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L-...~:: Synthe$izing-kbgsf romrhe rich and big& ./
b.,--F-1 .; aiwse-fossi-l r-e.c ord of amphibians, Robert Carroll .:>- . ,.-?-.1. :-;7-i-~1-1. : .1if7 il
m4.j\.~l=C,.akze. g.t r aces their. ...o.....r i&ibacls. 365 &ion years, when pc. - .:.. -....-,.!.. :.-.:.:. ;.. ,=-.gl:.r ::>S
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!..-<;a<:* zzt i-d. ar species of fiih traveled down an evolutionary .!E.-.:>.-= j-LI j%ig- -L
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clysrnic extinction 250 million years ago. After a long
G gap, modern amp-h ihian groups gradually emerged. ...-.... ... - , ,+ \-:.%.. CG
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N Oth~e n umber of amphibian species and individiials.-..!. .:;.l.I:.. %
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S in their Gtural habitats-t hroughout their long exis- EZjs!!
,L.v*- tence. The most cci.mprehmsiv~.examirration..omf ; .---il.) -&j. i.F*.!..E. . .. -iT.i g
-bE.,-.-_W Y phihian evolution everproduced, The Rise qf Amphibiam ---.,3 -F
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gists, geologists, and evo.l..u tionary biologists. i-i-:T-pI1tE + er :3:=x :i =-~~.
-p .. ...- .. . . . . >.... -.v.-._-.- .-- . .F--.:.. , . ... .. .- ........ ..... ..... .-.........-.-.. .,. . ...,. . . .p,.,. .-.. ....:.. .,-..-- --. :,-. . .-..: . ..-. :... .5-.L :,: . .: :==- :.:..... :,.,:.= .--.: :-- : ::-:=:-:.I-.*-. 2-_ :>- : LL
C 2009 The Johns Hopkins University Press
.U1 nghn reserved. Published 2009
hinted in the United States of America on acid-free paper
987654321
The Johns Hopkins University Press
2715 North Charles Street
Baltimore, Maryland 21218-4363
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Library of Congress Cataloging-in-Publication Data
Carroll, Robert Lym, 1938-
The rise of amphibians : 365 mdlion years of evolution I Robert Carroll.
p. cm.
Includes bibliographical references and index.
ISBN-13: 978-0-8018-9140-3 (hardcover : alk. paper)
ISBN-10: 0-8018-9140-X( hardcover : alk. paper)
1. Amphibians-Evolution. I. Title.
QL645.3.C37 2009
597.8'138-dc22 2008024792
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The Johns Hopkins University Press uses environmentally friendly book
materials, including recycled text paper that is composed of at least 30
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content.
To the many students I have supervised during my
professionaZ careu-undergraduates, graduate students,
and postdoctoraZfeZZows-who have assisted me in my
research and continue to contribute to my education
CONTENTS
Preface ix
Acknowledgments xi
I History of the Earth and Life 1
2 Advanced Metazoans and the Ancestry of Vertebrates 17
3 The Origin of Amphibians 38
4 The Radiation of Carboniferous Amphibians 61
5 Adaptation, Radiation, and Relationships 144
6 The Zenith of Amphibian Diversity 162
7 The Origin of Amniotes: Escapefiom the Water 193
8 Stereospondyls: Escapefiom the Land 209
9 The Enigma of Modern Amphibian Origins 228
10 The Ancestry of Frogs 253
I I The Ancestry of Salamanders 267
12 Eocaecilia and the Origin of Caecilians 291
13 The Success of Modern Amphibians 306
14 The Future of Amphibians 323
Abbreviations Used in Illustrations 331
Glossary 335
References 337
Index 355
PREFACE
0 DE RN AMPHIBIANS -the familiar frogs and salamanders of the
Northern Hemisphere and the less well-known, elongate, and limbless
caecilians of the Southern Hemisphere-appear as relatively minor com-
ponents of the living fauna, although they actually outnumber the dominant mam-
mals in terms of both numbers of species and individuals. In fact, the three modern
amphibian groups are but relicts of a much larger radiation that occurred between
370 and 270 million years ago, when their ancestors dominated terrestrial and shal-
low water environments throughout the world. Of even greater significance, the
early amphibians provided an evolutionary link between archaic fish and the ances-
tors of all more advanced terrestrial vertebrates: the reptiles, birds, and mammals.
That is, they were our own ancestors.
We retain many of the skeletal features of the earliest known amphibians, which
were able to move about on land more than 365 million years ago. They already ex-
hibited paired limbs, with bones comparable to ours, broadly similar vertebrae, and
homologues of our skull bones and sensory organs. But these animals had a much
more primitive life history, for they laid eggs in the water and developed via aquatic
larvae, as must have been the case for their immediate fish ancestors. This, of course,
is the pattern of development observed in the most primitive living amphibians,
which makes them potential models for the study of the transition between fish and
fully terrestrial vertebrates.
On the other hand, modern frogs, salamanders, and caecilians are far dfierent
from one another in both their adult anatomy and ways of life, and none can serve
as a model for the ultimate ancestors of terrestrial vertebrates. Fortunately, there
is an extremely rich fossil record of earlier amphibians that documents their prior
diversity and provides evidence of their origin from primitive fish, as well as relation-
ships to the antecedents of the reptiles, birds, and mammals that subsequently came
to dominate the earth.
Despite their importance in the history of life, neither fossil nor living amphibians
X PREFACE
have ever received the attention given to dinosaurs, birds, or ancient life), herpetology (the study of modem amphibians
mammals, and no previous book has attempted to document and reptiles), geology (the study of the earth and the p
their long and eventful evolution, covering a period of over cesses that have influenced its history), and astronomy he
365 d o ny ears. history and structure of the universe and the context of the
Study of the evolution of life is like a detective story, earth within that history), as well as biology (including de-
looking for clues from bodies dead for millions or hundreds scriptive and functional anatomy, physiology, and especiak-
of d o n so f years. Like forensic workers, we must under- evolution and its adaptive, genetic, and molecular basis).
stand their anatomy, physiology, and way of life, as well as Amphibians are but a single group of vertebrates. but in
the cause of their extinction. We also must know when they terms of their basic anatomy, physiology, and ways of l&
died and who their relatives were. But as paleontologists or they share major attributes with other animals, including a
evolutionary biologists, we must also be able to reconstruct backbone, an anteriorly placed brain with associated sense
the long periods of behavioral, anatomical, and physiological organs of smell, sight, and balance, and locomotion based
change that linked animals as distinct as fish, amphibians, and primitively on lateral undulation of the trunk. More broadly,
reptiles, and to understand the processes and causal factors amphibians and other vertebrates share with all other multi-
involved in adaptation to different ways of life and the origin cellular animals a unique system of genetic control that en-
of entirely new structures and body forms. ables them to evolve complex body parts associated with spe-
History, and especially the extremely long history of life, cialized means of feeding, locomotion, and reproduction.
is of interest in itself, but may also help us to understand To understand how these features evolved requires an
changes that are occurring in the modern biota and may be even wider view, encompassing the very origin of life and
expected to change in the future. Human history has been the evolution of biochemical and genetic processes that unite
but a brief moment in the evolution of life, but a more com- all organisms on earth and their ancestors, back to the first
plete understanding of the past might help us to prolong appearance of organic compounds that accumulated in the
our future, or at least that of the few surviving amphibian waters of the earth approximately 4 billion years ago. It is
groups. only when we place amphibians in this larger context that we
This book chronicles the history of amphibians from their can begin to understand their total evolutionary history.
origin among archaic fish, through their early dominance, a Considering amphibians in this broad context also dem-
period of catastrophic decline, and the emergence of their onstrates the overall similarities of scientific investigation in
humble living descendants. Our understanding of early am- all disciplines. The study of evolutionary history depends on
phibian history is based almost entirely on knowledge of the procedures shared with astronomy, chemistry, physics, geol-
skeletal anatomy as revealed by their fossil record, for the vast ogy, and the health sciences of observing natural phenomena
majority of amphibian groups are totally extinct, without and attempting to find logical and consistent explanations for
living survivors. However, the living amphibians do provide their occurrence. These explanations take the form of hy-
much information as to the probable soft anatomy and ways potheses that can be tested by further observations or experi-
of life of their long-dead ancestors, which allows us to recon- mentation. Paleontology, like astronomy, is not directly ame-
struct their biological diversification during the 365 million nable to testing in a laboratory, since one cannot expect to
years of their evolution. re-create the Big Bang or the origin of life on earth, but one
More broadly, this book is intended not only as a narrative can study the light generated by stars and galaxies millions or
of amphibian history but also as a model, or example, of how even billions of years old, and continue to search for earlier
evolution has occurred. This involves integration of numer- and earlier fossils, in an attempt to establish conditions that
ous scientific disciplines, including paleontology (the study of existed when they initially formed or first evolved.
ACKNOWLEDGMENTS
I
0W E MY INTEREST IN paleontology to my father. Soon after my fifth
birthday he showed me fossils of marine invertebrates that he used in teaching
a high school science course. I immediately wanted to collect some myself. Col-
lecting began on our farm and in local gravel pits, but later expanded to more distant
areas in Michigan and fmally to a number of classic vertebrate localities in the west-
ern United States, interspersed with visits to many museums. My professional career
was most strongly influenced by Alfred Sherwood Romer, who introduced me to the
world of Paleozoic amphibians through collecting in the Permian red beds of Texas
and a thesis on the armored dissorophids. Romer was a superb supervisor, teaching
by example, with the highest research standards in the profession. I also benefited
greatly from classes in evolution taught by George Gaylord Simpson and Ernst Mayr
and in herpetology by Ernest Williams.
Dr. Romer further broadened my career by arranging for postdoctoral research
on the unique fauna of amphibians and reptiles from the upright trees of Joggins,
Nova Scotia. This led me first to the Redpath Museum, McGill University, Montreal,
where my work was greatly facilitated by Louise Stevenson, and the director, Alice
Johannsen, who later offered me positions in the museum and in the Department of
Biology, which I have occupied throughout my career. I have profited greatly from
the atmosphere of these departments, which have enabled me to supervise a host of
undergraduates and graduate students who have greatly increased our understand-
ing of the anatomy and relationships of fossil amphibians and reptiles.
This book could not have been written without the help of colleagues in many
other universities and museums throughout the world. These are listed in approxi-
mately chronological order: Wann Langston, then at the National Museum of
Canada, Ottawa; Err01 White and Allan Charig, British Museum (Natural History),
London; D. M. S. Watson, University College, London; Alec Panchen, University of
Newcastle upon Tyne; Rex Parrington, University Museum of Zoology, Cambridge;
Dr. Zzvorka, National Museum of Prague; Hermann Jaeger, Humboldt Museum,
Berlin; Dr. Bliiher, Geological Survey of Saxony, Freiberg, Financial support for the research on which this book was
Germany; Hermann Prescher, State Museum for Mineralogy based was provided by the Natural Sciences and Engineering
and Geology, Dresden; E. C. Olson and Peter Vaughn, Uni- Research Council of Canada.
versity of California, Los Angeles; James Kitching, Bernard I thank Vincent Burke, my editor at the Johns Hopiuns
Price Institute for Palaeontological Research, Johannesburg, University Press, for asking me to write this book and for an
South Africa; Michael Williams and David Dunkle, Cleveland hss upport dumg its genesis. This volume owes its color ro
Museum of Natural History; Tan Rolfe and Mahala Andrews, Tonino Terenzi, who produced the plates. For assembling,
Royal Scottish Museum, Edinburgh; and most recently, col- arranging, and labeling the other illustrations, I am greatly
laboration with Hong Li and Qing-Long Shao, director, Inner mdebted to Mary-Ann Lacey, who also attended to other
Mongolia Museum, Hohhot, on the study of MiddleJurassic technical aspects of integrating the text. David Green, Red-
salamanders. path Museum, contributed to the ha1 chapter, but also as-
Special thanks for information on living and fossil caecil- sisted throughout in providing information on the modem
ians are due to Marvalee Wake for providing a wonderful amphibian groups. The final form of the text owes much to
environment for the study of modern caecilians in her lab at the proofreadmg by my wife, Anna Di Turi, to whom I am
the University of California, Berkeley, and to Farish Jenkins also grateful for her panence during the many hours I spent
(Harvard) and Denis Walsh (University of Toronto) for invit- bent over a microscope or computer.
ing me to participate in the study of Eocaecilia.
