Table Of ContentACKNOWLEDGMENTS AND DEDICATION
The genesis of this book required far more than the ideas of the
editors alone. The original impetus was the invitation to organize a
symposium, "Paleontological and Neontological Approaches to the
Origin of Amniotes", for the Fourth International Congress of
Vertebrate Morphology. We thank speakers and the audience for their
enthusiastic response. We are most grateful to Susan Herring and
James Hanken for their support, interest, and suggestions, and to Susan
Abrams and R. Eric Lombard for their counsel when the project was in
its embryonic stages. We are extremely grateful to Dr. Chuck Crumly
and Mr. David Berl-Hahn for shepherding us through the process of
organization, editing, and publication of this work. Their keen interest
has been a driving force behind this production.
We are grateful for many perceptive comments and suggestions
from the following people who reviewed parts of this book: Donald
G. Buth, Chuck Crumly, James Hanken, James Hicks, Victor H.
Hutchison, Lee Kats, Sean Modesto, Kevin Padian, David Polcyn,
Elizabeth Rega, Bob Roberts, David Sever, Vaughan H. Shoemaker,
Richard E. Strauss, Hans-Dieter Sues, and Thomas Vandergon.
Dankeshon and cheers to Dr. Elizabeth Rega, merci to Charles
Solomon, and muchas gracias to Therese Whitney who provided
thorough advice on the vagaries of accents and diacritical symbols in
German and British English, French, and Spanish, respectively.
Advisors and colleagues have played an important role in the
development of the conceptual direction of this collection. We are
particularly grateful to David Berman, Eric Lombard, Peter Vaughn
and the UCLA Physiological Ecology Group for providing stimulating
input and inspiration.
Vll
via Acknowledgments
Support for production portions of this volume has been
provided by the CaHfomia State University San Bernardino Division
of Graduate Studies and Research, the National Geographic Society
(grant 5182-94), the National Science Foundation (BIR-9925034), the
North Atlantic Treaty Organization (grant CRG.940779), and the
University Research Council of Pepperdine University.
Friends and family have been alternately patient and impatient
as the needs arose. For keeping us focused, sane, and thoughtful, we
are thankful to: Alex Martin, Doug Martin, Greg Martin, David
Polcyn, Elizabeth Rega, Charles Solomon, and Katherine Thome.
Finally, it must be noted that Dr. Everett C. Olson is a
coauthor of one of the chapters in this volume. He has been a driving
force in vertebrate paleontology and was a profound influence on both
of the editors during the formative years of our professional careers.
We are proud that he saw fit to contribute to this project, and we are
even more proud that we may provide a vehicle for one of his final
publications. Everett C. Olson has passed on, but his influence
continues to refresh vertebrate paleontology. It is with great pleasure
that we note the enduring nature of his influence. Ole was throughout
his life a teacher, a mentor, and a friend. He was open-minded but
tough, always ready to listen to new ideas and argue them thoroughly.
We think he would have been pleased and intrigued by the many new
ideas in this collection. It is with extreme affection, and a profound
sense of loss, that we dedicate this book to him.
Figure 1. Everett C. Olson: Mentor, teacher, and friend.
CONTRIBUTORS
Nancy Aguilar Larry Frolich
Center for Marine Biotechnology and Department of Biology
Biomedicine University of St. Thomas
Scripps Institute of Oceanography St. Thomas, Minnesota
University of California, San Diego USA
LaJolla, California 92093 Instituto Superior
USA Quito, Ecuador
David S Berman Carl Cans
Section of Vertebrate Paleontology Department of Biology
Carnegie Museum of Natural History University of Michigan
Pittsburgh, Pennsylvania 15213 Ann Arbor, Michigan 48109
USA USA
Richard Beerbower Theodore Garland Jr.
Department of Geological Sciences Department of Zoology
Binghamton University University of Wisconsin
Binghamton, New York 430 Lincolin Drive
USA Madison, Wisconsin 53706
USA
Ramon Diaz-Uriarte
Gary B. Gillis
Department of Zoology
University of Wisconsin Department of Ecology and Evolution
430 Lincolin Drive University of California, Irvine
Madison, Wisconsin 53706 Irvine, California 92717
USA USA
Robert Dudley Jeffrey B. Graham
Department of Zoology Center for Marine Biotechnology and
University of Texas Biomedicine
Austin, Texas 78712 Scripps Institute of Oceanography
USA University of California, San Diego
LaJolla, California92093
USA
IX
Contributors
Nicholas Hotton III Everett C. Olson
Department of Paleobiology Department of Biology
National Museum of Natural History University of California Los Angeles
Smithsonian Institution Los Angeles, California 90024
Washington, D.C. USA
USA
Mary J. Packard
George V. Lauder Department of Biology
Department of Ecology and Evolution Colorado State University
University of California, Irvine Fort Collins, Colorado 80523
Irvine, California 92717 USA
USA
Robert R. Reisz
Michel Laurin
Department of Zoology
Museum of Paleontology University of Toronto, Erindale
University of California Campus
Berkeley, California 94720 Mississauga, Ontario L5L 1C6
Canada
Michael Y. S. Lee
School of Biological Science Roger S. Seymour
Zoology A08 Department of Zoology
University of Sydney University of Adelaide
New South Wales 2006 Adelaide SA 5005
Australia Australia
R. Eric Lombard Patrick S. Spencer
Department ofOrganismal Biology Department of Geology
and Anatomy University of Bristol
The University of Chicago Queens Road, Bristol BS8 IRJ
Chicago Illinois 60637 United Kingdom
USA
James Stewart
Karen L. M. Martin
Faculty of Biological Science
Division of Natural Sciences University of Tulsa
Pepperdine University Tulsa, Oklahoma 74104
Malibu, California 90263 USA
USA
Stuart S. Sumida
Kenneth A. Nagy Department of Biology
Department of Biology California State University, San
University of California Los Angeles Bernardino
Los Angeles, California 90024 San Bernardino, California 92407
USA USA
CHAPTER 1
AN INTEGRATED APPROACH TO THE ORIGIN
OFAMNIOTES: COMPLETING THE
TRANSITION TO LAND
Karen L. M. Martin
Stuart S. Sumida
The origin of amniotes was a critical step in vertebrate evolution. It is
apparent that fundamental, macroevolutionary changes in the natural
histories and physiological features of tetrapods occurred at or near
this transition, which set the stage for the Age of Reptiles and,
ultimately, for the radiation of mammals and birds. Despite its
tremendous evolutionary importance, the origin of amniotes has been
addressed directly by relatively few studies. Other biologically
important transitions, for example the transition from water to air
breathing or the evolution from ectothermy to endothermy, have been
examined independently by many disciplines. However, the origin of
amniotes has been, for the most part, studied by paleontologists and
thus limited to osteological data. Our goal has been to bring together
paleontologists and neontologists specializing on both extant and
extinct organisms, to examine this evolutionary transition that is rich
in importance, but historically poor in testable hypotheses.
Amniote Origins
Copyright © 1997 by Academic Press, Inc. All rights of reproduction in any form reserved.
K. L. M. Martin and S. S. Sumida
Amniotes were the first vertebrates to complete the transition
to land, and this release from life history stages requiring bodies of
water provided a profound freedom for new evolutionary radiations.
Their descendants accomplished innovations in terrestrial herbivory,
behavioral thermoregulatory strategies, respiration in air, water
balance and conservation, and new means of locomotion, including
flight. In this volume we provide a holistic approach to understanding
primitive tetrapods that should increase our understanding of this
macroevolutionary change. Our aim is to provide a broad overview of
the evolution of the vertebrate body with both paleontologists and
neontologists addressing the origin of amniotes and making inferences
from a variety of different perspectives. Vertebrate paleontologists
have been slow to adopt experimental approaches, and reproducible
studies addressing function by vertebrate paleontologists are still
disappointingly few. Conversely, functional morphologists and
physiologists rarely address the influences that their work on extant
organisms might have on understanding the extinct animals that made
the transition from anamniote to amniote. We hope that this volume
will prove to be heuristic, generating dialogue and forging new
connections to stimulate novel ways of thinking about the evolution of
the tetrapods.
SCIENTIFIC AND HISTORICAL PERSPECTIVE
Early focus on the origin of amniotes inevitably turned to a
search for progressively more primitive, and in some cases
hypothetical, ancestors (Romer, 1966; Carroll, 1969a,b, 1970). Over
the course of the past thirty years, the context in which primitive
tetrapods have been examined has changed radically. New concepts in
biogeography and the acceptance of plate tectonics forced a
reexamination of the taxa presumed to be close to the origin of
amniotes (Hotton, 1992). The advent of cladistic methods of
phylogenetic analysis has suggested profoundly different hypotheses
regarding the primitive radiations of amniotes (e.g., Heaton, 1980;
Holmes, 1984; Heaton and Reisz, 1986; Gauthier et al, 1988a,
Berman et al, 1992; Lee, 1993, 1995; Carroll, 1995; Laurin and Reisz,
1995). This volume has grown out of our desire to address new
advances in our understanding of the phylogenetic relationships of
Completing the Transition to Land 3
early amniotes and to add the critically important experimental
approaches of functional biology.
The authors gathered here address the integrated influences of
morphology, physiology, evolutionary biology, behavior,
developmental biology, histology, ecology, and phylogeny on the
origin of amniotes. However, caveats are necessary. With fossil
animals, only the morphology of hard tissues can typically be studied;
the other aspects of their biology must almost always be inferred. Yet
morphology may be a poor predictor of physiology; animals with
similar morphologies may have very divergent physiologies (Burggren
and Bemis, 1990). Moreover, changes in physiology or function may
leave few morphological clues in the fossil record (Lauder, 1981).
Clearly, many inferences are not testable by experimentation or
observation when studying extinct organisms. Nevertheless, we
believe that the present can be gainfully considered as a key to the
past, provided caution is used (Garland and Carter, 1994). With
appropriate care, we believe that useful analogies can be made
between extant and extinct animals.
OVERVIEW OF TEXT
A major concern in approaches to the study of the origin of amniotes is
the controversy surrounding nomenclature and phylogeny of the
groups formerly known as the Amphibia and the Reptilia. In a
rigorous use of cladistic terminology, these two groups are radically
re-defined (Gauthier et al, 1988b). The word "amphibian" is not used
in a taxonomic sense, although it is often used by authors included
here as a colloquial means of communicating the concepts of
anamniote tetrapods. Groups of animals previously placed under the
term "Reptilia" are considered to be paraphyletic. Therefore, we have
attempted to focus this work on the earliest amniotes and their
immediate sister groups. In order to provide context, however,
neontological examples are taken from extant animals that may of
necessity be far removed phylogenetically from this transition. Where
inferences are drawn, chapter authors have stated their assumptions
explicitly. Laurin and Reisz examine current hypotheses about the
phylogeny of tetrapods in "A New Perspective on Tetrapod
Phylogeny," as do Lee and Spencer in "Crown-Clades, Key
4 K. L. M. Martin andS. S. Sumida
Characters and Taxonomic Stability: When Is an Amniote Not an
Amniote?" Significantly, the first chapter suggests that extant
lissamphibians may be more closely related to early amniotes than was
previously supposed, thus making them potentially much more useful
surrogates for testing physiological hypotheses. In "Biogeography of
Primitive Amniotes," Berman, Sumida, and Lombard update the
biogeographic context for the evolution of early amniotes and point
out the importance of Pangea and plate migration in the spread of
tetrapod groups.
The physical and physiological transition to land began long
before the origin of amniotes. Some of the most primitive fishes may
have had lungs for air breathing (Randall et al, 1981). Many
primitive tetrapods were semi-terrestrial and may have spent part of
their lives on land (Smithson, 1980), perhaps even breeding
terrestrially (Carroll, 1988). Their eyes, ears, and lateral lines must
have adjusted to the medium of air instead of water (Duellman and
Trueb, 1986). These changes may be considered exaptations (Gould
and Vrba, 1982). Insects and plants completed the transition to land
before the vertebrates came fiiUy ashore, providing habitat, cover, and
food for the explorers of this brave new world, but a diet of high-fiber
plants probably required changes in digestive physiology (Diamond
and Buddington, 1987). Habitat and climate are discussed in the
chapters "Biogeography of Primitive Amniotes" and "The Late
Paleozoic Atmosphere and the Ecological and Evolutionary
Physiology of Tetrapods" by Graham, Aguilar, Dudley and Gans.
Lauder and Gillis explore ways that these animals exploited food
resources in a chapter on "Origin of the Amniote Feeding Mechanism:
Experimental Analysis of Outgroup Clades." Hotton, Olson, and
Beerbower take a parallel approach with extinct taxa in the chapter
"Amniote Origins and the Discovery of Herbivory." Movement on
land required adjustments to the axial and appendicular skeleton
(Sumida and Lombard, 1991), discussed in the chapter "Locomotor
Features of Taxa Spanning the Origin of Amniotes" by Sumida.
The evolution of an amniotic egg was a key innovation
(Thomson, 1992) that defines this clade and provided one of the means
of invasion of a new habitat. Aspects of this process are included in
the chapters by Packard and Seymour in "Evolution of the Amniote
Completing the Transition to Land
Egg" and by Stewart in "Morphology and Evolution of the Egg of
Oviparous Amniotes." However, the differences between the adults of
the earliest amniote and its immediate anamniote "predecessor" may
have been minor and apparently unremarkable at the time of the
transition, and indeed, the exact identity of the earliest amniotes may
still be in doubt (Romer, 1966; Carroll, 1969a,b; Lombard and
Sumida, 1992; Smithson er a/., 1994).
The differences between present-day lissamphibians and extant
"reptiles" go far beyond the evolution of the amniotic egg. It has been
suggested that the group Reptilia should not be defined solely on the
basis of morphology but also on shared life history and physiological
traits (Gans and Pough, 1982). Such traits may permit wide variation
in structure. We suggest that this may also be true for the "Amphibia,"
and that the origin of amniotes may have been a step that left few
tangible morphological clues but engendered enormous physiological
changes that profoimdly altered the course of evolutionary history.
These differences are examined as clues to past physiological
evolution in the chapters on "The Role of the Skin in the Origin of
Amniotes: Permeability Barrier, Protective Covering, and Mechanical
Support" by Frolich and "Water Balance and the Physiology of the
Amniote Transition" by Martin and Nagy. In the final chapter,
"Reconstructing Ancestral Trait Values Using Squared-Change
Parsimony: Plasma Osmolarity at the Amniote Transition," Garland,
Martin, and Diaz-Uriarte use physiological data to test a historical
hypothesis with a phylogenetic analysis.
We are attempting to foster a closer communication between
experimental physiologists and morphologists who work on testable
models and the paleontologists who study the fossils of animals that
lived at the time of the origin of amniotes. The work of each group
has implications for the other, and we provide here a framework for
that cooperation. We intend this gathering of paleontological and
neontological specialists to provide an integrated benchmark collection
of studies that will be of use to students of vertebrate paleontology,
physiology, herpetology, fiinctional morphology, evolution, and
vertebrate biology in general. Furthermore we hope that it will
stimulate new work in this long-neglected area. This collaborative
effort is an optimistic beginning. As the biological sciences advance
6 K. L. M. Martin andS. S. Sumida
with new techniques and integrated approaches, we are hopeful that
this volume will invigorate the cooperative analysis, by students of the
past and present, of an event that took place at least 350 million years
ago.
ACKNOWLEDGMENTS
The authors thank Drs. David Polcyn, Elizabeth Rega, and
Thomas Vandergon for reading the text and providing useful
comments on its form and construction.
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