006). A phylogenetically informed comparison in Carrera and Botting, 2008). Specifically, sponge
of genomes from diverse microeukaryotes with fossils from between 750 Ma (Reitner and Wörheide,
those of metazoans and choanoflagellates prom- 2002) and 580 Ma (Li et al., 1998) represent the earli-
ises to further refi ne our understanding of pre- est known metazoan body fossils. By the time of
metazoan genome evolution. the Cambrian, sponge diversity was high, with
 O R I G I N S O F M U LT I CEL LU L A R I T Y 27

spicules from most major sponge groups forming existence of this clade is contradicted by numer-
an abundant component of the Cambrian fossil ous independent analyses and can be explained
record globally (Gehling and Rigby, 1996). by accelerated rates of evolution within Bilateria
A second, and less well established, phylo- (Dellaporta et al., 2006; Wang and Lavrov, 2008).
genetic result that has emerged is the possibility More recently, a genome-scale analysis of predicted
of sponge paraphyly. Under this scenario, some proteins from single-copy loci in the draft genomes
sponge lineages (e.g. calcareous and homoscle- of the sponge Amphimedon queenslandica and T.
romorph sponges) might be more closely related adhaerens strongly supported placozoans as an
to eumetazoans than to other, earlier branching independent lineage that branches after sponges,
sponge lineages (Collins, 1998; Borchiellini et al., and before cnidarians (Srivastava et al., 2008). This
2001; Medina et al., 2001; Peterson and Butterfield, result and others (Collins, 1998; da Silva et al., 2007)
2005; Sperling et al., 2007). The evolutionary impli- cast doubt on the hypothesis that T. adhaerens is the
cations of sponge paraphyly have been thoroughly earliest branching metazoan.
explored and can be distilled into an argument Recently, Dunn et al. (2008) published a phyl-
that all extant metazoans are derived sponges ogeny based upon 150 EST-derived genes that
(Sperling et al., 2007; Nielsen, 2008). However, the supports ctenophores as branching before two
proposition of sponge paraphyly remains tenuous, sampled sponge species. This fi nding would imply
in part because analyses that include expressed one of two unlikely evolutionary scenarios: that the
sequence tag (EST) and mitochondrial genome LCMA was much more complex than previously
data from the homoscleromorph species Oscarella predicted (e.g. it had nerves, muscles, and a digest-
carmela strongly support sponge monophyly ive gut) or that the ctenophore lineage and other
(Jimenez-Guri et al., 2007; Lartillot and Philippe, eumetazoans underwent extensive convergent evo-
2008; Lavrov et al., 2008; Ruiz-Trillo et al., 2008; lution (Giribet et al., 2007). The former scenario is
Wang and Lavrov, 2008). not supported by the fossil record—sponges would
have had to undergo morphological simplification
before their appearance as the first recognizable
3.2.3 The controversy
metazoan fossils—and the latter explanation would
Despite the weight of evidence supporting the require the improbable, independent evolution of
placement of sponges at the base of the metazoan nerves, muscles, and a gut in the ctenophore and
tree, placozoans (Dellaporta et al., 2006) and, more cnidarian/bilaterian lineages. Instead, the weight
recently, ctenophores have also been posited as the of evidence places choanoflagellates as the closest
earliest branching metazoan phylum (Dunn et al., living metazoan outgroup, sponges as the earliest
2008). The case for placozoans derives from an ana- branching metazoan phylum, and argues that the
lysis of the mitochondrial genome from the only choanocyte-based feeding strategy of sponges is
characterized species, Trichoplax adhaerens. This ana- ancestral to all Metazoa.
lysis can be distilled into three arguments: (1) like
choanoflagellates and unlike most metazoans the
3.3 Reconstructing the genetic toolkit
mitochondrial genome of T. adhaerens is large (c.
for cell–cell interactions
43 kb compared with the 15–24 kb genomes typ-
ical of metazoans); (2) it contains an assortment of Choanoflagellates and sponges, by virtue of their
introns, intergenic spacers, and genes that are lack- positions on the tree of life, bracket metazoan ori-
ing from all other sequenced metazoan mitochon- gins and are well situated to help us understand
drial genomes (albeit, also without orthologues in the genetic innovations associated with the transi-
choanoflagellates or other non-metazoans); and (3) tion to multicellularity. Indeed, a wealth of genomic
phylogenetic analyses of predicted mitochondrial data have begun to pour out from representatives of
proteins support T. adhaerens as the earliest branch- both of these groups. The single-celled choanoflag-
ing lineage in an unprecedented clade that also ellate Monosiga brevicollis is the subject of a recently
contains sponges, ctenophores, and cnidarians. The completed genome project (King et al., 2008), and
28 ANIMAL EVOLUTION

genome sequencing projects are under way for the c. 80 SH2 domains: King et al., 2008; Manning
freshwater choanoflagellate Monosiga ovata and a et al., 2008, Pincus et al., 2008). In addition, two
colony-forming choanoflagellate, Proterospongia sp. choanoflagellates (M. brevicollis and M. ovata) con-
(Ruiz-Trillo et al., 2007). Likewise, sponges have tain homologues of the proto-oncogene Src and
received increasing attention from a genomics per- biochemical analyses reveal these homologues to
spective. Pilot EST projects have been completed conserve most of the regulatory interactions asso-
for the sponges O. carmela and Suberites domuncula, ciated with metazoan Srcs (Segawa et al., 2006; Li
and genome-scale data are available for the sponge et al., 2008). These observations establish the pres-
A. queenslandica (Nichols et al., 2006; Perina et al., 2006; ence of bona fide tyrosine kinase signalling during
Adamska et al., 2007a). The juxtaposition of sponge the pre-metazoan era.
and eumetazoan sequences with those from cho- With the accumulation of genome-scale data from
anoflagellates is beginning to reveal the catalogue early branching metazoans and their close out-
of genes present in their common ancestor, thus per- groups, an emerging theme is that the functional
mitting the construction of hypotheses about gen- protein domains found in developmentally import-
omic innovations underlying metazoan origins. ant metazoan signalling and adhesion genes have
A prediction from the field of evo-devo is that histories and, presumably, ancestral functions inde-
genes involved in regulating development play pendent of their roles in metazoan proteins. In other
important roles in morphological evolution. One words, these protein domains evolved prior to meta-
such class of genes includes those involved in the zoan origins and only later, as a product of domain
conserved signalling pathways that transduce or exon shuffling (see Patthy, 1999), were linked in
extracellular cues in diverse metazoans. Although the combinations found in the canonical signalling
all cellular organisms engage in cell signalling, the and adhesion proteins of modern metazoans.
pathways required for metazoan development are One example of this is the case of the secreted
more elaborate than those of unicellular organisms ligand Hedgehog. In bilaterians, the Hedgehog
and distinct from those found in other multicellu- signalling pathway is involved in developmental
lar lineages (e.g. fungi and plants). Traditionally, patterning events as diverse as segment polarity in
seven intercellular signaling pathways are consid- Drosophila and brain, bone, muscle, and gut pattern-
ered unique to and abundant in Metazoa: nuclear ing in vertebrates. The canonical Hedgehog ligand
hormone receptor, WNT, TGF-E, Jak/STAT, Notch/ is composed of two protein domains, an N-terminal
Delta, Hedgehog, and RTK (Gerhart, 1998; Barolo signalling domain that is released through auto-
and Posakony, 2002; Pires-daSilva and Sommer, proteolytic cleavage by a linked C-terminal intein
2003). At least six of these seven pathways (Wnt, domain (reviewed in Perler, 1998). Analyses of the
TGF-E, RTK, Notch, Hedgehog, and Jak-STAT) choanoflagellate, sponge, and cnidarian genomes
have conserved components that are expressed in reveal that the two functional domains known
sponges and thus were present in the LCMA (Adell from the bilaterian Hedgehog family evolved
et al., 2003; Nichols et al., 2006; Adamska et al., independently and were subsequently coupled
2007a,b; Adell et al., 2007). through domain shuffling early in metazoan evo-
In contrast with sponges, only two of the major lution (Figure 3.3). Specifically, the genomes of
metazoan signalling pathways, the RTK pathway the choanoflagellate M. brevicollis and the sponge
and components of the Hedgehog signalling path- A. queenslandica encode the Hedgehog N-terminal
way, are present in the genome of the choanoflag- and C-terminal domains on separate, unrelated
ellate M. brevicollis (King et al., 2008). Despite early proteins, whereas the cnidarian Nematostella vect-
suggestions that RTK signalling might represent ensis has orthologues of these proteins in addition
a key innovation in the evolution of metazoans to true Hedgehog proteins typical of bilaterians
from their single-celled ancestors (Hunter, 2000), (Adamska et al., 2007a; King et al., 2008; Matus et al.,
components of the pathway are abundant in the 2008). This pattern suggests that the Hedgehog gene
choanoflagellate genome (including c. 120 tyrosine family evolved through domain shuffling after the
kinase domains, c. 30 tyrosine phosphatases, and divergence of sponges from other metazoans and
Exploring the Variety of Random
Documents with Different Content
Die mit * bezeichneten und weitere Bände in
Vo r b e r e i t u n g .
 Als Fortsetzung des vorliegenden Bändchens
ist von d e m s e l b e n V e r f a s s e r erschienen:

Vo n d e r R e n a i s s a n c e b i s z u r
Gegenwart
Mit zahlr. Abb. 2. Aufl. A. Nat. u. Geistesw. Bd. 318. M. 1.20, geb.
M. 1.50

Geschichte der bildenden Künste

Eine Einführung von Dr. E . C o h n - W i e n e r . Preis ca. M. 4.—
Das Buch will kein historisch geordnetes Nachschlagebuch sein, sondern
möglichst viel vom Wesen der Kunst und des Kunstwerkes geben. Es sucht
neben dem bloßen Wissen die Freude am Kunstwerk zu vermitteln, erkennen
zu lassen, daß hinter dem Werk der Künstler als schöpferische Persönlichkeit
steht. Seine Aufgabe, der Selbstbelehrung und als Lehrbuch zu dienen, sucht
es nicht zu lösen, indem es durch oberflächliche Behandlung eines
verwirrenden Vielerlei „mitzureden“ befähigt, sondern durch eingehende
Bildhaftigkeit und Anschaulichkeit anstrebende Besprechung der behandelten
Kunstwerke sucht es dem Leser den inneren Gehalt der Kunstepochen so vor
Augen zu stellen, daß er auch die Werke, die das Büchlein selbst nicht
erwähnen kann, zu verstehen vermag. Eine reiche Zahl von Abbildungen —
darunter auch farbige — dient der Anschaulichkeit. Die neueste Zeit ist
besonders eingehend behandelt worden, weil hier das Bedürfnis am
unmittelbarsten ist.

Wörterbuch zur Kunstgeschichte

Von Dr. E r n s t C o h n - W i e n e r . Gebunden M. 3.—

Elementargesetze der bildenden

Kunst
Grundlagen einer praktischen Ästhetik von Prof. Dr. H a n s
C o r n e l i u s . 2. Auflage. Mit 245 Abb. und 13 Tafeln. Geh. M. 7.
—, geb. M. 8.—
 „Es gibt kein Buch, in dem die elementarsten Gesetze künstlerischer
Raumgestaltung so klar und anschaulich dargelegt, so überzeugend abgeleitet
wären. Wir haben hier zum ersten Male eine zusammenfassende, an
zahlreichen einfachen Beispielen erläuterte Darstellung der wesentlichsten
Bedingungen, von denen namentlich die plastische Gestaltung in Architektur,
Plastik und Kunstgewerbe abhängt.“
(Z e i t s c h r i f t f ü r Ä s t h e t i k . )

Die bildenden Künste

Ihre Eigenart und ihr Zusammenhang. Vorlesung von Professor
Dr. K a r l D o e h l e m a n n . Geheftet M. —.80
„Eine tiefgründige Besprechung der bildenden Künste — Malerei, Plastik
und Architektur umfassend — in durchweg anregender Form. Die Fachwelt
wie die gebildeten Stände werden die Schrift mit hoher Befriedigung
aufnehmen.“
(W i e n e r B a u i n d u s t r i e - Z t g . )

U n s e r Ve r h ä l t n i s z u d e n b i l d e n d e n
Künsten
Von Geh. Hofrat Prof. Dr. A . S c h m a r s o w . Geh. M. 2.—, geb. M.
2.60
„Diese Vorträge bilden den wertvollsten Beitrag zur Literatur über die
Kunsterziehungsfrage. Schmarsow entwickelt seine Anschauung über das
Verhältnis der Künste zueinander, um zu zeigen, wie jede einzelne einer
besonderen Seite der menschlichen Organisation entspreche, wie darum auch
alle Künste eng miteinander verknüpft sind, da alle von einem Organismus
ausstrahlen.“
(D e u t s c h e L i t e r a t u r z e i t u n g . )

Psychologie der Kunst

Darstellung ihrer Grundzüge. V. Dr. R . M ü l l e r - F r e i e n f e l s . 2
Bde. I: Die Psychologie d. Kunstgenießens u. Kunstschaffens. II:
Die Formen d. Kunstwerks u. d. Psychol. d. Bewertung. Geh. je
M. 4.40, in 1 Bd. geb. M. 10.—
 „Was diesem Werke Beachtung und Anerkennung erworben hat, ist zum
Teil der Umstand, daß es zu den sehr seltenen wissenschaftlichen deutschen
Büchern gehört, die auch einen ästhetischen Wert besitzen, aus denen eine
Persönlichkeit spricht, die über eine ungewöhnliche Gabe der Synthese
verfügt.“
(Z e i t s c h r i f t f ü r Ä s t h e t i k . )

Verlag von B. G. Teubner in Leipzig und Berlin

Bau und Leben der bildenden Kunst. Von Dr. Theodor

Volbehr. Mit 44 Abb. Geh. M. 1.20, geb. M. 1.50
„Im Gegensatz zu den Kompendien und Leitfaden alten Stils,
die die ‚Stile’ nach ihren äußeren Merkmalen klassifizieren, sucht
der Verfasser von einem neuen Standpunkte aus in das
Verständnis des Wesens der bildenden Kunst hineinzuführen. In
durchaus allgemein verständlicher Darstellung führt uns das
Buch in das Verständnis der Künstlerpersönlichkeit als des für
die Kunst entscheidenden Faktors ein. Die Entwicklung eigener
Ansichten verleiht dem feinsinnigen Buche hohen Reiz.“
(Z e i t s c h r . f . d . g e w e r b l . U n t e r r . )

Untersuchungen zur Geschichte der Architektur

und Plastik des früheren Mittelalters. V. Priv.-Doz. Dr.
G. Weise. Mit 22 Abb. i. Text u. 9 Abb. auf 5 Tafeln. Geh. M. 6.—,
geb. M. 7.—
Die hier vereinigten Einzeluntersuchungen wollen neue
Ergebnisse für die wichtigste Voraussetzung zur Erkenntnis ihres
Entwicklungsganges durch eine möglichst genaue Datierung der
erhaltenen Werke gewinnen und so für die karolingische und
merowingische Zeit eine Vermehrung dieses Materials liefern. In
drei Aufsätzen sind die Ergebnisse der von dem Verfasser in
jüngster Zeit an verschiedenen karolingischen Denkmälern
durchgeführten Grabungen niedergelegt. Eine Reihe kleinerer
Aufsätze bringt den Versuch, das heute der Forschung
zugängliche Material an karolingischen Denkmälern durch
Rekonstruktion einzelner verschwundener Bauten auf Grund der
Quellennachrichten zu bereichern.

Die Renaissancearchitektur in Italien. Von Dr. P.

Frankl. I. Teil. Mit 12 Taf. u. 27 Abb. M. 1.20, geb. M. 1.50
„Ein glänzend geschriebenes Kapitel über die sich an den
Namen Brunelleschi knüpfende Stilwandlung leitet den Band ein,
der die Darstellung der Renaissancearchitektur von den
Florentiner Anfängen bis zu den durch Bramante, Spaventa u.
Raffael geschaffenen Höhepunkten führt. Das Bändchen ist den
wichtigsten Erscheinungen über die italienische
R e n a i s s a n c e a r c h i t e k t u r beizuzählen.“
(B a u - R u n d s c h a u . )

Michelangelo. Eine Einführung in das Verständnis seiner

Werke. Von Prof. Ed. Hildebrandt. Mit 1 Titelbild u. 43 Abb. i.
Text. Geh. M. 1.20, geb. M. 1.50
„Dies Buch dürfte zu den besten populären Werken über M.
gehören. In überzeugenden, klaren Worten behandelt der
Verfasser das übermenschliche Werk dieses großen Meisters,
sein Leben und sein Wirken. Bücher wie diese sind dazu
geschaffen, tieferes Interesse an der Kunst zu erzeugen.“
(D e r A r c h i t e k t . )

Deutsche Baukunst. Von Geh. Reg.-Rat Prof. Dr. Ad.

Matthaei. 3 Bände. Bd. I. Deutsche Baukunst im Mittelalter. 3.
Aufl. Mit 29 Abb. Bd. II: Deutsche Baukunst seit dem Mittelalter
bis zum Ausgang des 18. Jahrhunderts. Mit 62 Abb. und 3 Tafeln.
Bd. III: Deutsche Baukunst im 19. Jahrhundert und in der
Gegenwart. Mit 35 Abb. Geh. je M. 1.20, geb. je M. 1.50, in 1 Bd.
geb. M. 4.50
„... In bündiger, überaus verständlicher Sprache entrollt der
Verfasser die Entwicklungsgeschichte der deutschen Baukunst.
Das Buch ist so recht geeignet, das zu erfüllen, was der
Verfasser am Schlusse des Buches als Zweck desselben
ausspricht: ‚Den Laien Klarheit schaffen über die Fragen der
Baukunst und die Künstler auf jene Zeit hinweisen, in der die
Baukunst der Ausdruck deutschen Wesens war.’“
(K u n s t u n d H a n d w e r k . )

Die Entwicklungsphasen der neueren Baukunst.

Von Dr. Paul Frankl. Mit 50 Abb. im Text u. 24 Abb. auf Tafeln.
Geh. M. 6.— geb. M. 7.50
Inhalt: Problem u. Methode. Die Entwicklungsphasen der
Raumform — der Körperform — der Bildform — der
Zweckgesinnung. Das Unterscheidende und das Gemeinsame
der vier Phasen.
Das Problem, die Architekturstile seit der Renaissance streng
zu definieren, wird hier von neuem aufgenommen. Die Methode
ist die, daß die vier Elemente der Architektur, Raumform,
Körperform, Bildform und Zweckgesinnung für sich untersucht
werden und die Stilmerkmale, die für jede der Stilphasen,
Renaissance, Barock, Rokoko und Klassizismus, als die
entscheidenden gelten sollen, auf die allgemeinste Formulierung
gebracht werden. Der gemeinsame Grundzug der ganzen
Periode ist die Beziehung zur Antike zunächst und daraus
folgend zu einem die Kunst verwissenschaftlichenden Begriff von
Richtigkeit, der zuletzt sich ausweitet zu einem Nebeneinander
und Nacheinander anerkannter Stilrichtigkeiten im 19.
Jahrhundert.

Die Begründung der modernen Ästhetik und

Kunstwissenschaft durch Leon Battista Alberti. Eine
krit. Darstell. als Beitrag z. Grundleg. d. Kunstwissenschaft. Von
Dr. W. Flemming. Geh. M. 4.—, geb. M. 5.—
Muß Galilei der Begründer der modernen Naturwissenschaft
genannt werden, so darf sein etwas älterer Zeitgenosse L. B.
Alberti der Vater der modernen Kunstwissenschaft heißen.
Bedeutungsvoller noch als seine Einzelergebnisse ist seine
Methode. Diese herauszuarbeiten, ihre Fruchtbarkeit zu erweisen
und also den Weg des Florentiners weiterzuschreiten ist das Ziel
dieser Darstellung.

Die altdeutschen Maler in Süddeutschland. Von

Helene Nemitz. Mit Bilderanhang. Geh. M. 1.20, geb. M. 1.50
Das Bändchen sucht das Verständnis für die Eigenart und
Größe der altdeutschen Malerei des 15. Jahrhunderts und so den
Sinn für die in ihren Werken sich offenbarende echt deutsche
Schönheit zu wecken. Es zeigt, wie das kraftvolle, tiefinnerliche
Gefühlsleben jener Zeit kaum irgendwo eine künstlerisch reinere
Ausprägung und Verklärung gefunden hat als in den Bildern der
Meister Süddeutschlands.

Albrecht Dürer. V. Dr. R. Wustmann. M. Titelbild u. 32 Abb.

Geh. M. 1.20, geb. M. 1.50
Eine schlichte und knappe Erzählung des gewaltigen
menschlichen und künstlerischen Entwicklungsganges Dürers
und eine Darstellung seiner Kunst, in der nacheinander Selbst-
und Angehörigenbildnisse, die Zeichnungen zur Apokalypse, die
Darstellungen von Mann und Weib, das Marienleben, die
Stiftungsgemälde, die Radierungen v. Rittertum, Trauer und
Heiligkeit sowie die wichtigsten Werke aus der Zeit der Reife
behandelt werden.

Niederländische Malerei im 17. Jahrhundert. Von Dr.

H. Jantzen. Mit 37 Abb. Geh. M. 1.20, geb. M. 1.50
Gibt eine Einführung in das Verständnis dieser Blütezeit der
Malerei, indem es die zahlreichen, dort in immer neuen
Stoffgebieten: Historienmalerei, Porträt, Gruppenbild, Sittenbild,
Interieur, Landschaft, Seestück, Kirchenstück, Stilleben
auftauchenden malerischen Probleme sowie ihre gesetzmäßigen
Zusammenhänge darlegt und die einzelnen hervortretenden
Künstlerpersönlichkeiten und -gruppen kurz und treffend
charakterisiert.
Rembrandt. V. Prof. Dr. P. Schubring. Mit 1 Titelb. u. 49 Abb.
Geh. M. 1.20, geb. M. 1.50
Eine lebensvolle Schilderung des menschlichen u. künstl.
Entwicklungsganges R’s. Zur Darstellung gelangen seine
persönl. Schicksale bis 1642, die Frühzeit, die Zeit bis zu Saskias
Tode, die Nachtwache, sein Verhältnis zur Bibel, die
Radierungen, Urkundliches über die Zeit nach 1642, die Periode
des farbigen Helldunkels, die Gemälde nach der Nachtwache
und die Spätzeit. Beigefügt sind die beiden ältesten Biographien
Rembrandts.

Der Impressionismus. Von Prof. B. Lazar. Mit 1 farb. Tafel

u. 32 Abb. auf Taf. Geh. M. 1.20, geb. 1.50
Betrachtet Werden und Wesen des Impressionismus bis in
die jüngste Zeit, mit besonderer Betonung der geschichtlichen
Entwicklung und mit Charakterisierung aller großen
impressionistischen Maler der Neuzeit.

Die künstlerische Photographie. Entwicklung, Probleme,

Bedeutung. V. Dr. W. Warstat. M. Bilderanh. M. 1.20, geb. M.
1.50

Die Natur in der Kunst. Studien eines Naturforschers z.

Geschichte d. Malerei. V. Prof. Dr. F. Rosen. M. 120 Abb. n.
Zeichn. v. E. Süß u. Photograph. d. Verf. Geb. M. 12.—

Grundzüge der Perspektive nebst Anwendungen.

Von Prof. Dr. Karl Doehlemann. Mit 91 Fig. u. 11 Abb. Geh. M.
1.20, geb. M. 1.50
Das für den Selbstunterricht gedachte Bändchen sucht auch
dem den mathematischen Dingen Abholden durch die
Anschauung die Einsicht in den Vorgang der perspektivischen
Abbildung wie das Verständnis der „freien Perspektive“ zu
vermitteln. Das Wesentliche und Gesetzmäßige ist
hervorgehoben, mit einfachen auch figürlich veranschaulichten
Anwendungsbeispielen belegt, ebenso sind Einzelaufgaben zur
Übung beigegeben.

Mathematik und Malerei. Von Oberlehrer Dr. G. Wolff. Mit

18 Fig. und 35 Abb. im Text u. auf 4 Tafeln. Kart. M. 1.60
Die nahen historischen Beziehungen zwischen Malerei und
mathematischer Perspektive werden dazu benutzt, um aus
formaler Darstellung eines Bildes dessen künstlerischen Wert zu
beurteilen. Der 1. Teil entwickelt im engsten Anschluß an die
Malerei die Grundlagen der malerischen Perspektive. Der 2. Teil
analysiert mit den so gewonnenen Mitteln einzelne
perspektivisch besonders lehrreiche Bilder.

Mathematik und Architektur. Von Prof. Dr. K.

Doehlemann. Kart. M. —.80

Deutsche Kunsterziehung. Im Auftrage des Deutschen

Landesausschusses für den III. Internat. Kongreß zur Förderung
des Zeichen- und Kunstunterrichts veröffentl. Mit Schülerzeichn.
aus Preußen, Bayern, Sachsen u. Hamburg auf 16 Taf.
Ausstattung des Buches v. Prof. P. Behrens. Geb. M. 2.—
Inhalt: L. Pallat: Zeichenunterricht. G . K e r s c h e n s t e i n e r :
Die Entwicklg. d. zeichner. Begabung. P. J e s s e n : Handarbeit u.
Kunst. G . P a u l i : Das deutsche Bilderbuch. P. H e r m a n n : Das
Wandbild in der Schule. C . G ö t z e : Junge Kräfte. A .
L i c h t w a r k : Die Entwicklung der deutschen Kunstmuseen.

Die Erziehung d. Anschauung. Von Prof. H. E.

Timerding. Mit 164 Fig. Geh. M. 4.80, geb. M. 5.60

Wandtafel und Kreideim Elementarunterricht.

Gedächtniszeichn. m. erläut. Text von Lehrer Othmer. 25 bunte
Taf. mit Erläuterungsheft. In Mappe M. 6.50
Die Technik des Tafelzeichnens. Von Dr. Ernst Weber.
3. Aufl. 40 teils farb. in Kreidetechnik gezeichn. Taf. nebst 1
Erläuterungsheft m. 6 Illustr. In Mappe M. 6.—

Technisches Zeichnen. von Prof. Horstmann, Regierungs-

u. Gewerbeschulrat. Geh. M. 1.20, geb. M. 1.50

Verlag von B. G. Teubner in Leipzig und Berlin

 Das Wesen der deutschen Kunst
Von Geh. Rat Prof. Dr. H . T h o d e . Mit Abb. Geh. M. 1.20, geb.
M. 1.50
Eine eingehende Charakteristik der Eigentümlichkeiten deutschen
bildenden Schaffens und deren Erklärung aus der Wesensanlage unseres
Volkes, die an Einzelbeispielen zeigt, wie in dieser die künstlerischen
Anschauungen, die Wahl und Auffassung des Gegenständlichen und die
stilistischen Erscheinungen begründet sind, und auf Grund solcher Erkenntnis
die Stellung und Bedeutung unserer bildenden Kunst der antiken und der
romanischen gegenüber bestimmt.

Die deutsche Malerei im 19.

Jahrhundert
Von Prof. Dr. R . H a m a n n . Mit 57 ganzseitigen und 200
halbseitigen Abbildungen. In Halbpergament M. 7.—
„H. hat eine ausgezeichnete Darstellung des Entwicklungsganges der
Malerei während des letzten Jahrhunderts gegeben. Meines Wissens gibt es
in der ganzen modernen Kunstgeschichtschreibung keine annähernd so
vortreffliche Darstellung des Wesens der Malerei seit 1860 bis zum Einbruch
des Naturalismus, als sie H. im 6. Kap. seines Werkes gibt. Es ist ein Genuß,
sich der meisterhaften Behandlung dieser Epoche ruhig hinzugeben.“
(P r e u ß . J a h r b . )

Der Landschaftsmaler Joh.

Alexander Thiele
u. seine sächsischen Prospekte. Von Landgerichtsrat Dr. M .
S t ü b e l . Text mit 15 Abb. u. 30 Lichtdrucktaf. In Mappe M. 20.—,
in Leinwandmappe M. 24.—
Thieles Einfluß hat sich bis auf Richter und dessen Schule erstreckt. Seine
Radierungen sind die ersten künstl. deutschen Landschaftsblätter des 18.
Jahrh. Das Buch beschäftigt sich mit Thieles Leben und Werken vom kunst-
und kulturgeschichtl. Standpunkt aus. Im 2. Teil sind auf 30 Lichtdrucktafeln
sächsische Prospekte wiedergegeben und ausführlich beschrieben.
 Der Städtebau nach seinen
künstlerischen Grundsätzen
Von C a m i l l o S i t t e . Ein Beitrag zur Lösung moderner
Fragen der Architektur und monumentalen Plastik unter
besonderer Beziehung auf Wien. 4. Aufl. Vermehrt um
„Großstadtgrün“. Mit 1 Heliogravüre, 114 Illustrationen und
Detailplänen. Geh. M. 6.—, geb. M. 7.40

Kunst und Kirche

Vorträge aus dem 1913 zu Dresden abgehaltenen Kursus für
kirchliche Kunst- und Denkmalspflege. Herausgegeben vom
Evang.-luther. Landeskonsistorium. Mit 61 Abbild. auf 32 Tafeln.
Geh. M. 4.—, geb. M. 5.—
I n h a l t : Gurlitt: Kunst und Kirche. — Schmidt: Der sächs. Kirchenbau bis
auf Georg Bähr. — Bestelmeyer: Baukünstl. Aufgab. der ev. Kirche in der
Gegenwart. — Gurlitt: Kirchl. Denkmalspflege. — Berling: Die
Sonderausstellung kirchl. Kleinkunst. — Högg: Friedhofskunst.

Die Renaissance in Florenz und

Rom
8 Vorträge von Prof. Dr. K . B r a n d i . 4. Aufl. Geh. M. 5.—,
geb. M. 6.—
„... Meisterhaft sind die Erscheinungen von Politik,
Gelehrsamkeit, Dichtung, bildender Kunst zum klaren
Entwicklungsgebilde geordnet, mit großem Takte die
Persönlichkeiten gezeichnet, aus freier Distanz die Ideen der Zeit
betrachtet. Die Ausstattung des Buches dürfte zum
Geschmackvollsten der neueren deutschen Typographie
gehören.“
(H i s t . J a h r b u c h . )
 Schriften von Johann Georg,
Herzog zu Sachsen
Streifzüge durch die Kirchen und Klöster Ägyptens. Mit 239 Abb.
Geh. M. 8.—. Tagebuchblätter aus Nordsyrien. Mit 85 Abb. Geh.
M. 4.80 Das Katharinenkloster am Sinai. Mit 43 Abb. auf 12 Taf.
Geh. M. 3.20

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