How Vertebrates Left the Water [1 ed.] 0520266471, 9780520266476

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How Vertebrates Left the Water

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How Vertebrates Left the Water Michel Laurin

UNIVERSITY OF CALIFORNIA PRESS Berkeley

Los Angeles

London

University of California Press, one of the most distinguished university presses in the United States, enriches lives around the world by advancing scholarship in the humanities, social sciences, and natural sciences. Its activities are supported by the UC Press Foundation and by philanthropic contributions from individuals and institutions. For more information, visit www.ucpress.edu. Digital version available at the University of California Press website. University of California Press Berkeley and Los Angeles, California University of California Press, Ltd. London, England English edition © 2010 by the Regents of the University of California Systématique, paleontologie et biologie évolutive moderne: l’exemple de la sortie des eaux chez les vertébrés. First published in the French language by Ellipses. © 2008 Edition Marketing S.A. Library of Congress Cataloging-in-Publication Data Laurin, Michel. [Systématique, paléontologie et biologie évolutive moderne. English] How vertebrates left the water / Michel Laurin. p. cm. Includes bibliographical references and index. ISBN 978-0-520-26647-6 (cloth : alk. paper) 1. Vertebrates—Evolution. I. Title. QL607.5L3813 2010 596.13'8—dc22 2010027056 16

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The paper used in this publication meets the minimum requirements of ANSI/NISO Z39.48-1992 (R 1997)(Permanence of Paper). Front cover: Paleozoic amphibians. Artist: Douglas Henderson. Back cover: Seymouria sanjuanensis. Photographer: David Berman. Used with permission of the Carnegie Museum of Natural History and The Museum der Natur, Gotha, Germany.

I dedicate this book to my wife, Alexandra, and my daughter, Pénélope, who must have both felt neglected sometimes when I spent long hours in front of my computer working on this book and related projects.

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CONTENTS

Preface ... xi

one How Can We Reconstruct Evolutionary History? . . . 1 Classification and Biological Nomenclature . . . 2 Modern Phylogenetics . . . 16 Homology and Analogy: Lungs, Swim Bladders, and Gills . . . 37 Geological Time Scale and the Chronology of a Few Key Events . . . 39 A Few Relevant Paleontological Localities . . . 40

two

Conquest of Land: Data from Extant Vertebrates . . . 45

Are Animals Still Conquering the Land Today? . . . 45 The Coelacanth, a Living Fossil? . . . 47

Dipnoans: Our Closest Extant Finned Cousins . . . 49 Reproduction among Tetrapods: Amphibians Are Not All Amphibious! . . . 51

three Paleontological Context . . . 55 The Conquest of Land in Various Taxa . . . 55 The History of Our Ideas about the Conquest of Land by Vertebrates . . . 63 The Lateral-Line Organ and the Lifestyle of Paleozoic Stegocephalians . . . 68

four Vertebrate Limb Evolution . . . 73 The Vertebrate Skeleton . . . 73 Hox Genes and the Origin of Digits . . . 75 Sarcopterygian Fins and the Origin of Digits . . . 79 Fragmentary Fossils, Phylogeny, and the First Digits . . . 82 The Gills of Acanthostega and the Original Function of the Tetrapod Limb . . . 88 Bone Microanatomy and Lifestyle . . . 89

five Diversity of Paleozoic Stegocephalians . . . 99 Temnospondyls . . . 99 Embolomeres . . . 106

Seymouriamorphs . . . 109 Amphibians . . .116 Diadectomorphs . . .121 Amniotes . . . 125 Stegocephalian Phylogeny . . . 127

six

Adaptations to Life on Land . . . 135 Limbs and Girdles . . . 136

Vertebral Centrum and Axial Skeleton . . . 140 Breathing . . . 142 The Skin and Water Exchange . . . 147 Sensory Organs . . . 150

seven Synthesis and Conclusion . . . 161 Conquest of Land and the First Returns to the Aquatic Environment . . . 161 Why Come onto Land? . . . 163 Modern Paleontology and the “Indiana Jones” Stereotype . . . 166 Glossary . . . 169 Bibliography . . . 175 Index . . . 187

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PREFACE

Life appeared in the oceans in a past so distant that it is difficult to imagine. The exact age of life on Earth is debated because the structures once considered to represent the oldest fossils (remains of ancient organisms, or traces which they left) have been reinterpreted as mineral crystallization in microscopic fractures by some paleontologists (this reinterpretation is itself debated). The first life forms were very simple and resembled extant bacteria, some of which formed stromatolites, the oldest of which are about 3 Ga (billion years) old (Fig. p.1). Stromatolites are still being formed today in some coastal regions. For at least 1.5 Ga, life remained in its native aquatic environment. Thus, for the greatest part of the history of the biosphere, life remained in water, diversified, and radiated into several ecological niches. The oceans and seas teemed with life well before the first animal ventured out of the water. In the last few hundreds of millions of years (Ma), life has come onto dry land. This transition was very gradual; it was initiated by simple life forms, such as bacteria. Later, more complex organisms ventured onto land: lichens, simple green plants (the first of which were mosses, horsetails, and lycopods), arthropods (arachnids, insects, crustaceans, etc.), mollusks (slugs and snails), annelids (earthworms, leeches), and xi

Figure p.1. Cnidarians. The fi rst metazoans (animals with several cells) were all marine. Cnidarians are among the oldest and simplest metazoans. Reproduced from Haeckel (1904).

Preface / xiii

vertebrates. Despite their late arrival in this new environment, vertebrates will be emphasized in this book because they include humans and nearly all our domestic animals (dogs, cats, birds, cattle, sheep, pigs, horses, etc.). Thus, most readers are probably more interested in vertebrates than in any other group. The conquest of dry land is a fascinating evolutionary problem because all systems and organs of our distant ancestors had been adapted to their aquatic habitat through hundreds of millions of years of evolution. This episode in the history of life on Earth is probably one of the most difficult to understand, and precisely because of this, it is no doubt one of the most interesting. The problems that our ancestors had to solve were so severe that some creationists have used them to try to cast doubt on the scientific study of biological evolution and to try to strengthen the case of their creationist “explanation” (this word is not entirely appropriate in this context) of biodiversity. We will see that scientists have formulated several theories that explain this fascinating history, and that one of the main challenges of modern paleontology consists of testing these theories through more or less indirect methods. This book summarizes what we know about this history, without hiding the gaps that remain in our knowledge. It also presents the methods used by paleontologists, these “detectives” of life history, to reconstruct our distant past. To avoid the excessive simplifications that too often reduce this type of book to “just-so stories,” a few technical terms, for which there is no vernacular equivalent, must be introduced. The reader should refer to the Glossary, which includes all these technical terms. Despite the modular organization of this book, I advise reading Chapter One, “How Can We Reconstruct Evolutionary History?” first. A brief section on extant vertebrates illustrates the surprising amount of data that can be extracted from contemporary species, but for obvious reasons, the emphasis of this synthesis is on fossils and the evolution of the first land vertebrates. Finally, in the conclusion, the reader will discover that, contrary to the “Indiana Jones” stereotype, paleontologists do not necessarily spend a great proportion of their

xiv / Preface

time excavating fossils in the field, and that a major part of the most fundamental discoveries results from the study of fossils first described by older generations of scientists, or from sophisticated analyses of databases that centralize data that have long been available but used to be scattered. This book is mostly for life and earth science students who want to learn the basics of modern paleontology, systematics, and evolutionary biology, or those interested in the history of the conquest of land by vertebrates. It requires little prior knowledge in this field. Some points are covered in sufficient detail to give the reader a sense of how science works, but this book does not attempt to cover all relevant facts, because this would result in a much larger work. Those who want to know more will fi nd the key publications in the bibliography; they can also consult the exhaustive reviews of Devonian limbed vertebrates by Clack (2002, 2006). Another recent and very technical synthesis (Hall, 2007) covers the diversity, function, and evolution of fins and limbs and presents points of view not all of which are compatible with those found in this book (see Laurin, 2007). The history of our ideas about the origin and first evolutionary radiation of limbed vertebrates was recently summarized by Coates et al. (2008). Finally, a detailed review of the hypotheses about the origin of extant amphibians was recently published (Anderson, 2008), along with a commentary presenting a different perspective (Marjanovic and Laurin, 2009). This is a translation of a book initially published in French (Laurin, 2008b). The text and bibliography were updated (several papers published in 2008 and 2009 were added), and a few references to especially important older studies were also added. To the reader who may wonder how paleontological research can be useful, I answer simply that it enables us to know our distant history. Like archeology, paleontology is a historical science. Such research does not normally lead to patents, but it enables us to satisfy our curiosity and it has played an important role in the development of science fiction, especially since the discovery of Mesozoic dinosaurs. From Jules

Preface / xv

Verne’s Journey to the Center of the Earth through Michael Crichton’s Jurassic Park, paleontology has played a central role in popular culture. The reader will discover that reality can be as fascinating as fiction. I thank the colleagues who helped me write this book. Joseph Segarra has given me much advice and many comments on the French edition of this book. Various colleagues (Vivian de Buffrénil and Louise Zylberberg) and students (Aurore Canoville, David Marjanovic, and Laëtitia Montes) of the team “Squelette des vertébrés” have proofread chapters of the French edition of this book. Christopher A. Brochu, Stephen Godfrey, Michael S. Y. Lee, David Marjanovic, Sean P. Modesto, and Robert R. Reisz read chapters of this English translation. Douglas Henderson allowed me to reproduce his very nice reconstructions of early stegocephalians in their habitat. My former thesis advisor, Robert R. Reisz, has played a central but indirect role in drawing my attention to Paleozoic stegocephalians and in communicating his enthusiasm for the study of this episode in vertebrate evolution. My greatest debt lays with my parents, who have always actively supported my studies, and even the fairly bold project (which I had first imagined in the 1970s) of becoming a paleontologist.

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chapter one

How Can We Reconstruct Evolutionary History?

Our first ancestors were all aquatic. The oldest known vertebrates are about 500 Ma old, but the first potentially terrestrial vertebrates are less than 350 Ma old. For more than 150 Ma, our ancestors swam with their fins and breathed through their gills; on dry land, these structures were very inefficient. Their sensory organs worked poorly in air, if at all, and had to undergo various modifications to adapt to life on the continents. The eyes of our ancestors lacked eyelids and tear glands and could dry out rapidly; their ears did not enable them to hear most airborne sounds, such as the vocalizations of many frogs, birds, and mammals, such as the human voice. Yet all these problems were solved, and the few vertebrate species that succeeded in adapting to this new environment about 320 Ma ago diversified into the more than 25,000 extant species of land vertebrates. To reconstruct this history, we need objective methods to use the indirect information on evolution provided by fossils or the extant biodiversity, as well as principles of nomenclature to produce classifications. These techniques and concepts are widely used in modern evolutionary biology. Thus, phylogenetics provides evolutionary trees that are the starting point of comparative or biodiversity analyses for a broad range of evolutionary problems or taxa. Biological nomenclature 1

2 / How Can We Reconstruct Evolutionary History?

provides rules that enable systematists to present classifications (better called taxonomies) to summarize the evolutionary relationships between species and to sort our knowledge of the biosphere. Recent developments in phylogenetics and, to a lesser extent, in biological nomenclature have given new life to paleontology and evolutionary biology. Until approximately the 1970s, paleontologists reconstructed evolutionary trees by hand, using criteria that they did not always explain. Since then, the advent of cladistics, soon followed by software that enabled systematists to tap into the tremendous processing power of computers, introduced more objectivity into phylogenetics because the data used to produce the trees are generally published. This triggered a proliferation of phylogenetic studies and led to a re-examination of many long-held hypotheses on the phylogeny of life. As a result, we now have a much better resolved tree of life than a few decades ago, even though much of this tree will probably change as a result of future investigations. These methods are presented in a simplified manner in this chapter, and the bibliography provides an introduction to the most relevant papers where more technical information can be found.

CLASSIFICATION AND BIOLOGICAL NOMENCLATURE

Rank- Based Nomenclature A form of classification is essential to sort information, whatever its nature. Man has classified animals since antiquity, as attested in the Bible (ESV, 2001), in which we can read: “So out of the ground the Lord God formed every beast of the field and every bird of the heavens and brought them to the man to see what he would call them. And whatever the man called every living creature, that was its name.” (Genesis, 2:19). Since Aristotle (384–322 bce), many authors have proposed classifications of living beings. The subdiscipline of biology that consists of naming, defi ning, and delimiting the groups of living organisms (the taxa) is called “taxonomy,” like the product of this ac-

How Can We Reconstruct Evolutionary History? / 3

tivity (the taxonomies). Thus, taxonomy harks back to antiquity (under a form substantially different from today’s), but, initially, only vernacular names were used. These were part of the standard vocabulary of a language, in contrast to formal names that are often known only by scientists. The drawback of vernacular names is that their meaning can vary in space and time (this is typical of most words in any language), and there are often no exact synonyms among languages. Thus, the word “fish” once included whales (until the 19th century), although they are now excluded because we now know that whales are mammals that have returned to the seas. In English, this word has also included, at least in its broadest sense, aquatic animals that are no longer considered “fishes,” such as echinoderms (e.g., “starfish”), arthropods (e.g., “crayfish”), mollusks (e.g., “cuttlefish”), or even cnidarians (e.g., “jellyfish”); but this is not true of many other European languages, such as French, in which the equivalent word “poisson” has long had a narrower sense restricted to aquatic vertebrates. These two words (“fish” and “poisson”), often considered synonyms, have thus not always referred to the same groups of animals. Vernacular words are not ideally suited to scientific use because of their variability in space and time, and because of the imperfect synonymy between names used in various languages (Minelli et al., 2005). Thus, scientists began to develop, as early as the 18th century, precise taxonomies based on names that would ideally have the same meaning for all scientists, no matter when or where they lived. Such developments were becoming increasingly important because of the exponential growth of our knowledge of the biodiversity that resulted from the scientific exploration (in which several biologists took part) of various continents in the 18th century. The Swedish botanist Linnaeus (1707–1778) was the first to propose a comprehensive taxonomy that was widely adopted among scientists. In his system, the names were based on Ancient Greek and Latin roots, an advantage because these dead languages were no longer changing, and because they were widely read by 18th-century

4 / How Can We Reconstruct Evolutionary History?

scientists. (Most of Linnaeus’ works, and even his letters to foreign colleagues, are written in Latin.) To cope with the astronomical number of species to name, he proposed to form names consisting of two words, a genus name and a specific epithet. This constituted a great nomenclatural simplification because species names had grown to Latin descriptions sometimes spanning several lines of text. Thus, our species belongs to the genus Homo and bears the epithet sapiens. Furthermore, each genus belongs to an order, each order belongs to a class, and each class fits into a kingdom. For our species, the taxa of these ranks are Primates (order), Mammalia (class), and Animalia (kingdom). Linnaeus thus used the categories species, genus, order, class, and kingdom that encompass increasingly more inclusive groups. More recently, additional categories (ranks) were introduced, such as the family between the genus and the order. For some ranks, there are now standard endings. Thus, in zoology, taxa at the family rank end in -idae. The stem of the name of a family is always formed by the name of a genus that belongs to the family. Our family name (Hominidae) derives from our genus name (Homo) and the suffix -idae. For subfamilies, the suffix is -inae, and this explains why our subfamily is named Homininae. Using such rules, the following classification of our species can be given: Kingdom Animalia Subkingdom Metazoa Superphylum Deuterostomia Phylum Chordata Subphylum Vertebrata Superclass Gnathostomata Class Mammalia Subclass Eutheria Order Primates Suborder Haplorhini Superfamily Hominoidea Family Hominidae Subfamily Homininae Tribe Hominini Subtribe Hominina Genus Homo Species Homo sapiens

How Can We Reconstruct Evolutionary History? / 5

Species 12

Genus 4 Species 11*

Species 9

Species 8

Genus 3* Species 7*

Species 6

Species 5*

Genus 2 Species 4

Species 3*

Species 2

Species 1

Genus 1*

Family 2

Species 10

Family 1

Figure 1.1. Delimitation of taxa in Linnaean (rank-based) nomenclature. Hypothetical phylogeny of a dozen species. The types are designated by asterisks (*). Type species defi ne genera, and type genera defi ne families.

Well after Linnaeus, taxonomists proposed rules to determine how to apply names; this forms what we call “nomenclature.” Such an explicit nomenclature became necessary in the 19th century because of the very rapid growth in our knowledge of biodiversity (we presently know about 2,000,000 species, and several thousand are added every year). The nomenclature used by most taxonomists is often called “Linnaean” because some of its principles were established by Linnaeus, but it differs by using types, a nomenclatural novelty introduced in the 19th century. Types are either individuals (an animal preserved in alcohol or a skeleton, for instance) used in defi ning species, or taxa of lower rank that are used to defi ne taxa of higher rank. Thus, a genus is defi ned by a type species, and a family is defi ned by a type genus (Fig. 1.1). Because of these additions and the extensive use of ranks, some systematists now prefer the expression “rank-based nomenclature.”

6 / How Can We Reconstruct Evolutionary History?

Delimitation of Taxa in Linnaean (Rank-Based) Nomenclature In rank-based nomenclature, taxa are delimited using their type and rank. A taxon of a given rank cannot be included in another taxon of the same or lower rank (a kingdom contains classes, and the latter contain orders, but not the reverse). This system rests largely on subjective absolute ranks, also called Linnaean categories. Indeed, no objective criterion has ever been used to determine the rank of taxa, except in a few studies (see Laurin, 2005). The geological age of taxa was used a few times to determine ranks, but this practice was soon abandoned because it resulted in drastic changes to the ranks traditionally attributed to most taxa. For instance, several arthropod families are as old as the class Mammalia (which includes all mammals); most mammalian families are no older than several arthropod tribes.

Evolution and Vertebrate Taxonomy: There Are No Fishes Anymore! When Linnaeus proposed his taxonomy, virtually no scientists accepted any sort of theory of biological evolution (Linnaeus was initially a creationist). The theory of evolution by natural selection was proposed, discussed, and accepted (at least by scientists) in the middle to late 19th century. This theory was further elaborated in the 20th century by the discovery of genetic mutations and genetic drift. However, biologists have only recently changed their taxonomies to reflect this scientific revolution, and the rules of rank-based nomenclature have not drastically changed for more than a century. Acceptance of the idea of organic evolution has led biologists to include all descendants of an ancestor in the same taxon as that ancestor. A group thus delimited is objective because it includes species that share a common history and inherited similarities. Such a taxon is called “monophyletic,” as opposed to a “paraphyletic” group (Fig. 1.2A), which

How Can We Reconstruct Evolutionary History? / 7

Taxon 12 Geological time

Taxon 11

Taxon 12

Taxon 10

Taxon 16 monophyletic

Taxon 11

Taxon 9

Taxon 8

Taxon 15 paraphyletic

Taxon 7

Taxon 6

Taxon 5

Taxon 14 paraphyletic

Taxon 3 Taxon 4

Taxon 1 Taxon 2

Taxon 13 paraphyletic

A

Geological time

Taxon 10

Taxon 9

Taxon 8

Taxon 7

Taxon 6

Taxon 5

Taxon 3 Taxon 4

Taxon 1 Taxon 2

Taxon 17 polyphyletic

B Figure 1.2. Monophyly, paraphyly, and polyphyly. Hypothetical example of monophyletic, paraphyletic (A), and polyphyletic (B) taxa. The last common ancestors of lowranking taxa included in higher-ranking taxa 13 to 17 are identified by shaded squares. The content of taxa 13 to 17 is identified by brackets and by shades of gray.

excludes part of the descendants, or a “polyphyletic” group, which contains species that are not closely related to each other (Fig. 1.2B). The taxon Pisces (the “fishes”) is no longer considered valid by most biologists because it excludes some descendants of “fishes,” namely, the tetrapods (Fig. 1.3). Paraphyletic taxa are artificial because their delimitation is arbitrary. They were erected long ago, when biologists classified organisms according to their similarities and along the gaps

8 / How Can We Reconstruct Evolutionary History?

Tetrapods

Dipnoans

Coelacanth

Actinopterygians

(chimeras, sharks)

Chondrichthyans

Lampreys

Hagfishes

“Agnathans”

(sturgeon, salmon, etc.)

“Fishes”

Rhipidistians Sarcopterygians Osteichthyans Gnathostomes Vertebrates Craniates

Figure 1.3. Phylogeny and vertebrate taxonomy. The groups “fi shes” and “agnathans” are paraphyletic, and as such invalid, according to most contemporary taxonomists. All  the other taxa in this figure are monophyletic. The time axis on this diagram is vertical, the past being at the bottom and the present at the top. Thus, each node (bifurcation) of the tree represents the last common ancestor of two taxa.

in biodiversity. Such gaps, found between “fishes” and tetrapods in the extant fauna, result from the extinction of intermediate forms. Fossils can fill these gaps, though only to an extent, because museum collections of fossils represent only a small proportion of the extinct species that once inhabited the Earth. Thus, these gaps are merely artifacts that reflect inadequacies in our knowledge of nature; they do not form justifiable borders between taxa. Indeed, why exclude only the tetrapods from the “fishes”? Why should we not also exclude the lungfishes and the coelacanth as well? The taxon Pisces is paraphyletic (Fig. 1.3), and it is preferable to replace it by a monophyletic taxon issued from the same ancestor, namely, Vertebrata, the taxon that includes all vertebrates. Monophyletic groups are considered natural and can be considered individuals in the philosophical sense: they have an origin (the appearance of the last common ancestor) and an end (the extinction of the last descendant of that ancestor). However, the rank-based codes (that

How Can We Reconstruct Evolutionary History? / 9

Birds

Crocodilians

Sphenodon

Squamates

Turtles

Reptilia

Mammals

Anurans

Urodeles

Gymnophionans

Ichthyostega

Tristichopterids

Dipnoans

Amphibia

Amniota

Traditional taxonomy “Fishes” “Amphibians” “Reptiles” Mammals Birds

Tetrapoda Stegocephali Tetrapodomorpha Rhipidistia

Figure 1.4. Phylogeny and sarcopterygian taxonomy. The traditional taxonomy, including paraphyletic taxa (between quotation marks), is indicated by shades of gray; the more recent delimitation of the taxa Amphibia and Reptilia is indicated by brackets above the tree. The famous sarcopterygian Eusthenopteron is a tristichopterid; the gymnophionans (caecilians) are limbless tropical amphibians; the squamates include the “lizards” (a paraphyletic group) and the snakes. The time axis is vertical, with the past at the bottom and the present at the top. The nodes (bifurcations in the tree) represent the last common ancestors of pairs of taxa.

presently rule the application of taxon names) do not require that taxa be monophyletic; paraphyletic and even polyphyletic taxa are allowed. Taxonomy has been deeply transformed by the application of these principles. For instance, it was once customary to divide the limbed vertebrates (often called tetrapods, but called stegocephalians in this book) into amphibians, reptiles, birds, and mammals, but the fi rst two of these groups are paraphyletic (Fig. 1.4). Today, some authors want to eliminate all names of paraphyletic taxa, such as Reptilia (which traditionally includes the turtles, snakes, and crocodilians, but not the birds, which are nevertheless the closest relatives of the crocodilians in the extant fauna), whereas others prefer to re-delimit these taxa to make them monophyletic. Under this latter approach, Amphibia no longer

10 / How Can We Reconstruct Evolutionary History?

includes the first limbed vertebrates, such as the Devonian genus Ichthyostega (360 Ma old), because the latter are not more closely related to the extant amphibians (frogs, toads, salamanders, etc.) than to the mammals. The taxon Reptilia can be made monophyletic by excluding the “mammal-like reptiles” (stem synapsids) and including the birds (Fig. 1.4), as advocated by some authors.

Phyloge ne tic Nomenclature Taxonomy is currently undergoing a revolution in an attempt to make biological classification less ambiguous. Use of rank-based nomenclature is increasingly unsatisfactory because taxa are delimited under that system through the use of a type and a rank (a Linnaean category, such as species, genus, or family). Since these ranks are subjective, taxonomists can—and often do— change them at will. This system also allows new taxa to be erected (to encompass the same species or individuals) and established taxa to be suppressed (by declaring them synonyms) without requiring an objective basis for any such decisions. Understandably, this results in great taxonomic instability, even if the evolutionary tree (the phylogeny) is stable. In other words, even if our ideas about the evolution of a taxon are stable (in the long term this is admittedly an idealized scenario), the classification of this taxon can be unstable, simply because taxonomists are free to expand or reduce the membership of taxa. This problem can be illustrated by an example using the origin of mammals (Fig. 1.5). The formal name of the taxon that includes all mammals is Mammalia. This name was used by Linnaeus, who knew only placental mammals (Placentalia) and one marsupial (Marsupialia), the Virginia opossum (1). Later, we discovered monotremes, which lay eggs (unlike other mammals) but possess mammary glands. Mammalia was then expanded to encompass the monotremes (2). With the subsequent discovery of fossils similar to extant mammals, Mammalia was further expanded (3 to 6; most commonly 4 in recent times), although some authors advocate a return to an older meaning of this

Figure 1.5. Delimitations of the taxon Mammalia in rank-based nomenclature. The smallest clade that includes all extant mammals is shaded. The last common ancestor of the clades that have been called Mammalia in various studies are identified by numbered gray circles. The sign “+” designates extinct taxa. The reptiles, the mammals’ closest extant relatives, are highlighted in a gray rectangle. Modified from Rowe and Gauthier (1992).

12 / How Can We Reconstruct Evolutionary History?

word (2, or occasionally even 1). Other authors extend the taxon Mammalia to encompass a much larger clade (7 to 10), although they fortunately represent a small minority. This problem, far from affecting only the taxon Mammalia, results from the application of principles of rank-based nomenclature (see the box titled “Instability in rank-based nomenclature”), which were proposed in the 18th and 19th century, when most taxonomists considered taxa to be classes in the philosophical sense of the word. Classes can be defi ned by intrinsic properties that are both necessary and sufficient for an element to belong to this class. For instance, tetrapods possess four limbs, as suggested by their name, and this could be viewed as the defi ning property of the class Tetrapoda. However, many contemporary systematists think that taxa are individuals in the philosophical sense of the word, since they have a beginning (the appearance of a clade) and an end (the extinction of the clade) in time. Because taxa evolve, their members do not necessarily share intrinsic properties (Ereshefsky, 2007). Thus, snakes and caecilians are tetra-

Instability in Rank-Based Nomenclature The inherent instability in taxon delimitation under rank-based nomenclature can be illustrated by a hypothetical example (shown below) of a taxon including four species (a to d), initially attributed (by the first taxonomist who worked on this group) into two genera (E and F) and a single family (Eidae). Since determination of the rank (Linnaean category) of taxa is subjective, the rank of any taxon can be changed for subjective reasons (such as personal preference) and result in taxonomic changes that do not reflect objective discoveries. A taxonomist can declare that genus F is invalid because he considers the species that it includes not sufficiently distinct from those included in genus E; he then declares genus F a ju nior synonym of E, thus abolishing it. On the other hand, he

How Can We Reconstruct Evolutionary History? / 13

may recognize additional genera, which results in yet other taxonomies for the same set of species under the same phylogeny. Finally, he may erect new families, which yields additional alternative taxonomies. All these changes are allowed by the codes of rank-based nomenclature (the zoological, botanical, and bacteriological codes). As a result, even in the absence of any objective reasons to reject the fi rst proposed taxonomy, several alternatives can be proposed and coexist in the scientific literature; all are then simultaneously valid. This makes taxon delimitation ambiguous; for instance, genus E can contain species a, or species a and b, or species a to d. The examples of allowed alternative taxonomies figured here are not exhaustive; see Laurin (2008a) for a more exhaustive list.

Original taxonomy Eidae E* F

Family Genus

Mechanisms

Alternative taxonomies based on the same phylogeny

Synonymy of a genus

Eidae E* a* b c d

a* b c* d Species * Types

Erection of new genera

Eidae E*G F

Eidae E* F H

a* b* c* d a* b c* d*

Erection of new families

Eidae Fidae

EidaeGidae Fidae

E*G F*

E*G* F*

a* b* c* d

a* b* c* d

Types, ranks, and instability in rank-based nomenclature. Rankbased nomenclature cannot stabilize taxonomy, because even without changes to our objective knowledge of nature (such as the discovery of new species or publication of a new phylogeny), taxonomists can suppress taxon names (by putting them into synonymy) or erect new ones. Taxa identified by an asterisk (*) are types.

14 / How Can We Reconstruct Evolutionary History?

Z

A

B

Node-based

Apomorphy-based

M

Branch-based Node Branch

Figure 1.6. Defi nitions of taxon names in phylogenetic nomenclature. The three main kinds of phylogenetic defi nitions of taxon names. A, B, and Z are species or specimens (individuals); M is an apomorphy (derived character state). Modified from Lee (1998).

pods, even though they have lost their limbs, because they are descended from tetrapods. For these reasons, it is preferable to defi ne taxon names using types and the phylogeny. This is analogous to the delimitation of families (in humans) or breeds (of domestic animals), which depends on ancestry (genealogy). To replace rank-based nomenclature (at least above the species level), several systematists have developed a phylogenetic nomenclature. In that system, the taxon name Mammalia could be defi ned (for instance) as the smallest clade that includes monotremes, marsupials, and placentals (Fig. 1.5, node 2). If we wish to discuss more or less inclusive clades than this one, we have to use other names for them (each name must have a single defi nition). Phylogenetic nomenclature should clarify the meaning of taxon names since each name will correspond to a single clade on a given tree. For this reason, it is adopted in this book. It differs from rank-based nomenclature by using at least two types, called “specifiers,” to define taxon names. In phyloge-

How Can We Reconstruct Evolutionary History? / 15

Nodes, Apomorphies, and Branches A node is a point on a tree or on a cladogram that gives rise to two distinct evolutionary lineages. Two nodes are shown in Figure 1.6: one gave rise to species Z and the clade (A, B), and the other is the last common ancestor of species A and B. An apomorphy is a new character state; for instance, apomorphy M is shared by species A and B in Figure 1.6. A branch is a segment located between two nodes (also called an “internode”), or between a node and a terminal taxon (such as species Z, A, and B). For example, a branch links the two nodes shown in Figure 1.6.

netic nomenclature, three main kinds of defi nitions can be given to these names (Fig. 1.6): 1, node-based (for instance, the smallest clade that includes species A and B, in pale gray); 2, apomorphy-based (an apomorphy is a new character state; such a defi nition can be, for instance, the clade delimited by apomorphy M shared with species A, shown in white); 3, branch-based (the largest clade that includes species A but not species Z in dark gray). (See the box titled “Nodes, apomorphies, and branches.”) Contrary to rank-based nomenclature, in phylogenetic nomenclature, the taxonomy is stable if the assumed phylogeny does not change and if we do not discover new species. Only such changes to our objective knowledge of nature can result in changes in taxonomic content. A code of phylogenetic nomenclature, called the PhyloCode, has been developed (Cantino and de Queiroz, 2006). Its development is overseen by the International Society for Phylogenetic Nomenclature (Laurin and Cantino, 2007; Laurin and Bryant, 2009).

16 / How Can We Reconstruct Evolutionary History?

MODERN PHYLOGE NE TICS

Ancestors and Characters From the 19th century to the 1980s, paleontologists searched for ancestors of extant species and higher taxa. This search has not been especially successful, for several reasons. First, only a small proportion of the species that once existed have left fossils. This is hardly surprising because, normally, only mineralized structures (especially skeletons) fossilize. Thus, some taxa, such as slugs and earthworms, normally leave no body fossils. Earthworm burrows may fossilize, and these may enable us to determine that earthworms were present in a given area at a certain time, but such trace fossils yield very little morphological data, so that the identity of the animal that left such burrows is often uncertain. Even taxa that develop a mineralized skeleton may leave no fossils if they live in a habitat unfavorable to fossilization. Most fossils form underwater, in environments characterized by a high sedimentation rate (i.e., where many particles suspended in water are deposited on the substrate), which ensures that carcasses are buried before they are entirely destroyed by carnivores and scavengers. Thus, desert or mountain dwellers are almost unknown in the fossil record. Given the low overall proportion of extinct species represented by fossils, it is likely that fossils of most ancestors of extant and extinct species will never be found. The second reason why few ancestors are known is that most fossils do not represent ancestors of extant or extinct species; instead, they are simply relatives (which, like cousins, are not ancestors) that we call “sister groups” (Fig. 1.7). This is shown by the presence of derived character states in these fossils that should also occur in their descendants, if they were known, but that do not in fact occur in more recent species. Characters describe attributes of taxa; they may be morphological (for instance, they may describe the presence or absence of limbs, their size, or their shape), physiological (e.g., metabolism, ecto- or endothermy, ability to hibernate), behavioral (solitary, gregarious, social, etc.), or molecular (presence or absence of certain genes, number of copies of a

Taxon 1 Taxon 2 Taxon 3 Taxon 4 Taxon 5

Taxon 9

Taxon 6 Taxon 7 Taxon 8

How Can We Reconstruct Evolutionary History? / 17

Geological time Present

Recent past

Real ancestor of 6-8

Distant past

Real ancestor of 2–9

Figure 1.7. Real ancestors, hypothetical ancestors, and sister groups. Taxa 1 to 9 are closely related to each other; thus, taxon 8 is the sister group of taxon 7; together, they form the sister group of taxon 6, and so on. The portions of the evolutionary tree represented by fossils are shown in black; the inferred portions are shown as thin gray lines. Some extinct species are totally unknown (no fossil is preserved, as in taxa 3 and 5). Only two real ancestors are known, but all hypothetical ancestors (gray squares) can be inferred.

gene, insertions or deletions in the genome, substitutions of nucleotides, etc.). They constitute the data that phylogeneticists use to reconstruct the evolutionary tree of life. Even if we had the extraordinary good luck of finding a fossil representing a direct ancestor of an extant taxon, it would be impossible to prove that it is indeed an ancestor, rather than the sister group, because ancestral status can only be shown by a lack of evidence: the absence of unique character states in the ancestor. For all these reasons, most vertebrate paleontologists have stopped looking for direct ancestors and concentrate instead on determining the sister group relationships between extant and extinct taxa. Taxa are considered a priori not to be ancestral to each other, but even if some are, this does not invalidate the approach. The advantage of this

18 / How Can We Reconstruct Evolutionary History?

approach is that it is testable and that it does not rest on absence of evidence, but instead on the discovery of new characters that unite sister groups. For instance, digits are recent structures (compared with fi ns), and this suggests that amphibians are closely related to amniotes (mammals and reptiles), because these taxa all possess digits (Fig. 1.8). Conversely, primitive (old) character states cannot demonstrate relationships, because they have been inherited from an old, distant ancestor. Thus, the presence of fins in sharks, actinopterygians (sturgeons, salmons, etc.), the coelacanth, and dipnoans (lungfishes) does not indicate that these taxa are more closely related to each other than to tetrapods, because the fin is an older structure than the limb. Using such primitive characters to infer the phylogeny of gnathostomes ( jawed vertebrates) would lead to erroneous results (Fig. 1.9). The age of character states is their fi rst appearance on an evolutionary tree, as shown by fossils or inferred by their distribution in extant taxa. A character state is primitive (and not to be used to infer clades) if its appearance precedes the divergence between the taxa whose phylogeny we want to study. Thus, the presence of fi ns cannot be used to study gnathostome phylogeny, because fossils show that the last common ancestor of extant gnathostomes lived at least 430 Ma ago, but fins appeared earlier, in jawless vertebrates, at least 490 Ma ago. However, the presence of limbs with digits in tetrapods (amphibians, mammals, and reptiles) suggests that they form a clade that excludes all fi nned vertebrates because digited limbs appeared about 365 Ma ago, well after gnathostomes. The presence of such limbs can thus be used to assess gnathostome phylogeny. In the context of phylogenetic analyses, we usually consider only the polarity of characters (relative age), rather than their absolute age, which simplifies discussions. Indeed, we often cannot determine the absolute age of character states, especially if they concern soft anatomy, physiology, or behavior and leave no fossils. Similarly, the age of many taxa cannot be determined by fossils, because they lack a mineralized skeleton; examples include slugs and earthworms. The relative age is much easier to determine,

Reptiles

Mammals

Amphibians

Dipnoans

Coelacanth

(sturgeon, salmon, etc.)

Actinopterygians

(chimeras, sharks)

Chondrithchyans

Appearance of digits

Appendage type Fin Limb with digits

Reptiles

Mammals

Amphibians

Dipnoans

Coelacanth

(sturgeon, salmon, etc.)

Actinopterygians

(chimeras, sharks)

Chondrithchyans

Figure 1.8. Phylogeny and character polarity. Phylogeny based partly on the appearance of the limb with digits and showing that the limb is more recent than the fi n and results from a transformation of the latter.

Appendage type Fin Limb with digits

Figure 1.9. Incorrect phylogeny based (in part) on a primitive character state. Incorrect gnathostome phylogeny that would result from using old (primitive) character states (here, fi ns) to infer relationships.

20 / How Can We Reconstruct Evolutionary History?

by looking at the distribution of character states on the tree (widespread characters are generally older than characters with restricted distributions). Old characters are called “primitive,” and recent ones are called “derived.” Determining the status of these character states (in other words, determining the polarity of the character) is called polarizing the character. Character polarity is always relative. Thus, the presence of limbs with digits is derived in the context of an analysis of gnathostomes, but primitive in the context of an analysis of tetrapod phylogeny. In a study of reptilian phylogeny, we could not exclude snakes to form a clade uniting turtles, crocodilians, and birds, because the limb appeared well before the first reptile (which is barely 315 Ma old). In that context, the presence of a limb is a primitive character. Conversely, the presence of limbs is derived (hence phylogenetically useful) in the context of metazoan phylogeny because the first metazoans (multicellular animals) are older (550 Ma) than the first fins. Therefore, the chondrichthyans and the actinopterygians can be grouped into the gnathostomes, whereas the echinoderms, mollusks, and arthropods can be excluded, based on the presence or absence of fins in these taxa. Generally, character polarity is assessed through outgroup comparison. The outgroup must be fairly closely related to the taxon whose phylogeny we want to study, but it must not be part of it. Thus, to study sarcopterygian phylogeny, actinopterygians can be used as an outgroup (Fig. 1.3). The character state found in the outgroup and in part of the ingroup (the group whose phylogeny we want to study; sarcopterygians in this example) is generally primitive, whereas character states found only in part (or all) of the ingroup are generally derived. This criterion enables us to establish that, for the character “appendage type,” the state “fin” is primitive (because it is found in actinopterygians and in some sarcopterygians) whereas the state “limb” is derived (Fig. 1.8), because it occurs only in some sarcopterygians. The phylogenetic relationships that can be established through parsimony specify only a topology, which is information about the relative kinship of taxa. Figures 1.8 and 1.9 represent topologies (cladograms).

How Can We Reconstruct Evolutionary History? / 21

By itself, the topology does not yield the geological age of taxa. On the contrary, a phylogeny (Fig. 1.7) incorporates a topology and additional data represented by branch lengths (which usually represent evolutionary time).

Parsimony and Reconstruction of Character Evolution It is impossible to read the history of characters directly, even when their evolution is documented in a fairly rich fossil record. This history must nearly always be inferred using various methods. Before the advent of cladistics in zoology in the 1970s and 1980s, paleontologists inferred these events mentally, each in their own way, and often without providing the data on which their reasoning was based. In 1950, the German entomologist Willi Hennig proposed a new method, cladistics. Cladistics can be used to infer character history based on parsimony, a principle that is used in various ways in all sciences, since it rests on the principle that as few hypotheses as possible must be made to explain data (and these hypotheses should be as simple as possible). For instance, if the relationship between two variables (between temperature of a gas, for example, and its volume at a given pressure) is tested for three values, and if the three data points seem to line up (Fig. 1.10, black circles), we always infer a linear relationship between these variables (Fig. 1.10, black line), even if other relationships can also explain these data (Fig. 1.10, gray lines). Why? Simply because the linear relationship is the simplest, since it requires estimating only two constants, “a” and “b” in the following equation, where X and Y represent the variables): Y = aX + b The other relationships (Fig. 1.10, gray lines) could be represented by more complex equations that require estimating more variables. The latter would be invoked only if further research yielded data that suggest that a more complex model is required (for example, the gray circle in

Variable 2 (Y )

22 / How Can We Reconstruct Evolutionary History?

Variable 1 (X ) Figure 1.10. Principle of parsimony in science. If three data points (in black) document the relationship between two variables, and seem to line up, we always infer a linear relationship (black line). Other relationships are possible (gray lines), but they are chosen only if discovery of additional data require it. The gray circle suggests that the dark gray line fits the data better than the straight black line.

Figure 1.10 suggests that the dark gray line is more adequate than the black straight line). Parsimony, when used to study character evolution, simply stipulates that we must infer as few character transformations as possible to explain the distribution of its states. This does not imply that the most parsimonious pattern is the true one (one might say that Nature is not necessarily parsimonious), but if evolution has followed a more complex pattern, more data and further analyses can potentially demonstrate it. Thus, the distribution of the character on the tree of Figure 1.11 suggests that the state “dark gray” appeared twice and that the state “light gray” is older, because this history implies only two character transformations (two appearances of the state “dark gray,” as shown in Figure 1.11A). Other hypotheses could be made, but they are all more complex; they require at least three transformations (Fig. 1.11B). The procedure to infer the history requiring the lowest possible number of steps in a character is called “parsimony optimization.” Since we infer that the state “light gray” is older than the state “dark gray,” we conclude that the fi rst one is primitive and

Taxon 7

Taxon 6

Taxon 5

Taxon 4

Taxon 3

Taxon 2

Taxon 1

How Can We Reconstruct Evolutionary History? / 23

Taxon 7

Taxon 6

Taxon 5

Taxon 4

Taxon 3

Taxon 2

Taxon 1

A

B Figure 1.11. Parsimony and character evolution. Given the character distribution and the phylogeny, hypothesis A is simpler because it requires only two transformations. Any other hypothesis, such as shown in B, requires at least three transformations, and will not be discussed further.

the second derived. A derived state is what we call an apomorphy. When it is shared by at least two taxa that inherited it from a common ancestor (like the state “dark gray” in taxa 6 and 7 in Figure 1.11A, or the appearance of digits in amphibians, mammals, and reptiles in Figure 1.8), we call it a synapomorphy of those taxa. When it is present in a single taxon, such as feathers in birds in Figure 1.4, we call it an autapomorphy of that taxon. A primitive character is often called a plesiomorphy (such as the state “light gray” in Figure 1.11A), and it must

24 / How Can We Reconstruct Evolutionary History?

not be used to infer the existence of clades, because this would often result in errors (Fig. 1.9).

Evolutionary Trees: Intuition, Parsimony, and Evolution The evolutionary history of taxa cannot be read directly from the fossil record, even when fossils are abundant; just like for characters, the history of taxa must be inferred. For a long time, paleontologists and other systematists tried to reconstruct that history using global (unpolarized) similarity. This method went out of fashion (for good reasons) with the introduction of cladistics, which uses the principle of parsimony; it was initially developed by Hennig (1950, English translation 1965), and has been in use by other systematists since the 1970s (in some field). Cladistics can be used to infer both character history and phylogeny. The trees that imply the fewest character transformations must be preferred, just as we saw for character histories. For n taxa, at least n – 2 characters with at least two states are required to get a fully resolved phylogeny, since each node needs to be justified by at least one character-state transformation (Fig. 1.12). We also need to know, before we begin the analysis, which of the taxa is the most distantly related to the others (this is the outgroup, as opposed to the ingroup). The identification of the outgroup rests on prior knowledge. For instance, if we wanted to determine the relationships among amphibians, mammals, and reptiles among tetrapods, and if we already knew that lungfishes and the coelacanth are closely related to tetrapods, we could choose lungfishes, the coelacanth, or both, as the outgroup. It is generally advisable to choose the outgroup that is most closely related to the ingroup, although this is not strictly necessary. However, the outgroup must never be part of the ingroup (i.e., it must never be more closely related to part of the ingroup than to another part), or the results will be erroneous. Since most evidence suggests that the lungfishes are

How Can We Reconstruct Evolutionary History? / 25

Table 1.1. Data Matrix Character 1, limb type: a, fi n; b, limb (with digits). Character 2, skin permeability: a, great; b, small.

Taxon Lungfishes

Character 1

Character 2

a

a

Amphibians

b

a

Mammals

b

b

Reptiles

b

b

Table 1.2. More Complex Data Matrix Containing Some Convergence Taxon

Character 1

Character 2

Character 3

Character 4

Lungfishes

a

a

a

a

Amphibians

b

a

a

b

Mammals

b

b

b

b

Reptiles

b

b

b

a

more closely related to the tetrapods than to the coelacanth, lungfishes would be the preferred outgroup. It would nevertheless be possible to choose the coelacanth, but under no circumstance could urodeles (salamanders, a group of amphibians) be selected, because they are tetrapods and therefore are more closely related to one part of the ingroup (in this case, frogs and other amphibians) than to another (mammals and reptiles). After having established the list of taxa (ingroup and outgroup) and characters, we have to code the data matrix, which could look like Table 1.1. This matrix suggests the tree shown in Figure 1.12, because this tree requires a single transformation for each character. On the contrary,

26 / How Can We Reconstruct Evolutionary History?

the tree in Figure 1.13 requires two transitions for one of the characters (skin permeability); it is less parsimonious and so we prefer the tree shown in Figure 1.12 for further testing. This very simple demonstration hides a far more complex reality. Most analyses include dozens of taxa and many more characters; therefore, fi nding the most parsimonious tree requires computers and sophisticated software such as PAUP* (Swofford, 2003). The presence of convergence often makes analysis fairly difficult because no tree requires a single transformation for each character, but we must still minimize the number of assumed evolutionary steps. For instance, the matrix in Table 1.2 would result in the tree shown in Figure 1.12, but note that character 4 requires at least two steps on that tree. So far, only morphological or physiological characters have been discussed, but, for more than a decade, phylogenetic analyses have been performed most frequently on molecular data, particularly on DNA and RNA sequences, and, less frequently, on amino acid sequences. Furthermore, to keep the discussion simple, only parsimony has been presented, but most recent phylogenetic analyses of molecular data use more complex methods (which do not, however, necessarily guarantee more accurate results), such as maximum likelihood and Bayesian analysis (Huelsenbeck et al., 2001).

Dating Taxa paleontological dating For a long time, the age of taxa was determined almost exclusively using the fossil record. Indeed, what simpler method than using fossils to date the appearance of taxa could we devise? Unfortunately, fossils cannot provide complete information about the age of taxa, because only a small proportion of species, and a small proportion of the temporal range of each species, are represented in the fossil record (Fig. 1.14). To determine if paleontological data are

Reptiles

Mammals

Dipnoans

Amphibians

How Can We Reconstruct Evolutionary History? / 27

Ch. 4, ta 1.2

Geological time

Water-proofing of the skin

Appearance of the limb with digits

Geological time

Mammals

Reptiles

Amphibians

Dipnoans

Figure 1.12. Most parsimonious tree. Shortest tree for the data matrices (Tables 1.1 and 1.2). Ch. 4, ta. 2, Convergent appearance of character 4 from Table 1.2 on this tree.

Waterproofing of the skin Appearance of the limb with digits

Figure 1.13. Less parsimonious tree. Less parsimonious phylogeny for the same data matrices (Tables 1.1 and 1.2).

reliable for dating taxa, various indices of stratigraphic fit have been developed. Some of these indices use the congruence between the expected order of appearance of taxa (based on the topology of the tree) and the observed order of appearance of taxa as shown by fossils. For instance, according to Figure 1.14, taxon 2 must have appeared before

n5 n3

n4

n6 n5 n2 n3

n2

A

B

Main periods

FS X + 7

MP X + 2

Taxon 8

t8

t7 FS X + 6

t6 n7

n8 FS X + 5

n4

t5 n6 n5 n2 n3

n1

n1

Taxon 9

Taxon 6 Taxon 7 Taxon 2 Taxon 3 Taxon 4 Taxon 5

n8

Finer scale

FS X + 8

n1

C

FS X + 4

n4

MP X + 1

n7

n7

Taxon 1

Taxon 2 Taxon 3 Taxon 4 Taxon 5

n8

Taxon 1

Taxon 1

MIG

n6

Taxon 9 Taxon 8

Taxon 2 Taxon 3 Taxon 4 Taxon 5

Taxon 8

Taxon 6 Taxon 7

Taxon 9

Taxon 6 Taxon 7

Geological time scale

FS X + 3 FS X + 2 FS X + 1

MP X

t4

FS X

Figure 1.14. Paleontological dating. Fossils can be used to determine the minimal age of taxa. However, except if a mistake is made, this age will always underestimate the (generally unknown) true age of taxa. The true phylogeny (A) is imperfectly known because only a small fraction of its lineages is represented in the fossil record (bold black lines). If we possess temporal data of the order of resolution of the fi ne scale (FS X to FS X + 8), and if we consider that each fossil occurs at the end of the time subdivision in which it occurs, we will underestimate the geological age of the taxa (B). Note that use of a fi ner temporal scale would not solve this problem. Even an error-free, extremely precise dating of fossils does not resolve the problem of underestimation of the age of taxa according to the fossil record. If we consider that each species occupies an entire temporal subdivision (C), we no longer estimate a minimal age, but we may still underestimate the age of some taxa (n2, 5, 7), whereas the age of other taxa (n1, 3, 4, 6, 8) is overestimated. This dating method is less biased than using the minimal age of each fossil, and its precision increases with the resolution of the temporal scale used. The MIG (“Minimum Implied Gap,” or ghost range) of taxon 6 is shown in the true phylogeny (A); the MIG of a tree is the sum of MIGs of all the taxa (1 to 9, plus the clades that include these terminal taxa).

t3 t2 t1 t0

How Can We Reconstruct Evolutionary History? / 29

taxon 3, and the fossil record is congruent. On the contrary, taxon 6, which should appear before taxa 7 and 8, appears after them, according to the fossil record, and this implies a long ghost range (a temporal extension of a taxon beneath the lowest stratigraphic level in which it is represented by fossils; it is usually inferred because its sister group is older). Other indices estimate the minimal length of branches unrepresented by fossils, the “Minimum Implied Gap” (MIG), which indicates the minimal proportion of missing data in the fossil record. In all cases, for these measures to be useful, they must be compared with a null distribution of the same index produced by a large number of randomized datasets. Such data sets are produced by randomly permuting the observed ages of taxa (assessed through the fossil record) over the tree a large number of times (typically, a thousand or ten thousand times). Thus, if the stratigraphic fit over the reference tree is better than in at least 95% of the randomized datasets, we can conclude, with a 5% probability of being wrong, that there is a genuine correlation between the predicted and observed order of appearance of taxa (we reject the null hypothesis that no relationship exists between both orders). This conclusion suggests that the paleontological data are reliable. If we cannot reject the null hypothesis (if at least 5% of the randomized datasets display as good a stratigraphic fit as the original data), paleontological data presumably do not provide a reliable estimate of the absolute and relative age of taxa. A computer program can compute these indices and create a null distribution based on randomized datasets through permutations (Wills, 1999). Of course, this method rests on the assumption that the age of the fossils was not used to infer the topology of the tree, and that the latter is reliable. This technique was recently used (Fig. 1.15) to show (by comparison with the results of other methods) that paleontological data provide a reliable estimate of the age of lissamphibian taxa (Lissamphibia is the smallest clade that includes extant amphibians).

Rhinophrynidae

Rhadinosteus parvus Shomronella jordanica Cordicephalus gracilis Cordicephalus longicostatus Palaeobatrachus grandipes Palaeobatrachidae Pliobatrachus langhae Villeveyrac paleobatrachid Avitabatrachus uliana Thoracociliacus rostriceps Saltenia ibanezi Shelania pascuali Llankibatrachus truebae Silurana Xenopus arabiensis Xenopus laevis Eoxenopoides reuningi Vulcanobatrachus mandelai Pachybatrachus taqueti Hymenochirus Pipa Neusibatrachus wilferti Xenopodinae

Pipimorpha

Xenoanura Pipoidea Pipanura Anura

Bombinanura

Coniacian Turonian Cenomanian Albian

112.0 Aptian 125.0 130.0 136.4 140.2 145.5 150.8 155.7 161.2 167.7 171.6 175.6 183.0 189.6 196.5 199.6

Barremian Hauterivian Valanginian Berriasian Tithonian Kimmeridgian Oxfordian Bathonian Aalenian Toarcian Pliensbachian Sinemurian Hettangian

Paleogene Cretaceous

Pipidae

Campanian 83.5 89.3 93.5 99.6

Jurassic

Xenopodinomorpha

0 5.332 Pliocene 11.608 Tortonian 15.97 Burdigalian 23.03 28.4 Chattian 33.9 Rupelian 40.4 Bartonian Lutetian 48.6 55.8 Ypresian Thanetian 61.7 65.5 Danian 70.6 Maastrichtian

Neogene

Pipinae

Pelobatoidea + Neobatrachia (fig. 6)

Eodiscoglossus oxoniensis Eodiscoglossus santonjae Callobatrachus sanyanensis

Discoglossidae

Prosalirus bitis Notobatrachus degiustoi Yizhoubatrachus macilentus Vieraella herbstii Mesophryne beipiaoensis

Pipinomorpha

Bombina orientalis Bombina variegata Bombina sp. Opisthocoelellus weigelti Opisthocoelellus hessi ?Latonia sp. Latonia vertaizoni Latonia cf. L. gigantea Alytes obstetricans Alytes cisternasii Alytes sp. Discoglossus troscheli Discoglossus galganoi Discoglossus sardus Discoglossus occipitalis Rhinophrynus dorsalis Rhinophrynus canadensis Chelomophrynus bayi Eorhinophrynus septentrionalis

Amphicoela

Notobatrachidae

Ascaphus + Leiopelma

Discoglossoidea

Figure 1.15. Time-calibrated supertree of Anura and its closest relatives. This phylogeny incorporates data on topology and on stratigraphy, based on several sources. It was compiled using new software that facilitates the compilation of paleontological trees incorporating stratigraphic information. In that tree, each taxon occupies at least a whole geological stage. For instance, Prosalirus bitis (to the left) occupies the Pliensbachian (from 189.6 to 183 Ma). Each internal branch had a minimal length of 3 Ma. Modified from Marjanovic and Laurin (2007).

How Can We Reconstruct Evolutionary History? / 31

molecular dating Paleontological data are fairly easy to use to estimate the age of taxa, but what can be done when a taxon has little or no fossil record? This fairly common situation prevails in soft-bodied taxa lacking a mineralized skeleton, such as annelids and nematodes. Even in taxa with a rich fossil record, gaps may result in serious underestimation of the age of various clades. Thus, even though vertebrates are well represented in paleontological collections, taxa restricted to mountainous areas have left virtually no fossils. This is why other sources of data may be very useful for dating taxa. Since the 1990s, molecular data have been increasingly used to date the origins of taxa. The first methods rested on the hypothesis of a global molecular clock, which assumed that DNA substitutions accumulated at a steady, constant rate in all taxa and at all times. If we know at least one divergence date within a clade (usually through the fossil record, but occasionally using geological data, such as the separation of continental plates), we can then estimate other dates using molecular data, assuming that molecular distances (the proportion of nucleotides that differ) are proportional to divergence dates (Fig. 1.16). The known divergence date (which is not estimated using molecular data) is called a calibration date or calibration constraint. Two types of calibration dates are known: internal and external. Internal calibration dates occur within the clade that we want to date (Fig. 1.16, IC1–2). External calibration dates occur outside the taxon whose age is to be estimated (Fig. 1.16, EC). The hypothesis of a global molecular clock is occasionally useful, but this is mostly in noncoding portions of the genome (which do not code for proteins and do not regulate gene expression), so most phylogenetically informative data do not fit this model. In the simplest possible case, if the data fit the molecular clock model, the simplest method is to estimate the rate of molecular evolution and to divide the molecular distances by this rate to obtain the ages of

32 / How Can We Reconstruct Evolutionary History?

Tetrapoda

Anura IC2

IC1

Gymnophiona

Lissamphibia Mammalia

Aves

Dipnoi

Amniota

250 MA

310 MA

?

EC

410 MA

Figure 1.16. Molecular dating. We wish to estimate the divergence date between lissamphibians and amniotes; this is the date of origin of tetrapods. In this phylogeny, we know from the fossil record two internal calibration dates (IC1 and 2), which are the divergence between birds and mammals (at least 310 Ma) and the divergence between gymnophionans and anurans (at least about 250 Ma). We also know an external calibration date (EC), which is not used in this example but could be (even though its age is not as precisely known).

nodes. Thus, in the tree shown in Figure 1.16, and using the data in Table 1.3, the molecular evolutionary rate can be estimated at about 0.000341 substitutions/site/Ma. This is the average value of two evolutionary rates that can be computed: 0.09/250 for lissamphibians and 0.10/310 for amniotes. We could then infer the divergence date between lissamphibians and amniotes by dividing the divergence between each pair of taxa including a lissamphibian and an amniote (Anura/ Aves, Anura/Mammalia, Gymnophiona/Aves, and Gymnophiona/ Mammalia) by this rate, which yields an average age of 344 Ma. Since the molecular evolutionary rate differs slightly between branches, the estimated ages range from 322 to 381 Ma, but this hypothetical example fits the molecular clock hypothesis nicely (real applications are always more complex than this).

How Can We Reconstruct Evolutionary History? / 33

Table 1.3. Hypothetical Molecular Distance Matrices Showing the Proportion of Divergent Nucleotide Sites Taxa

Anura

Gymnophiona

Aves

Mammalia

Anura

–

0.09

0.12

0.11

–

0.11

0.13

–

0.10

Gymnophiona Aves Mammalia

–

NOTE: This proportion can range from 0 (no difference, which normally occurs only within a small part of the genome and often only within a given species) to 1 (no similarity, a value never reached since there are only four nucleotide types, so we always expect a distance inferior to 0.75). The distance between a taxon and itself is always 0, so the diagonal is represented by dashes (–). Since the matrix is symmetrical (the distance between A and B is the same as between B and A), only half the matrix (without the diagonal) needs to be shown. In this example, only internal calibration dates have been used, but similar calculations could be performed using the external calibration date.

The quartet dating method (Rambaut and Bromham, 1998) is more realistic and was widely used in the late 1990s. This method can use two calibration dates and estimates two evolutionary rates (one per date). Thus, in the example shown in Figure 1.16, the method estimates separately evolutionary rates for amniotes and for lissamphibians. These two evolutionary rates are then used for the three branches to the left, and the three branches to the right of the last common ancestor of tetrapods (identified by a question mark on the figure). This method allows moderate deviations from the global molecular work, since it only requires that the evolutionary rate be constant within each of the two clades on each side of the node whose date we want to estimate. It incorporates an evolutionary model estimated from the sequences (using different software), and this allows for a more precise branch-length estimate accounting for multiple substitutions. This is useful because successive substitutions at a site may result in a return to the initial state; for instance, a site initially occupied by an adenine can be occupied by a thymine, and then switch back to adenine. Without an evolutionary

34 / How Can We Reconstruct Evolutionary History?

model, we would always conclude, in such cases, that no change has taken place, whereas in fact two changes took place but resulted in identical initial and terminal states. Quartet dating is now rarely used because several more sophisticated methods have been developed. Among these methods, we find Penalized Likelihood (PL), which can use several calibration points simultaneously, and these can be both internal and external (Sanderson, 2002). Furthermore, uncertainty about these dates can be incorporated into the analysis. Indeed, quartet dating uses calibration dates as if they were known without error, but PL allows specification of lower and maximal values of calibration ages. Thus, the divergence date between birds and mammals is not really 310 Ma ago; instead, it is comprised within the interval between 310 and 345 Ma ago (Marjanovié and Laurin, 2007). For some calibration points, it is possible to specify only a minimal age, for others, only a maximal age, or, finally, both can be specified for a given event. This method rests neither on the unrealistic hypothesis of a single, global evolutionary rate nor on two rates; it allows the evolutionary rate to be estimated for each branch, although this rate depends on the rate of neighboring branches (the degree of this dependency can be estimated from the data). Other methods at least as sophisticated as PL exist. Some are based on a Bayesian approach, but they fall outside the scope of this introduction to molecular dating. A good review of these methods and relevant software was recently published (Rutschmann, 2006). comparison between paleontological and molecular ages Several molecular studies have dated the diversification of life (e.g., Kumar and Hedges, 1998). A strange but widespread phenomenon is that estimated molecular ages are in most cases considerably older than minimal paleontological ages. Several molecular biologists explain this discrepancy by invoking gaps in the fossil record. On the contrary, several paleontologists blame simplifying assumptions made in the

How Can We Reconstruct Evolutionary History? / 35

estimation of molecular ages, and important variations in molecular evolutionary rates between taxa and in time. A partial explanation of this discrepancy lies in the choice of calibration dates. Brochu (2004) showed that molecular ages estimated by quartet dating are proportional to the age of the calibration points used. His demonstration was based on sequences of five mitochondrial genes of crocodilians, a group represented by a rich fossil record that gives reliable data on the true ages of various clades. Thus, using recent calibration points (less than 20 Ma) to estimate the divergence date between crocodilids (crocodiles in the strictest sense) and alligatorids (alligators and caimans) yielded estimates more recent than the age of the oldest fossils (78 Ma) that belong to those clades. The age of this divergence was estimated at less than 30 Ma in some cases, which clearly reveals a major problem in the method. Conversely, using ancient calibration points (more than 50 Ma old) overestimated the age of this divergence, which was sometimes estimated at more than 200 Ma; this is not plausible given our knowledge of the fossil record of crocodiles and the fauna that lived 200 Ma ago. These problems do not affect only quartet dating. It is probable that they affect all molecular dating methods, since Marjanovié and Laurin (2007) showed a similar phenomenon using PL. This would explain the huge age difference between some molecular and paleontological estimates of the age of Lissamphibia (Fig. 1.17): the very old ages inferred by Zhang et al. (2005) were based only on two very old external calibration dates. Molecular ages compatible with the paleontological estimates can be obtained if ancient external and more recent internal calibration dates are used simultaneously, and if both minimum and maximum bounds are specified for at least some calibration dates. Unfortunately, many molecular biologists are reluctant to accept paleontological evidence about maximum ages for clades and only use minimum bounds for most calibration dates, which results in biased, inflated ages (Marjanovié and Laurin, 2007).

Rana Polypedates

Bombina Xenopus Bufo Hyla Microhyla Kaloula

Amniota Typhlonectes Ichthyophis Paramesotriton Mertensiella Ranodon Andrias

Rana Polypedates

Bombina Xenopus Bufo Hyla Microhyla Kaloula

Amniota Typhlonectes Ichthyophis Paramesotriton Mertensiella Ranodon Andrias

36 / How Can We Reconstruct Evolutionary History?

Geological time scale Neogene 23.0

N/A

97 (81, 115)

115 (95, 135) 142 (123, 162)

Neobatrachia 173 (152, 195)

Apoda

Neobatrachia

101 (94, 101)

108 (72, 129)

138 (131, Urodela 138)

Apoda 250 (224, 274)

145.5 Jurassic

165 (152, 171)

162 Bombinanura 174 (166, 190) (152, 166)

199.6 Triassic

Urodela 197 (176, 219)

65.5 Cretaceous

250 (226, 274)

251.0 255 (246, 257)

Lissamphibia 261 (246, 267)

Bombinanura 290 (268, 313) 308 (289, 328)

Lissamphibia 337 (321, 353) 354 (341, 367)

A

B

Late Middle

260.4 270.6

Early 299.0

Pennsylvanian

318.1

Mississi.

158 (135, 181)

96 (81, 113)

58 (34, 74)

Dev Carboniferous Permian

139 (119, 160)

99 (72, 101)

70 (57, 84)

46 (33, 54)

Paleogene

Viséan

345.3 Tournaisian 359.2

Famennian 374.5

Figure 1.17. Age of lissamphibian diversification. Age of Lissamphibia inferred from mitochondrial data by a Bayesian approach (A), and minimum age estimated by the fossil record (B). The molecular ages include credibility intervals (in parentheses). For paleontological ages, the numbers in parentheses represent the minimal ages implied by various hypotheses about minimal branch lengths. These are not true confidence intervals. Note that the molecular ages are systematically older than the paleontological ages, and that the latter fall outside the credibility intervals of the molecular ages (represented by rectangles). Modified from Marjanovic and Laurin (2007).

After an initial period of unrealistic euphoria, during which numerous scientists thought that molecular dating would enable us to easily date the whole tree of life, we have entered a period of greater realism. Some molecular biologists have strongly criticized the molecular approach and even argued that it should be dropped completely (Shaul and Graur, 2002; Graur and Martin, 2004). Others have discussed the

How Can We Reconstruct Evolutionary History? / 37

difficulty in estimating time from branch lengths (Britton, 2005). Indeed, molecular distances yield branch lengths, but these lengths depend on both the rate of evolution (which is unknown) and time (also unknown). This means that if only a small proportion of taxa can be dated using fossils (or other geological data), even very long molecular sequences will not necessarily result in very reliable molecular ages. However, as the dating methods become more sophisticated, as the number of available sequences and sampled species increases, and as new calibration dates become available, these methods will become more reliable and lead to plausible results (e.g., Zhang et al., 2008).

HOMOLOGY AND ANALOGY: LUNGS, SWIM BLADDERS, AND GILLS

Organs of animals often resemble each other in their structure, embryonic origin, and function, but these similarities can result from at least two very different processes. If the similarity results from a shared evolutionary origin, we call these organs homologous, whereas if it results from convergence (independent origin), the organs are analogous. Convergence often arises from the development of organs that perform similar functions in various taxa. An example of homologous organs is provided by the lung and the swim bladder (Fig. 1.18). The latter exists in teleosts (a taxon that includes most actinopterygians, such as the trout, salmon, and swordfish, among tens of thousands of others) and is a median air-filled structure located against the dorsal wall of the thoracic cavity. By varying the amount of gas in this bladder, teleosts can regulate its volume and, hence, their body density, which enables them to move up or down the water column with minimal energy expenditure. This organ only remotely resembles the tetrapod lung, which is paired (there is a left and a right lung), ventral, and is mostly involved in breathing. Yet, the teleost swim bladder is homologous with the tetrapod lung, despite the differences in function, position, and morphology. In other words, the last

38 / How Can We Reconstruct Evolutionary History?

Figure 1.18. Lung and swim bladder. Lung and swim bladder in transverse section, seen from the front (to the left) and in lateral view (to the right). In all these taxa except in teleosts (A), the lung or swim bladder is involved in gas exchange. In most teleosts, the connection between the swim bladder and the esophagus has disappeared. The oxygen is brought to and removed from the swim bladder by the blood. The phylogeny is shown on the left. Redrawn from figure 3.4 (p. 71) of Graham (1997). PARTS: A, typical teleost with swim bladder. B, the teleost Erythrinus. C, Lepisosteus and Amia. D, Polypterus and Erpetoichthys. E, the dipnoans (lungfishes) Lepidosiren and Protopterus. F, tetrapods.

common ancestor of tetrapods and teleosts already possessed a structure that gave rise to the tetrapod lung and the teleost swim bladder. We have evidence that this organ was a relatively simple lung (Fig. 1.18). As examples of analogous organs, the lung and gills may be mentioned. Gills of primitively aquatic vertebrates (sharks, trout, etc.) are the main organ for gas exchange (although they are also involved in osmoregulation), just like the tetrapod lung. Thus, gills and lungs perform the same function. However, their evolutionary origin differs, as shown by the presence of both lungs and gills in dipnoans (the presence of both organs in a species proves that they are not homologous),

How Can We Reconstruct Evolutionary History? / 39

and by the numerous anatomical and developmental differences (for instance, gills are outgrowths of the aortic arches, whereas lungs are outgrowths of the pharynx). This is why lungs and gills are analogous structures.

GEOLOGICAL TIME SCALE AND THE CHRONOLOGY OF A FEW KEY EVENTS

Since the 19th century, geologists have been mapping geological strata on our planet, trying to establish the relative age of rocks. This chronology is based (at least for sedimentary rocks) on the principle of superposition (generally, the lowest, deepest strata are the oldest, because successive strata are laid on top of each other), on the fossil record, and, since the 20th century, on radiometric methods that can yield absolute ages (in millions of years) of certain rocks. We have thus established that the Earth is about 4.56 Ga (billion years) old, and that life probably appeared more than 3 Ga ago, even though fossils are extremely rare before the Cambrian, which started a measly 542 Ma ago according to the latest dating. The geological times were thus divided into the Cryptozoic (which means “hidden life”), also called the Precambrian (both terms are informal and refer to the formal eons Archean and Proterozoic), and the Phanerozoic (which means “visible life”). This means that only the last 12% of the Earth’s history, and at most 25% of the history of life, is represented by the rich Phanerozoic fossil record. Towards the end of the Precambrian, animals (metazoans) appeared, even though they are represented by few fossils, most of which are difficult to interpret. The Phanerozoic is subdivided into three eras of unequal duration: the Paleozoic, which means “ancient life” (from 542 to 251 Ma ago), the Mesozoic, which means “middle life” (from 251 to 65.5 Ma ago), and the Cenozoic, which means “recent life” (from 65.5 Ma ago to the present). Vertebrates appeared and diversified in the Paleozoic. The conquest of

40 / How Can We Reconstruct Evolutionary History?

Age (Ma)

Eras

Epochs

Permian

Cenozoic

Phanerozoic

Periods

300

65

Carboniferous

Mesozoic

360

250

Paleozoic

Devonian

Late Carboniferous (Pennsylvanian)

Silurian

Cryptozoic

440

Ordovician 490

Cambrian 4500

540

Important events

First amniotes

318

Early Carboniferous (Mississippian)

First terrestrial vertebrates

360

420 540

Age (Ma)

Late Devonian

Appearance of the limb with digits

385

Middle Devonian Early Devonian

First trees

398 420

First terrestrial herbivorous arthropods First vascular plants First terrestrial plants, similar to mosses, probably only near permanent bodies of water; amphibious or terrestrial arthropods Appearance of vertebrates

Figure 1.19. Simplified geological time scale. This geological time scale emphasizes the periods during which the oldest terrestrial vertebrates lived. The drawing is not to scale, since the Cryptozoic should be about eight times as long as the Phanerozoic. The limb with digits may have appeared in the Middle Devonian if the dating of the recently described trackway from Poland is correct (Niedzwiedzki et al., 2010).

land by plants and various animal groups, including vertebrates, likewise took place during the Paleozoic, which is the era on which this book focuses. The Paleozoic comprises six periods, which are, from the oldest to the most recent, the Cambrian, the Ordovician, the Silurian, the Devonian, the Carboniferous, and the Permian (Fig. 1.19). The first gnathostomes ( jawed vertebrates) appeared in the Ordovician or Silurian, but the limb with digits appeared only in the Devonian. The fi rst truly terrestrial vertebrates appeared in the Carboniferous, the period during which the oldest amniotes lived. A FEW RELEVANT PALEONTOLOGICAL LOCALITIES

Fossils occur in many places; it is thus not possible to list all sites that have yielded early limbed vertebrates or their precursors. Only locali-

How Can We Reconstruct Evolutionary History? / 41

MongolKazakhstan arc China blocks

SIB Antler Orogeny

7

NAM 8 2

3 9

BAL 6

5

11

1 10

Paleo-Tethys Ocean GON 4

Glaciation Figure 1.20. Distribution of vertebrate fossiliferous sites from the Late Devonian and Carboniferous. This map shows the position of continents in mid-Early Carboniferous times (335 Ma ago). Sites from the Late Devonian (1 to 7), from the Early Carboniferous (8 and 9), and from the Late Carboniferous (10 and 11) are shown The Paleo-Tethys ocean occupied a position vaguely similar to that of the present-day Mediterranean and the Indian Ocean. The Variscan (or Armorican) orogeny was caused by the collision between Laurasia (a northern supercontinent that included North America, Baltica, and Siberia) and Avalonia (a small plate that included the Avalon peninsula of Newfoundland, Nova Scotia, England, the northern half of Germany, and part of Poland; it was located a bit south of numbers 10 and 11). It formed mountains whose traces remain in Brittany, in the French Massif Central, in the Ardennes, in central Germany, and in the northern part of the Appalachian Mountains. Later, this complex collided with Gondwana and Asia to form Pangea, which encompassed most continents from the Carboniferous to the Early Jurassic. Modified from Gradstein et al. (2004). localities: 1, Miguasha, Quebec, Canada. 2, Red Hill, Pennsylvania, USA. 3, eastern Greenland. 4, New South Wales, Australia. 5, Ningxia Hui Autonomous Region, China. 6, Tula, Russia. 7, Ellesmere island, Canada. 8, Delta, Iowa, USA. 9, East Kirkton, Scotland. 10, Joggins and Florence, Nova Scotia, Canada. 11, Nyqany, Czech Republic. abbreviations: BAL, Baltica (a continental plate that included a major portion of central and western Europe). GON, Gondwana (southern continent that included South America, Africa, Antarctica, Australia, India, and other fragments). NAM, North America. SIB, Siberia.

ties that have yielded many specimens or especially important taxa are described below (Figure 1.20). Fossils of our closest fi nned relatives have been found in several localities, including Miguasha, in the province of Quebec (Canada). That site is especially famous for the Escuminac Formation (rock stratum), which dates from the Late Devonian (about 380 Ma). It has yielded

42 / How Can We Reconstruct Evolutionary History?

numerous fossils of the sarcopterygian Eusthenopteron, which is one of the best-known Devonian vertebrates thanks to the detailed anatomical descriptions of the Swedish paleontologist Erik Jarvik (1980). Elpistostege, which is more closely related to us, was also found in Miguasha. Tiktaalik is still closer to us, although it, too, retained paired fins; it was found in southern Ellesmere Island in the Canadian Arctic. Several sarcopterygians more distantly related to limbed vertebrates were found in the Gogo Formation (also Late Devonian) in western Australia. The first limbed vertebrates come from eastern Greenland and date from the end of the Devonian, a little more than 360 Ma ago. They include Ichthyostega and Acanthostega. A similar, contemporary taxon called Tulerpeton was found near Tula, Russia. Fragmentary remains suggest that, in the Late Devonian, other limbed vertebrates or their near relatives also lived in the territories that now fall into the Baltic countries, Belgium, Australia, and China. After the Devonian, “Romer’s gap” (360–345 Ma), which may have been caused by the low atmospheric concentration of oxygen that prevailed around that time (Ward et al., 2006), hampers research on Early Carboniferous continental vertebrate faunae. Slightly more recent Early Carboniferous tetrapods (345–326 Ma) are known mostly from the coal-rich formations of Great Britain. These may include the first truly terrestrial vertebrates, some of which had already lost their limbs (Germain, 2008). Similar, contemporary forms have been found in West Virginia and Iowa (USA). In the Late Carboniferous, several fossiliferous sites now located in North America and Europe document the extensive diversification of limbed vertebrates. For instance, at least 26 species (Hook and Baird, 1986) were found in Linton (Ohio, USA). All these sites were then located close to the Equator, and North America then formed, along with much of Europe, a continent called Euramerica. It has not been possible to establish if the apparent absence of limbed vertebrates from higher paleolatitudes reflects their climatic preferences, or if this is simply caused by the absence of fossiliferous localities preserving the appro-

How Can We Reconstruct Evolutionary History? / 43

priate environments. The first amniotes appeared in the Late Carboniferous and are represented by fossils found at Joggins in Nova Scotia (Canada); these demonstrate that the conquest of land by vertebrates was completed by about 315 Ma ago. Joggins is unusual to the extent that most vertebrate fossils found there were preserved in the fossilized stumps of tree-sized lycopods (club mosses), such as Sigillaria and Lepidodendron. It is thought that after the death of these lycopods, the loose tissue in the pith at the base of the stumps decomposed, thus leaving a hollow stump into which small vertebrates fell. The nearby site of Florence, also in Nova Scotia, similarly preserves slightly more recent (310 Ma) limbed vertebrates in giant lycopod tree stumps.

. . . To study the evolution of life, we need a precise system of nomenclature adapted to dealing with taxa, since we already know millions of species, and since we cannot classify evolving beings in the same way as universal entities such as atoms. For a long time, rank-based nomenclature was used to classify living beings, but this system is ill-adapted to biological classification, since taxa are individuals rather than classes. Thus, a phylogenetic nomenclature was developed to better delimit taxa with the help of the phylogeny (the tree of life). Inferring phylogenetic relationships between taxa and character evolution requires relatively sophisticated methods. Thus, even when a rich fossil record is available, as is often the case with vertebrates, we cannot read the history of the group directly from it; this history must be reconstructed through various methods, such as parsimony (one of the simplest and most widely used methods, at least for morphological data), maximum likelihood, and the like. These methods, developed mostly in the 1960s, have triggered a true revolution in systematics and allow a tremendous gain in objectivity and, probably, in precision as well. We can thus study the transformation of homologous structures (such as the lung and swim bladder), and trace the origin of taxa in the distant past. The age of origin of taxa can be determined either through

44 / How Can We Reconstruct Evolutionary History?

the fossil record, which yields a minimal age, or through various molecular dating techniques, which estimate the time of origin of taxa using molecular data (DNA or, more rarely, proteins). Molecular dating methods have progressed steadily in the last decade, but their use remains difficult; many studies, even recent ones, have obtained ages that seem unrealistic when compared with paleontological ages. However, recent progress in these methods, and the increasing number of available calibration dates, makes molecular dating a very useful tool. The geological time scale is divided into the Cryptozoic (hidden life) and the Phanerozoic (visible life). The latter is subdivided into the Paleozoic, Mesozoic, and Cenozoic. The conquest of land occurred in the Paleozoic.

chapter two

Conquest of Land Data from Extant Vertebrates

The most direct source of information about the conquest of land by vertebrates is of course the Paleozoic fossil record of limbed vertebrates and their closest fi nned predecessors. However, the extant fauna also yields more indirect clues that are equally informative. Indeed, while fossils tell us about the morphology of extinct species, they often reveal little about the lifestyle of early vertebrates or the function of fossilized structures. To interpret fossils correctly, we must carefully study extant taxa, whose behavior and function can be observed. The extant taxa most relevant to studies about the conquest of land by vertebrates are obviously the closest relatives of tetrapods, the coelacanth and the dipnoans (lungfishes), which are described in this chapter.

ARE ANIMALS STILL CONQUERING THE LAND TODAY?

We generally consider that the conquest of land (the invasion of a new habitat, which did not, of course, result from a deliberate intent) by vertebrates took place in the Devonian or the Carboniferous. Here, we will see that this conquest did not result from a single event; instead, there were probably several independent acquisitions of an amphibious or a 45

46 / Conquest of Land: Data from Extant Vertebrates

terrestrial lifestyle in vertebrates. Additional invasions of land (i.e., the acquisition by an aquatic taxon of an amphibious lifestyle) took place more recently. An example is provided by Periophthalmus, a teleost that lives on the shores of tropical rivers and lakes and feeds on prey generally caught on land. Periophthalmus is lungless; it breathes through slightly modified gills and moves around on land using its strengthened pectoral fi ns and tail, with which it can jump. Its large eyes are set high up on the head, enhancing its panoramic view (360 degrees) on land. Periophthalmus (which includes several species) is not the only teleost with eyes adapted to see in air (rather than in water); in a few teleost species, the eyes are subdivided to see simultaneously in air (through the upper half ) and in water (through the lower half ). These teleosts swim near the water surface and can simultaneously observe potential prey and predators coming from above (birds, bats, and insects) or below (other teleosts). Periophthalmus is amphibious rather than truly terrestrial because it never ventures far from the water, where it must return regularly to moisten its skin and gills. It is impossible to know if some of its descendants will become more terrestrial in a distant future, although this is unlikely, given that just about every terrestrial ecological niche is occupied by tetrapods ( Vermeij and Dudley, 2000). Tetrapods became terrestrial more than 320 Ma ago, whereas Periophthalmus ventured onto land only a few million years ago, since it is part of the gobiid evolutionary radiation, which started no earlier than the Lutetian, 40 to 50 Ma ago (Patterson, 1993). Periophthalmus is deeply nested within this group and must therefore be much more recent. Thus, it seems likely that unless tetrapods become extinct (at least locally), other vertebrate taxa that could adapt to terrestrial life (such as Periophthalmus) will remain restricted to near-shore terrestrial habitats. Other animals, such as crabs, ventured onto land in the more recent past, well after other arthropods (insects, arachnids, myriapods, etc.) occupied most terrestrial niches. For instance, some crabs became terrestrial in Jamaica about 4 Ma ago (Schubart et al., 1998). This recent colonization of terrestrial

Conquest of Land: Data from Extant Vertebrates / 47

environments probably explains why most crabs live near the sea or on islands with a low diversity of insects and arachnids (this often occurs in islands located far from the nearest continent). The relationship between time of land invasion and geographic distribution also illustrates the contingent and irreversible nature of evolution; if tetrapods had not become terrestrial in a distant past, it is possible that other vertebrate taxa would have moved onto land, and an entirely different terrestrial vertebrate fauna might have evolved.

THE COELACANTH, A LIVING FOSSIL?

“Living fossil” is an expression often applied to extant taxa that resemble old lineages (often extinct for at least several dozens of millions of years [Ma] or more), especially if these extant taxa were discovered after their extinct relatives. According to these criteria, the coelacanth (Latimeria chalumnae) is indeed a living fossil because paleontologists described actinistians (the taxon that includes the coelacanth) from the Carboniferous to the Cretaceous, well before the coelacanth was discovered, and the coelacanth seems to have changed little in over 65 Ma. Scientists discovered the coelacanth in 1938, but peoples living in the vicinity of one of its habitats (on the southeastern coast of Africa, in Madagascar, and on the Comoro Islands) have known it since at least the 17th century. This is shown by the discovery of small statues of that period that are unmistakable representations of the coelacanth. Thus, the coelacanth was known to indigenous populations well before the discovery of the first actinistian fossils. A new species of coelacanth (Latimeria menadoensis) was unexpectedly discovered in Indonesia in 1998 (Pouyaud et al., 1999). The coelacanth is particularly relevant to this book because it is thought to resemble fairly closely the Paleozoic (400 Ma) sarcopterygians that were ancestral to all tetrapods, including us. Like those sarcopterygians, the coelacanth has fleshy fins strengthened by robust bones, including proximal elements homologous with our femur and humerus—the thigh and arm bones, respectively. It also

48 / Conquest of Land: Data from Extant Vertebrates

Figure 2.1. Coelacanth skull. Coelacanth skull in dorsal view (left), showing the intracranial articulation (gray line), and in palatal view (right), showing the subcephalic muscles that must have been present in our distant ancestors. Modified from Janvier (1996).

retains a hinge within the head, termed an intracranial articulation (which was lost in tetrapods), that may have allowed our distant ancestors to bite faster by lowering the anterior part of the head while the lower jaw was being raised (Fig. 2.1). Finally, the coelacanth displays various other characters that were previously known only from fossils. The concept of living fossil has recently been criticized because no extant species is identical to its distant ancestors, which lived dozens of millions of years ago, and in this respect, the coelacanth is no exception (Fig. 2.2). For instance, the coelacanth’s lung has lost its respiratory function, which is not surprising, given that it lives at great depth. Nevertheless, the coelacanth provides precious data about our distant ancestors, by showing that its fleshy fi ns are not used to walk on the substrate (contrary to the presumed use of these fins in our distant ancestors), but that they are nevertheless capable of complex movements very similar to those of a tetrapod walk. The coelacanth uses these movements to move above the substrate, sometimes vertically, without touching it.

Conquest of Land: Data from Extant Vertebrates / 49

Figure 2.2. Actinistian evolution. This tree shows the evolution of the group from the Late Devonian (top) to the present (bottom). Note that the coelacanth (bottom) is not identical to the oldest actinistians. Modified from Janvier (1996).

DIPNOANS: OUR CLOSEST EXTANT FINNED COUSINS

The closest extant relatives of tetrapods are probably dipnoans (also called lungfishes). There are three extant genera of dipnoans: Protopterus, Lepidosiren, and Neoceratodus, which inhabit tropical rivers in Africa, South America, and Australia, respectively. Dipnoans possess functional lungs and gills and can consequently breathe both air and

50 / Conquest of Land: Data from Extant Vertebrates

water. For Protopterus and Lepidosiren, this is very useful because the rivers that they inhabit periodically dry out. These animals then dig a burrow in the mud and secrete a mucus cocoon, in which they wait for the return of the wet season. While in the cocoon, they breathe air. Fossilized cocoons from the Carboniferous show that at least some dipnoans had acquired this ability by then. For a long time, paleontologists believed that early dipnoans inhabited fresh water, like extant dipnoans, but we now know that the earliest ones (from the Early Devonian) were marine or euryhaline (i.e., tolerated considerable salinity variations, as are often encountered in marginal marine environments, such as deltas and lagoons) and that they invaded fresh water later, in the Devonian and Carboniferous. Just like the coelacanth, dipnoans have fleshy fi ns with a welldeveloped endoskeleton, which are not used to crawl on the ground. Dipnoans never venture out of the water, but if left on dry land, they use lateral body undulations rather than fi ns to move about, just like eels (whose long and slender body shape is more suitable for this type of locomotion). Unlike the coelacanth, dipnoans were never considered living fossils, because scientists discovered extant dipnoans before encountering fossils of this taxon. Dipnoans display several specialized characters, such as dental plates that result from the fusion of several small teeth. These tooth plates are used to crush prey, which are sometimes protected by a hard shell (e.g., mollusks) or exoskeleton (e.g., crustaceans). They have lost the marginal teeth, which are present on the premaxilla, maxilla, and dentary of most other osteichthyans. Two of the three extant genera (Protopterus and Lepidosiren) have reduced, very slender paired fins. Thus, extant dipnoans look even less like our distant, fi nned ancestors than does the coelacanth, but like the latter, they can provide indirect clues about early sarcopterygians.

Conquest of Land: Data from Extant Vertebrates / 51

REPRODUCTION AMONG TETRAPODS: AMPHIBIANS ARE NOT ALL AMPHIBIOUS!

It is often said that extant amphibian ontogeny (development) recapitulates the history of the conquest of land by vertebrates. Indeed, many species have a biphasic life history, with aquatic larvae that metamorphose into terrestrial adults. In that context, amniotes (which include mammals and reptiles) are often considered the only truly terrestrial vertebrates because their egg (Fig. 2.3) is adapted to be laid on dry land. In most mammals, the egg is not laid, but it is present in the uterus; it surrounds the embryo and makes up part of the placenta. A unique structure of the amniotic egg, the amnion, surrounds the cavity in which the embryo develops. No amniote has larvae, because the hatchling already closely resembles the adult. Thus, amniotes are often considered to be completely adapted to life on dry land, whereas amphibians are considered partially adapted to terrestrial life. In fact, however, this distinction is not entirely justified. Several amphibian species are well-adapted to terrestrial life. For instance, some

Figure 2.3. Amniotic egg. The amnion and the chorion are characteristic of the amniotic egg. The amnion surrounds the amniotic cavity, in which the embryo of all amniotic species develops.

52 / Conquest of Land: Data from Extant Vertebrates

species of gymnophionans (an ancient group of limbless amphibians often called caecilians) and of anurans (tailless amphibians, i.e., frogs and toads) are viviparous (live-bearing) and have direct development (without aquatic larvae). A few other anuran, gymnophionan, and urodele (tailed amphibians such as salamanders and newts) species lay eggs on land with direct-developing embryos that hatch as terrestrial juveniles. Intermediate reproductive strategies also exist, in which the eggs are laid on leaves over freshwater bodies, into which tadpoles fall soon after hatching. Some aquatic amphibians have atypical reproductive modes; for instance, the eggs of pipid anurans are carried on the back of one of the parents. To sum up, amphibians display a great variety of reproductive modes. Furthermore, it is not certain that egg laying in fresh water is the primitive reproductive mode of amphibians, because many Paleozoic sarcopterygians laid their eggs in the sea (in salt water), and it is not necessarily easier to adapt such eggs to fresh water than to land (Skulan, 2000). Eggs adapted to be laid in salt water have a high concentration of ions that provides them with an appropriate osmotic pressure. If they are laid in fresh water, their volume increases drastically because water enters them via osmosis, killing the embryos. Such eggs could be laid in the ground, where interstitial moisture might be enough to avoid dehydration and where osmotic pressure is favorable for embryo survival (Skulan, 2000). It is thus possible that amphibians that lay eggs in fresh water evolved from ancestors that laid terrestrial (rather than marine) eggs. According to this hypothesis, amphibian metamorphosis does not constitute a recapitulation of their evolutionary history; it simply represents an adaptation to reproduction in fresh water. This would not be an isolated case, because freshwater insect larvae do not represent a case of recapitulation (retention of an ancient condition in an early developmental stage); rather, they represent an invasion of freshwater habitats (some ancestors of insects lacked aquatic larvae). In any case, it is clear that numerous amphibian species have adapted to reproduction on dry land, independently from amniotes.

Discoglossus

Leiopelma

Ascaphus

Ichthyophiidae

Rhinatrematidae

Hynobiidae

Cryptobranchidae

Sirenidae

Reptiliomorpha

Gymnophiona

Geological time scale Periods Time (Ma)

Temnospondyli

Cenozoic 65 Cretaceous

Karaurus

Caudata

145 Anura

Lysorophia

Brachystelechidae

Pantylus

Microbrachis

Keraterpetontidae

Urocordylidae

Scincosauridae

Aistopoda

Adelogyrinidae

Seymouriamorpha

Embolomeri

Nectridea

Urodela 200 Batrachia

Triassic 250

Lissamphibia

Permian 299

Habitat (observed or inferred)

Amphibia Tetrapoda Batrachomorpha

Jurassic

Carboniferous

Aquatic Amphibious Terrestrial Polymorphic Uncertain, amphibious or terrestrial Ambiguous, aquatic or amphibious

Figure 2.4. Evolution of lifestyle in amphibians. The fi rst lissamphibians were probably amphibious. From this primitive lifestyle, some became more terrestrial, whereas others returned to a more aquatic lifestyle. Modified from Vallin and Laurin (2004).

359

54 / Conquest of Land: Data from Extant Vertebrates

We should not conclude that a clear, unidirectional evolutionary trend towards a more terrestrial habitat is present in amphibians. The evolution of habitat use can be easily studied among extant amphibians, called lissamphibians. Such studies, based on a parsimony optimization of habitat (aquatic, amphibious, or terrestrial), suggest that the fi rst lissamphibians were amphibious (Vallin and Laurin, 2004), but many extant amphibians have now become completely aquatic and never venture out of the water (Fig. 2.4). These include pipids, a group of tropical anurans with a dorsoventrally flattened body, and several urodele taxa, such as sirenids, with small anterior limbs (the posterior limbs are lost), amphiumids, with diminutive limbs, and cryptobranchids, which include the largest extant urodeles, such as the Giant Japanese and Chinese Salamanders, which can reach lengths of about 2 m. Thus, the evolution of habitat in amphibians is complex.

. . . The conquest of land by vertebrates occurred more than 320 Ma ago, but today various taxa still venture onto land, as shown by Periophthalmus, a teleost that became adapted to live near the shores in the Cenozoic. However, these taxa are confronted with strong competition from taxa that are already well adapted to terrestrial life, such as tetrapods, insects, and arachnids. Our closest finned relatives include the coelacanth and dipnoans. The coelacanth is not literally a living fossil (and indeed, all suggested examples of living fossils can be similarly disproved), because it is not identical to Paleozoic actinistians, but it nevertheless provides precious anatomical data about early sarcopterygians. Dipnoans have retained functional lungs that enable them to aestivate in mucus cocoons, as their Paleozoic and Mesozoic predecessors did. Amphibians are not all amphibious, contrary to what their name suggests. Some are fully aquatic, whereas others complete their entire life cycle on dry land and are as terrestrial as amniotes. Thus, the amniotic egg is not necessary for adaptation to life on dry land.

chapter three

Paleontological Context

To better understand the conquest of land by vertebrates, we must keep in mind a minimal amount of background information about the development of terrestrial ecosystems. Indeed, without the presence of green plants on continents, animals would have probably not colonized this new habitat, which was so different from the marine environment in which life was born. This chapter presents a brief survey of the appearance and evolution of various taxa in continental habitats.

THE CONQUEST OF LAND IN VARIOUS TAXA

Photosynthetic Organisms Plants ventured onto continents well before vertebrates, and probably before animals. Since plants form the basis of the food chain of most ecosystems, animal life on continents became possible only after a continental flora had evolved. It is thus not surprising that terrestrial green plant fossils precede the oldest continental animal fossils by several millions of years. Unfortunately, only a small proportion of terrestrial plants have left fossils, which hampers reconstruction of their evolutionary history. The word “plant” used to designate various autotrophic organisms (i.e., those capable of producing organic substances using 55

56 / Paleontological Context

inorganic matter and an energy source, usually sunlight, which is used in photosynthesis to produce sugars). Autotrophic (and photosynthetic) organisms form a polyphyletic group, and it is useful to distinguish main taxa. The first photosynthetic organisms were probably the cyanobacteria, which have existed for more than 2,5 Ga. These unicellular organisms are bacteria, as their name implies; they have a simple structure, lacking a cellular nucleus or most other organites found in eukaryotes. Cyanobacteria have long been considered plants (and their names are regulated by the International Code of Botanical Nomenclature), but they are not closely related to green plants (which form the terrestrial flora) and are classified accordingly in recent taxonomies. Algae form a large, polyphyletic group of autotrophic, photosynthetic organisms; it includes several taxa (brown, red, green algae, among others) that have convergently acquired chloroplasts, the organites that perform photosynthesis. Chloroplasts probably represent cyanobacteria that became endosymbionts (symbiotic organisms that lived in the cells of the host organism). Thus, cyanobacteria are closely related to the chloroplasts of various photosynthetic eukaryotic organisms, but the nuclear genome of the latter is closer to that of various other eukaryotic taxa than to that of cyanobacteria. Only green algae are closely related to terrestrial green plants; the terms “algae” and “plants” are thus not taxa, although they are useful ecological terms. Cyanobacteria and algae are mainly aquatic, and only the former may have contributed in forming a very simple primordial terrestrial ecosystem by forming a thin organic layer over emerged rocks, perhaps only close to the water, nearly 2.5 Ga ago. Truly terrestrial plants may have appeared as early as the Cambrian (540 to 490 Ma) because their spores (reproductive cells) have been discovered in strata from that period. A few fossils show the presence of terrestrial plants in the Silurian (440 to 420 Ma), but these are much better known from the Devonian (420 to 360 Ma) onwards. In the Devonian, the terrestrial flora experienced a spectacular evolutionary radiation; at the beginning of that period, terrestrial plants were small

Paleontological Context / 57

and resembled mosses, whereas at the end of the Devonian, forests composed of tall trees (about 30 m) covered the continents. The Carboniferous (360 to 300 Ma) forests included ferns and some seed plants, such as conifers. Green plants plausibly became terrestrial only once, since they form a clade. However, other autotrophic organisms, such as lichens, also play an important role on land. Lichens are not plants; they are symbiotic organisms combining an alga, which provides sugars required for their survival through photosynthesis, and a fungus, without which the alga could not survive on dry land. Fungi are not plants and are not autotrophic. They feed on decaying organic matter in the soil. They are mentioned here because they have often been wrongly associated with plants, and because they play an important role in recycling organic substances in the soil. Like lichens, they originate from an independent conquest of the land (they have distant marine ancestors).

Arthropods Arthropods form one of the largest groups of animals; more than a million species have been described. This taxon includes crustaceans, insects, centipedes, and arachnids. The first arthropods, from the Cambrian, were all marine. There were at least four conquests of land (and perhaps many more) in this group: among crabs (probably several conquests) and isopods among crustaceans; among insects; among arachnids; and fi nally, in myriapods, which include, among others, the Diplopoda (millipedes) and Chilopoda (centipedes). Parsimony analysis suggests that these all represent independent appearances of a terrestrial lifestyle because the fi rst crustaceans were all marine; the closest relatives of arachnids (the horseshoe crabs, pycnogonids, and extinct eurypterids) are all marine. The history of insects and myriapods is more complex because their origins are uncertain, but all their potential sister taxa are marine (Fig. 3.1).

58 / Paleontological Context

Mollusca

Crustacea

Porifera Cnidaria Chordata Echinodermata Pterobranchia Onychophora Arachnida Xiphosura Pycnogonida Chilopoda Hexapoda Diplopoda Decapoda Isopoda Branchiopoda Trilobita Tardigrada Nematoda Priapulida Chaetognatha Brachiopoda Cephalopoda Gastropoda Echiura Annelida

Chelicerata

>1

1

1

1

1

1-2 1

1

1

Arthropoda 1

Ecdysozoa

Lophotrochozoa

Deuterostomia

Figure 3.1. Metazoan phylogeny. Simplified metazoan evolutionary tree emphasizing taxa that include terrestrial species, as well as the best-known strictly aquatic taxa. Arthropod phylogeny is still controversial, but all hypotheses imply numerous appearances of a terrestrial lifestyle in that group. Only the primitive condition of each terminal taxon is indicated (white, aquatic; black, terrestrial). Horizontal bars indicate the acquisition of a terrestrial lifestyle, which may concern only a part of each clade. The numbers next to the bars indicate the minimal number of transitions to a terrestrial lifestyle. Thus, chordates are coded aquatic, but one or two clades in this group has acquired a terrestrial lifestyle. Branch lengths are arbitrary. Modified from Peterson and Eernisse (2001) for the main metazoan taxa, and from Giribet et al. (2001) and Hwang et al. (2001) for arthropods.

The main gas exchange organs of marine arthropods are gills, usually located above their legs (Fig. 3.2). On dry land these gills dry out easily, and in most terrestrial arthropods they have been modified through evolution into lungs or were replaced by trachea. Gills are absent in most terrestrial arthropods, with the exception of crabs, which mostly live near the water (although this geographic distribution does not necessarily result from a limitation of their respiratory system, and

Figure 3.2. Arthropods. Trilobites (A, B) are among the oldest known arthropods; they became extinct at the end of the Paleozoic. All were marine. A dorsal view (A) shows the three longitudinal subdivisions (head, thorax, and abdomen) that gave them their names (“three lobes”). The appendices are poorly differentiated (B). Horseshoe crabs (C, D) are marine chelicerates (hence, they are related to arachnids). The large compound eyes are visible in dorsal view (C). The posterior appendices are modified into swimming appendages and bear gills on their dorsal surface. Their larvae resemble adult trilobites. Reproduced from Haeckel (1904).

60 / Paleontological Context

may simply reflect their late arrival on continents). Terrestrial isopods breathe through gills that have been modified into lungs or trachea. Among arachnids, the gill-bearing legs have fused to the ventral surface of the abdomen and the gills have been modified into lungs (not homologous with the osteichthyan lung). These lungs communicate with the environment through small pores, which limit dehydration. Among insects and centipedes, another respiratory system evolved; it is composed of tubes called trachea that bring air directly into the body. However, in one group of centipedes (Chilopoda), the trachea resemble lungs and may result from an independent transformation of gills into an air-breathing organ (Barnes, 1987). Among arthropods, contrary to vertebrates, terrestrial locomotion was not problematic because their appendices allowed them to walk on the bottom of oceans, seas, lakes, and rivers, and they could be used with little or no modifications to walk onto emerged land. The small size of most arthropods, compared with vertebrates, facilitated the adaptation of their locomotory system to life on dry land. Arachnids (Fig. 3.3) and insects have a thin wax layer on their cuticle, which waterproofs it to reduce water loss. They can thus live on most continental habitats. Many centipedes (Chilopoda) are more vulnerable to dehydration and generally live in more humid environments. Arthropods may have ventured onto land as early as the Silurian (Labandeira, 2005), or possibly as early as the Ordovician. Scorpions are known from the Silurian, whereas acarians (a group of arachnids) and hexapods (collembolans and insects) are known from the Early Devonian. Burrows from the Ordovician (Retallack and Feakes, 1987) suggest that myriapods were perhaps the first terrestrial arthropods, but the oldest fossils from that group date from the Late Silurian (Prothero, 2004). Plant fossils showing traces of browsing suggest that some arthropods had become herbivorous by the Devonian; this was an important step in the development of terrestrial ecosystems.

Figure 3.3. Arachnids. Arachnids are mainly terrestrial arthropods, but the related horseshoe crabs (Fig. 3.2) are marine. Reproduced from Haeckel (1904).

62 / Paleontological Context

Mollusks, Annelids, Onychophorans, and Tardigrades Mollusks, and to a lesser extent annelids, are mainly marine groups, but both have freshwater and terrestrial members (Fig. 3.1). Among mollusks (Fig. 3.4), only gastropods (which have a spiral shell, as in snails, or lack a shell, as in slugs) are terrestrial; cephalopods (squids, cuttlefish, etc.), bivalves (also called pelecypods, these include clams, mussels, etc.), monoplacophorans, and polyplacophorans are exclusively aquatic or live in the intertidal zone and are active mostly when submerged. Terrestrial gastropods are known as early as the Late Carboniferous (Pennsylvanian). Most terrestrial mollusks belong to the taxon known as pulmonates; these have become adapted to breathe air by losing the gills (not homologous to vertebrate gills) and by transforming the inner surface of the mantle into a lung (not homologous to the vertebrate lung, either). However, at least eight clades of gastropods have become terrestrial at various times from the Carboniferous to the Cenozoic (Vermeij and Dudley, 2000). A group of annelid, the earthworms, plays an important role in aerating the soil. Another group of annelids, the leeches, is less popular, but

Figure 3.4. Mollusks. Mollusks are a primitively aquatic group. Thus, all cephalopods (A: ammonite from the Middle Jurassic), bivalves (B), and most gastropods (C) are aquatic. Reproduced from Haeckel (1904).

Paleontological Context / 63

it is also well-adapted to terrestrial life. Earthworms and leeches form the taxon called “clitellates,” which includes all terrestrial annelids. The date of appearance for clitellates is difficult to determine because they lack mineralized body parts and therefore rarely fossilize. The oldest fossil attributed to clitellates dates from the Carboniferous, but its affinities are disputed; thus, clitellates may have appeared more recently. The origin of onychophorans and tardigrades is poorly understood because these taxa have a sparse fossil record. They are related to arthropods and share a few of their characteristics, such as a thin cuticle that is periodically shed and walking appendages (in onychophorans and tardigrades, the appendages lack well-defined articulations). Onychophorans superficially resemble caterpillars, but this resemblance is convergent. Tardigrades are much stubbier and have only four pairs of legs. Possible relatives of these taxa appear as early as the Cambrian, but by that time genuine tardigrades are also known from the fossil record. All these Cambrian forms were marine. Onychophorans are terrestrial, and their oldest known fossils date from the Carboniferous. Some tardigrades are terrestrial, but these are not known before the Cretaceous; it is probable that the group invaded land much earlier, but this cannot be demonstrated, because it has left no fossils between the Cambrian and the Cretaceous.

THE HISTORY OF OUR IDEAS ABOUT THE CONQUEST OF LAND BY VERTEBRATES

The Old Red Sandstone, Fresh Water, and Seasonal Aridity For most of the 20th century, scientists have thought that our fi nned ancestors started venturing onto land by crawling on the shores of seasonally drying lakes and ponds, to reach deeper bodies of water to survive the dry season. This idea did not arise spontaneously in the minds of geologists and paleontologists; it was based on scientific data. Several Devonian sarcopterygians and Permo-Carboniferous stegocephalians

64 / Paleontological Context

(limbed vertebrates) were found in red sandstone formations (often called red beds). The red color of these sediments results from the presence of iron oxide. It was long thought that this red color could arise only in an arid environment. Since sandstones originate from sand particles carried by water, the presence of large quantities of water was required for their deposition. The paradox was solved by postulating that these environments, in which many early sarcopterygians lived, were seasonally arid. It was also thought that these sands were deposited in freshwater, partly because extant dipnoans live in freshwater; the only other extant fi nned sarcopterygian, the coelacanth, was still unknown to scientists when they formulated this hypothesis. Furthermore, extensive ossification of the paired fi n skeleton of several Paleozoic sarcopterygians led some authors to suggest that these animals were adapted to (at least occasional) terrestrial locomotion. Thus, it seemed logical to infer that our last aquatic ancestors lived in fresh water. As we will see in “Recent Geological Works: Our Ancestors Lived in the Seas” later in this chapter, this theory is now abandoned, but it has deeply influenced generations of paleontologists, and it therefore deserves to be introduced. Devonian sarcopterygians were mid-sized to large predators (from 30 cm to 3 m total body length). They probably fed on other aquatic vertebrates, such as placoderms (an extinct group of gnathostomes normally covered by a fairly thick bony armor), acanthodians (small, spiny gnathostomes), and actinopterygians (ray-finned vertebrates).

Amphibians and Freshwater Sharks Early stegocephalians were long thought to have been freshwater inhabitants, like other Paleozoic sarcopterygians. This idea is still fi rmly entrenched in the literature, but it rests partly on a confusion created by an imprecise nomenclatural system. Many authors have referred to early anamniotic stegocephalians as “amphibians.” Extant amphibians (the lissamphbians) rarely tolerate salt water; they live on land, in fresh water,

Paleontological Context / 65

and more rarely, in brackish water. Thus, it seemed logical to consider that early “amphibians” (stegocephalians) lived in fresh water or on land. More objective arguments also supported this hypothesis. Several Permo- Carboniferous stegocephalians were found in red beds that, as we saw in the section above, were then considered to have formed in seasonally arid environments, hence, in fresh water. These red beds are fairly abundant in the U.S. Southwest and contain several of the richest fossiliferous localities for Late Carboniferous and Early Permian stegocephalians. Both arguments combined (the freshwater habitat of lissamphibians and the fossilization of Paleozoic limbed vertebrates in red beds) must have seemed fairly convincing, because clues that should have raised suspicion about the presumed freshwater habitat of the first stegocephalians were ignored. For instance, xenacanthids, a group of chondrichthyans from the Carboniferous and Permian, were interpreted as freshwater sharks, partly because they were associated with early “amphibians” (stegocephalians). Yet extant chondrichthyans are marine, with very few exceptions. In the last few years, a few specialists argued that xenacanthids must have occupied marine as well as freshwater habitats, and a few even proposed that xenacanthids were mostly marine animals (Schultze and Soler- Gijón, 2004; Falcon-Lang et al., 2006). We have long known that a few geologically younger (Triassic) stegocephalians lived in salt water, but this was viewed as a specialization of these groups. Recent discovery of various clues, including microfossils associated with stegocephalians, indicates that some Devonian, Carboniferous, and Permian stegocephalians lived in salt or brackish water for at least part of their life cycle. Thus, the geographic distribution of Devonian limbed vertebrates suggests that at least some of them tolerated salt water because Metaxygnathus was found in Australia, which was separated from the Old Red Sandstone Continent (in which most other Devonian stegocephalians were located) by an epicontinental sea (de Ricqlès and Laurin, 1999). The Devonian stegocephalian

66 / Paleontological Context

Sinostega was found in a part of China that was then located on an isolated continent (Zhu et al., 2002). The Devonian stegocephalian Tulerpeton was fossilized in a clearly marine environment (Lebedev and Coates, 1995). Thus, a good proportion of Devonian stegocephalians lived or dispersed through the sea. In the Carboniferous and Permian, most stegocephalians seem to have lived on land and in fresh water, but several species seem to have tolerated salt water. In Puertollano, in the center of the Iberian Peninsula, two species inhabited a coastal environment. Three skeletons of a fairly large species (Iberospondylus schultzei) and trackways (fossil footprints) of a much smaller species (Puertollanopus microdactylus) were discovered there (Soler-Gijón and Moratalla, 2001; Laurin and SolerGijón, 2006). The Puertollanopus trackways are superimposed on those of a chondrichthyan (Undichna unisulca, probably a xenacanthid), which proves the presence of tides in that fossiliferous locality (the Puertollanopus trackways were left at low tide, and the Undichna trackway at high tide). Puertollanopus must have walked at least occasionally in sediments soaked with salt water (if the soil had been dry, no trackway would have been preserved). These are not isolated examples; various works suggest that several stegocephalian species representing all the main clades tolerated salt water (Schultze and Maples, 1992; Schultze et al., 1994). These discoveries suggest that contrary to the long-prevailing view, saltwater tolerance was probably widespread in early stegocephalians, and that the saltwater intolerance characteristic of lissamphibians is a synapomorphy of extant amphibians (Fig. 3.5), as shown by a review of the evidence placed in a phylogenetic context (Laurin and Soler-Gijón, 2001). The name “amphibian” probably misled paleontologists, to an extent. Rather than considering a priori that these “amphibians” and associated chondrichthyans were freshwater forms, it would have been more rigorous to also consider the alternative: the presence of sharks, which are usually marine, suggests that the associated “amphibians” tolerated salt water.

Paleontological Context / 67

Stegocephali Tetrapoda

Approximate age (millions of years)

Geological eras and periods

Salientia

“Microsaurs” Lysorophia Gymnophiona Urodela

Seymouriamorpha

Lissamphibia Amniota Diadectomorpha Aïstopoda

Embolomeri

Temnospondyli

Amphibia

Jur 200 Tri

Mesozoic

145

Per

250

Saltwater tolerance Saltwater intolerance

Car 360 Dev

Paleozoic

300

420

Figure 3.5. Evolution of osmotic tolerance in stegocephalians. Extant groups are in bold type. The fi rst amphibians tolerated saltwater; this capability was lost in an ancestor of extant amphibians, probably in the Carboniferous or the Permian. Abbreviations: Car, Carboniferous. Dev, Devonian. Jur, Jurassic. Per, Permian. Tri, Triassic.

Recent Geological Works: Our Ancestors Lived in the Seas Recent works show that red beds do not require an arid climate to form. On the contrary, these rocks require humidity for oxidation to take place. We also know that this oxidation may take place millions of years after the sediments are deposited. Hence, the red color may not reflect the depositional environment or the environment inhabited by the red bed fossils. Why is this important? Because this suggests that Devonian

68 / Paleontological Context

sarcopterygians and Permo-Carboniferous stegocephalians found in red beds did not necessarily experience seasonal aridity. We have seen above that Paleozoic stegocephalians lived in salt and fresh water. The same conclusion holds for Devonian sarcopterygians; we now know that the first sarcopterygians were marine and that they invaded fresh water later in the Devonian, but sarcopterygians never ceased to inhabit the seas. Several early sarcopterygians were marine, as demonstrated by their association with marine organisms, such as corals, echinoderms (the group that includes starfishes and urchins), or brachiopods. The very broad geographic distribution of some sarcopterygians confirms this interpretation, because it is difficult to imagine how strictly freshwater species could spread to various continents separated from each other by seas (Fig. 1.20). As marine animals, most early sarcopterygians could not have experienced seasonal aridity, because sea level does not vary from one season to the next. Hence, sarcopterygians did not have to venture on dry land to seek deeper bodies of water, and another explanation must be sought for the origin of the limb and of terrestrial locomotion. We now think that early sarcopterygians, except for stegocephalians, were strictly aquatic animals, and that many of them were marine.

THE LATERAL- LINE ORGAN AND THE LIFESTYLE OF PALEOZOIC STEGOCEPHALIANS

Several Permo- Carboniferous stegocephalians seem to have been aquatic because they probably had a lateral-line organ, even as adults. This organ includes a long line that extends along the flanks of the body (hence, the name “lateral line”) and more complex cephalic portion; the latter is discussed here because it is the only one that is visible on fossilized limbed vertebrates. In extant vertebrates, this organ is used to detect movements in water. It is found only in aquatic vertebrates, because on land it does not work and dehydrates quickly. Among amphibians, this organ exists only in aquatic larvae, and in the adults of the most

Paleontological Context / 69

aquatic forms, such as the axolotl, sirenids, and pipids; it disappears at metamorphosis in amphibious or terrestrial species. Thus, the presence of this organ indicates a fairly aquatic lifestyle. This organ, composed of ciliated cells, has not fossilized, but grooves (or canals, in Devonian taxa) that housed it attest to its presence in many early stegocephalians. These grooves are easy to detect because the dermal bones of most early limbed vertebrates were firmly attached to the dermis, as in extant crocodilians, as shown by the remarkable dermal ornamentation of early stegocephalians (Fig. 3.6). The presence of these grooves in several early limbed vertebrates suggests that they were aquatic. This organ also existed in finned Devonian sarcopterygians, but in these taxa, the organ was located deeper in the bones, in canals that opened to the outside through a series of pores. In the Devonian stegocephalian Acanthostega, the lateral-line organ was housed partly in grooves on the surface of the skull, and partly in deeper canals. The lateral-line organ was presumably functional in the adults of many taxa, at least when the grooves or canals were well defined (in some species, the grooves appear to have been present in larvae but disappeared progressively in development, which suggests a more terrestrial lifestyle in adults). The presence of grooves or canals for the lateral-line organ in all Devonian stegocephalians, and in many of their Permo-Carboniferous descendants, suggests that these animals were aquatic and that stegocephalians may have become terrestrial several millions of years (perhaps as much as 20 or 30 Ma) after the appearance of the limb. Unfortunately, the absence of canals on the skulls of other stegocephalians does not prove that they were terrestrial, because the lateral-line organ often leaves no trace on the skull. Thus, in aquatic lissamphibians the organ, when present, is located in the dermis, and it leaves no trace on the skull or in any other part of the skeleton. For this reason, a terrestrial lifestyle is more difficult to establish using this line of evidence. Even in the oldest known lissamphibians, the skull shows no trace of the lateralline organ, but this does not imply that it was absent (Fig. 3.7). The absence of grooves cannot be used as evidence to infer the habitat.

70 / Paleontological Context

Figure 3.6. Skull of Dutuitosaurus ouazzoui, a Triassic stegocephalian. The superficial ornamentation of the bones, as in extant crocodilians, indicates that the dermis was firmly attached to the bone. The skull of this animal shows grooves for the cephalic portion of the lateral-line organ. They are especially easy to recognize between the external nares and near the right orbit (among other places). From this, we can conclude that this animal was aquatic. This skull measures about 57 cm in length. Reproduced from Dutuit (1976), © Publications Scientifiques du Museum ´ national d'Histoire naturelle, Paris.

Contrary to various extant vertebrate groups, such as cetaceans (whales), pinnipeds (seals, sea lions, and walruses), sirenians (sea cows and dugongs), or marine turtles, it is difficult to infer the lifestyle of most early stegocephalians from their morphology. Few early limbed vertebrates display obvious aquatic adaptations such as modifications of limbs into swim paddles (as seen in whales and the Mesozoic ichthyosaurs) or pachyostosis (thickening of the bones), which is carried to an extreme in extant sirenians, whose ribs lack a medullary cavity (Buf-

Paleontological Context / 71

Figure 3.7. Skull of the Jurassic lissamphiiban Karaurus. Karaurus is one of the oldest known lissamphibians, dating from the Jurassic (Kimmeridgian, more than 150 Ma). It is a stem urodele (it is related to salamanders and newts, but outside the crown clade that includes these forms). The texture of the dermal bones is a little reminiscent of Dutuitosaurus (see Figure 3.6). This skull lacks grooves for the cephalic portion of the lateral-line organ. The skull measures 3.9 cm in length. Photo by the author of the holotype, located in the Paleontological Institute, Moscow.

frénil and Schoevaert, 1989). The body shape of Paleozoic stegocephalians does not display as great a diversity as in extant tetrapods; most species vaguely resembled urodeles (salamanders and newts) and crocodilians. In rare cases, a long, deep tail with tall neural and hemal spines suggests a caudal fi n and, hence, an aquatic lifestyle. In other cases, the very long, slender body suggests an anguilliform (eel-like) mode of locomotion, but this body shape is found both in terrestrial and aquatic forms, among snakes and gymnophionans, among other examples. Even a stubby body shape, which seems ill-adapted to swimming, does not necessarily indicate a terrestrial lifestyle, as shown by the hippopotamus, marine turtles, and sirenians. For all these reasons, it is difficult to obtain reliable inferences about the lifestyle of many

72 / Paleontological Context

Paleozoic stegocephalians. We will see, in Chapter Four, how we may attempt to tackle this problem.

. . . The stepwise development of terrestrial ecosystems required much time. Autotrophic, photosynthetic organisms, such as cyanobacteria and green plants, were presumably the first life forms to colonize emerged land. Green plants diversified quickly in the Devonian, and by the end of that period, tall forests covered the continents. Arthropods were among the first animals to invade dry land, by the Late Silurian or Early Devonian (420 to 400 Ma). Their small body size and their walking appendages may have helped them invade terrestrial ecosystems dozens of millions of years before vertebrates, whose presence on emerged land harks back to the Carboniferous (340 Ma). The invasion of continents by other taxa, such as mollusks, annelids, onychophorans, and tardigrades, is poorly documented by a sparse fossil record resulting from the absence of mineralization in most of these taxa (many mollusks excepted). Thus, terrestrial onychophorans are known as early as the Carboniferous, whereas terrestrial tardigrades appear much later in the fossil record, in the Cretaceous; this large timing difference presumably reflects a large gap in the fossil record. We have long thought that the latest aquatic ancestors of terrestrial vertebrates were freshwater inhabitants, but it now appears that several of them lived in salt water, in coastal regions. The fi rst amphibians probably tolerated salt water; the loss of this tolerance is probably an autapomorphy of Lissamphibia. We lack reliable data on the lifestyle of most early stegocephalians, which hampers dating the invasion of land by vertebrates. The presence of grooves for the lateral-line organ indicates an aquatic lifestyle in many early stegocephalians, but the absence of such grooves in many other limbed vertebrates does not necessarily indicate a terrestrial lifestyle, because the organ does not always leave traces on the skull.

chapter four

Vertebrate Limb Evolution

The limbs are the main locomotory structures in most tetrapods. There are of course exceptions (gymnophionans, snakes, etc.), but most tetrapods walk, run, or fly using their limbs, which probably played an important role when our ancestors ventured onto land. To understand the colonization of land by vertebrates, we must study the origin and evolution of limbs, and especially of their skeleton, which is often the only part to fossilize.

THE VERTEBRATE SKELETON

The vertebrate skeleton can be divided into an internal endoskeleton and a dermal skeleton, which is located in a more superficial position (in the deep part of the dermis and immediately below). The dermal skeleton of vertebrates is not an exoskeleton, because it is generally covered by the epidermis (at least). The vertebrate skeleton is composed mostly of bone and cartilage. Cartilage is lighter and more flexible than bone and it is generally not mineralized. However, it wears down and heals more poorly than bone, which explains that old individuals (at least in our species) often suffer from arthrosis caused by extensive cartilage erosion around articular surfaces. In contrast, bone is mineralized (its 73

74 / Vertebrate Limb Evolution

mineral component is hydroxyapatite) and it heals relatively well if broken. It is also stiffer than cartilage. Thus, it is no surprise that the skeleton of most large vertebrates is composed mainly of bone, cartilage being found around articulations and during early development. The dermal skeleton was primitively composed of bony scales of variable size that covered the whole body. Among stegocephalians, it is represented by the dermal skull (composed of superficial bones, such as the frontal and parietal), the dermal part of the shoulder girdle, and small dermal scales, which are usually ossified and are most commonly found on the ventral surface of the abdomen (Fig. 4.1). Contrary to the endoskeleton, the dermal skeletal elements do not go through a cartilaginous developmental stage; these bones form directly from mesenchyme condensations (mesenchyme is a loose tissue composed of poorly differentiated cells). The endoskeleton (Fig. 4.1) includes the axial skeleton (vertebral column and ribs), the neurocranium (the braincase that protects the brain and sense organs like the inner ear, the eye, and the olfactory epithe-

Figure 4.1. Vertebrate skeleton. Skeleton of Acanthostega, from the Late Devonian. The dermal skeleton consists of the dermal skull, the dermal shoulder girdle, and the caudal fi n rays. The endoskeleton includes the vertebrae, ribs, visceral skeleton, neurocranium, pectoral and pelvic girdles, limbs, and caudal fi n rays). Modified from Coates (1996). Reproduced with permission from the Royal Society of Edinburgh from the Transactions of the Royal Society of Edinburgh : Earth Sciences, volume 87 (1996), pp. 363–421.

Vertebrate Limb Evolution / 75

lium), the visceral skeleton (gill arches and the mandibular arch, which represents part of the jaw), and most of the appendicular skeleton (which supports the fi ns and limbs). The oldest part of the endoskeleton is probably the notochord, a slender rod that stiffens the body of the amphioxus, a close relative of vertebrates. The notochord is a precursor of the vertebral column, around which the vertebrae appeared and around which they develop in embryos. Vertebrae provide additional support and greater stiffness, which were required as vertebrates increased in size. They are composed of a neural arch, which surrounds and protects the spinal chord, and of a centrum, which surrounds and strengthens the notochord. In the tail, there is also a hemal arch, which surrounds a large artery. The endoskeleton of the first vertebrates was mostly cartilaginous, but in stegocephalians, most of the cartilage is replaced in ontogeny (individual development) by endochondral bone (which develops in a cartilage and later replaces it) or perichondral bone (which forms around a cartilage without destroying it). The appendicular skeleton includes the girdles (pectoral and pelvic), the stylopod (fi rst segment of the limbs: humerus in the forelimb, and femur in the hind limb), the zeugopod (second segment of the limb: radius and ulna in the arm, tibia and fibula in the leg), and the autopod (hand and foot, from the wrist and ankle to the tip of the fi ngers and toes). All these structures are endoskeletal, except part of the shoulder (pectoral) girdle, in which several dermal bones were primitively present (interclavicle, clavicle, cleithrum, and anocleithrum, in a ventral to dorsal order). In many extant tetrapods, the dermal portion of the shoulder girdle is much reduced and only the clavicle is retained (as in humans).

HOX GENES AND THE ORIGIN OF DIGITS

Recent works in developmental molecular biology have yielded new insights into old evolutionary problems, especially through data on gene expression patterns in developing embryos. The classical problem of the origin of digits has thus been tackled using Hox gene expression

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Hox Genes The Hox genes (short form of Homeobox) are expressed in embryonic development; their expression influences development by determining (along with other genes) the destiny of cells located in various positions in the embryo. Among vertebrates, they are particularly important in determining the identity of cells along the anteroposterior axis (through which the vertebral column extends), but they also play an important role in secondary axes, such as the fin and limb axes. They are also involved in the development of other metazoans. Even plants have similar homeotic genes, although they have a different origin and are not homologous. They were discovered independently in 1983 by two teams (Scott and Weiner, 1984). In early metazoans, there was a single Hox gene complex comprising 13 genes (Hox 1 to 13). This single complex persists in some chordates, such as the amphioxus Branchiostoma fl oridae. Among vertebrates, this number increased quickly through duplication. Hox gene evolution is complex (because some genes, or even whole complexes, that had appeared through duplication were subsequently lost) and still under study, but it seems that the first craniates had at least two complexes, and the first gnathostomes, four. This number persists in sarcopterygians and in some actinopterygians (such as Polypterus senegalus), but another duplication took place in a teleostean ancestor, because three distantly related teleost species possess seven such complexes (Amores et al., 2004).

patterns in limb or fin buds. Hox genes, present in several copies in vertebrates, are involved in body plan organization (fate mapping) in animals (see the box titled “Hox genes”). Since the 19th century, anatomists and paleontologists have studied the origin of the autopod (the distal part of the limbs, from the wrist or

Vertebrate Limb Evolution / 77

ankle to fi nger and toe tips). The oldest studies suggested that the phalanges were homologous with the distal radials of our ancestor’s fins, but this idea was rejected in 1941. Early works on Hox gene expression patterns in developing fi n buds of the teleost Danio rerio and in developing limb buds of the chick (Gallus gallus) and mouse (Mus musculus) suggested that the hands and feet were neomorphs, new structures without homologues in the vertebrate fi ns. These data showed that in mice and chicks, a few Hox genes (D-10 to 13) were expressed in three phases in early limb development (Fig. 4.2). The first phase seems to delimit the territory of the stylopod (proximal segment of the limb, in which the humerus and the femur, the arm and thigh bones, are located); it consists of a distal expression pattern (Fig. 4.2A, B). The second phase, which is expressed in the posterior half of the limb bud (Fig. 4.2C, D), seems to delimit the zeugopod (second segment, which includes the radius and ulna of the upper arm, and the tibia and fibla of the leg). In mice, the third expression phase is restricted to the posterior part and the distal portion of the limb bud (Fig. 4.2E); it seems to correspond largely to the territory of the autopod (hand and foot). In the teleost Danio, there is no third phase; in the developmental stage at which it could be expected to occur, we still fi nd the expression pattern of the second phase (Fig. 4.2F). This suggests, according to some authors, that there is no homologue between the autopod (hand and foot) and the fi n of Danio. The Hox A-11 expression pattern leads to the same conclusion because it is expressed in the distal portion of the zeugopod, far from the limb bud apex in mice (Fig. 4.2G), whereas it is expressed in the fin bud apex in Danio (Fig. 4.2H). The problem with this argument is that Danio, like all teleosts, has a reduced fin endoskeleton, as shown by a comparison with the sturgeon (Fig. 4.3, Acipenser), and it lacks a metapterygial axis (which appears in fin development, and along which the structures homologous with the limb differentiate); thus, no homologue of the autopod is expected in

78 / Vertebrate Limb Evolution

Development

Mouse

Danio rerio

A

B

C

D

Phase 1 Hox D-10 Phase 2 Hox D-11

E

F Phase 3 Hox D-11

G

H

Hox A-11 Figure 4.2. Hox gene expression pattern in actinopterygian and tetrapod appendages. Hox gene expression pattern in mouse limb buds (left) and in fi n buds of the teleost Danio rerio (right). The zones of various Hox gene expressions are shaded dark gray; the apical ectodermal ridge, in which fi n rays develop, is in light gray. Note that in Danio, the third expression phase is not distinct from the second one (the same expression pattern prevails), contrary to the pattern displayed by the mouse. Redrawn from Sordino et al. (1995).

the Danio fi n. It would have been much more interesting (although admittedly much more difficult) to perform similar studies on sarcopterygians, such as dipnoans, in which the metapterygial fin axis is well developed (Fig. 4.3, Neoceratodus). A similar study on an extant basal actinopterygian that retains a metapterygial axis (Polyodon spathula) subsequently showed a distinct third phase of Hox gene expression in fin buds, which is similar to the tetrapod third phase. The authors thus concluded that the third phase is an osteichthyan synapomorphy that was lost in teleosts, along with the metapterygial axis (Davis et al., 2007). To sum up, the few available data on Hox gene expression patterns in fin and limb buds do not settle the debate on the origin of the autopod (neomorph, or homologue of distal radials), even though several recent studies raise the possibility that the autopod is homologous with the distal part of the fi n (Fig. 4.3).

Vertebrate Limb Evolution / 79

SARCOPTERYGIAN FINS AND THE ORIGIN OF DIGITS

The origin of the autopod (hand and foot) has also been studied using molecular developmental data, as we saw above, but the morphology of the fins of extant and extinct vertebrates also provides critical data on this topic. Among actinopterygians, the paired fi n endoskeleton is composed of a series of small parallel rods (the radials), sometimes accompanied by smaller bones (Fig. 4.3A). In these fins, only the posterior portion, located along the metapterygial axis, can be homologous with the tetrapod limb, although this implies no homology of the individual skeletal elements. The anterior portions of these fins (Fig. 4.3A, in gray) has no homologue among tetrapods. The sarcopterygian paired fi n is monobasal; it articulates with the girdle through a single proximal radial, which is homologous with the humerus or the femur (Fig. 4.3B–F). The distal portion of the fi n is much more variable; the second segment (these skeletal segments are called mesomeres) may consist of a single element (homologous with the radius and ulna, for the anterior appendage), as in the coelacanth (Fig. 4.3B) or in dipnoans (Fig. 4.3C), or of two elements, the radius and ulna, as in various stem tetrapods (Fig. 4.3D–F). The third mesomere, homologous with the wrist and ankle, is even more variable: it may consist of one to as many as five radials. From the fourth mesomere upwards, the morphology is still more variable and its homology is more controversial. These radials may be homologous with metacarpals and metatarsals, the bones that extend from the wrist and ankle to the base of the fi ngers and toes. Similarly, the potential homology between the radials of the fi fth mesomere and the proximal phalanges of fi ngers and toes is highly controversial. After having initially supported homology between the fourth and fifth fin mesomeres and the metacarpals (or metatarsals) and phalanges (early in the 20th century), morphologists and paleontologists rejected

pha mor odo

C r

A

B

C Radius andulna or second mesomere

Withoug homologue in sarcopterygians

in un

u

r

u

r

u

u

r

h

h h

h

Humerus or first mesomere

Incre a Com sing plex ity

in un

h

h

Simp lifica tion

F

ng

Nod e

deni

E

Broa

Nod e

ng

Tetra p

heni

Nod e

Sarc opte

rygii

Oste ichth yes Leng t

D

E

Carpals or third mesomere

Metacarpals or fourth mesomere

F

G Phalanges or fifth mesomere (and more distal portions)

Figure 4.3. Appendicular skeleton of osteichthyans. Right pectoral appendages in dorsal view (the head is to the left). Hatching and shading indicate the hypothesis of maximal homology that can be proposed based on the topology of the elements (Laurin, Girondot, and de Ricqlès, 2000); it is fairly speculative for distal elements (metacarpals and phalanges). Note the great morphological diversity of osteichthyan appendages and the apparent complexity of their evolution. A to C are extant, whereas D to G date from the Late Devonian. The metapterygial axis is shown as a gray line (its distal position in rhizodontids is uncertain; two possibilities are proposed). The fi n of Acipenser, the sturgeon, retains a metapterygial axis which is homologous with the axis in the sarcopterygian fi n and of the stegocephalian limb. parts: A, the actinopterygian Acipenser sturio (sturgeon). B, the actinistian Latimeria chalumnae (the coelacanth). C, the dipnoan Neoceratodus forsteri. D, a rhizodontid. E, the tristichopterid Eusthenopteron foordi. F, Tiktaalik roseae. G, the stegocephalian Acanthostega gunnari. Abbreviations: h, humerus. in, intermedium. r, radius. u, ulna. un, ulnare.

Vertebrate Limb Evolution / 81

Figure 4.4. First hypothesis of the neomorph nature of the autopod. According to Gregory and Raven (1941), most of the autopod is a neomorph (in gray). The pectoral appendages of three sarcopterygians show the hypothesized evolution of fi ns into limbs. The metapterygial axis of the appendage is shown (gray line); it is located elsewhere in tetrapods, according to more recent works. The limb of Eryops actually features four digits, rather than six as shown here. Modified from Gregory and Raven (1941). parts: A, Eusthenopteron fi n (Late Devonian). B, hypothetical intermediate stage. C, limb of Eryops (Early Permian).

this homology in the 1940s. They proposed that the autopod (hand and foot) was a neomorph without homology with the sarcopterygian fin, as if it had been added to the distal extremity of these fi ns (Fig. 4.4). That interpretation was initially proposed by Gregory and Raven (1941). It is not entirely convincing, because we generally consider that the radials of the fi ns of various sarcopterygians are homologous, despite important morphological differences (Fig. 4.3B–F), and numerous

82 / Vertebrate Limb Evolution

transformations must have occurred to explain the diversity of these fi ns. Why should the stegocephalian autopod (Fig. 4.3G) be treated differently? Could it be because of our anthropocentrism? The great similarities between rhizodontid fi ns (Fig. 4.3D) and the limb (Fig. 4.3G) could be interpreted as synapomorphies (implying homology between autopod and fi n), even though that is not the prevailing interpretation in recent works. Such an interpretation, suggesting homology between fi n radials and phalanges, was proposed a decade ago (Laurin, 2000) as a hypothesis that should be tested in the future, but it was ignored for several years. The discovery of a Devonian sarcopterygian named Tiktaalik, which is probably our closest known finned relative (Fig. 4.3F), prompted its describers (Shubin et al., 2006) to propose the hypothesis of homology between fi ns and autopod anew, but with more conviction. Shubin et al. (2006) suggest that the origin of limbs involved the proliferation of structures (endoskeletal radials) that were already present in fi ns such as those of Tiktaalik. However, this idea remains a hypothesis because the morphological gap between the fi n of Tiktaalik and the limb of the first stegocephalians remains substantial. For instance, the preaxial rays of the fi n (located cranial to the metapterygial axis), which are present in Eusthenopteron (Fig. 4.5A), are retained in Tiktaalik (Fig. 4.5B). Yet the presence of these preaxial rays had been used as an argument against the hypothesis of homology between autopod and fi n (Laurin, 2006).

FRAGMENTARY FOSSILS, PHYLOGENY, AND THE FIRST DIGITS

The origin of digits was an important event because digits are part of the autopod, and this structure enabled stegocephalians to walk on emerged land. It was long thought that the fi rst autopods possessed five digits, which is the maximum number normally present (i.e., in nonpathological cases) in extant tetrapods. However, the oldest known

Vertebrate Limb Evolution / 83

A

B

C

Figure 4.5. Appendicular skeleton of tetrapodomorphs. Right appendages of Devonian sarcopterygians in dorsal view (the head of the animal would be to the left). The main (metapterygial) axis is represented by a thick line; the preaxial rays (A, B) are shown as slightly thinner lines. parts: A, the tristichopterid Eusthenopteron foordi. B, Tiktaalik roseae. C, the stegocephalian Acanthostega gunnari.

Figure 4.6. Tulerpeton forelimb. This fossil was found near Tula, in Russia. It dates from the end of the Devonian (Famennian) and comes from a marine environment. The right forelimb is shown in dorsal view (the head of the animal would be to the left). Modified from Lebedev and Coates (1995).

limbs, from the latest Devonian (Famennian, about 360 Ma), all display more than five digits; thus, they are polydactylous. These include the limbs of Acanthostega, whose hand possesses eight digits (Fig. 4.5C), Ichthyostega, whose foot shows seven toes, and Tulerpeton, whose hand has six fingers (Fig. 4.6). From this we can conclude that polydactyly is the primitive condition for stegocephalians, and that pentadactyly, which characterizes tetrapods, appeared later, in the Carboniferous, through a reduction in digit number.

Figure 4.7. Fragmentary fossils attributed to Elginerpeton. These fossils were found in Scotland, but similar remains were also found in the Baltic countries. They date from the Late Devonian (Frasnian). Right (A) and left (B) mandibles in dorsal view; possible left humerus in dorsal (C) and ventral (D) view; right tibia in ventral (E), dorsal (F), and distal views (G). Modified from Ahlberg (1991).

Vertebrate Limb Evolution / 85

However, two points were debated recently. The fi rst is the date of the appearance of digits. The debate originated with the description of fragmentary fossils slightly older (Frasnian, Late Devonian, about 380 Ma) than Ichthyostega. These fossils were called “tetrapods,” even though the distal portion of the appendage is not preserved. The best known of these very old stegocephalians is Elginerpeton, a taxon represented by jaw fragments, a bone that might be a humerus (its identity has been disputed), and a tibia (Fig. 4.7). Another contemporary genus, Obruchevichthys, is represented only by a fragmentary lower jaw. Other Famennian stegocephalians are represented by similarly fragmentary remains. In the absence of preserved digits, we may wonder why several authors have stated that these animals were “tetrapods.” In fact, an optimization of appendage type on a consensual sarcopterygian phylogeny shows that these taxa may not have had digits, except Hynerpeton, which is known from a shoulder girdle (Fig. 4.8). The position of Hynerpeton in the clade of stegocephalians with digits suggests that it had a true autopod. Recently described stegocephalian trackways from the Eifelian (Middle Devonian) of Poland suggest that digits appeared much earlier than previously thought, about 395 Ma ago, rather than about 365 Ma ago (Niedzwiedzki et al., 2010). The authors also suggested that this implied very long ghost lineages at the base of the stegocephalian tree, but this is only one of several possible interpretations. Niedzwiedzki et al. (2010: fig. 5b) placed the Middle Devonian trackway in a polytomy with Acanthostega, Ichthyostega, and the clade that includes Tulerpeton and post-Devonian stegocephalians (at the base of the gray portion, in Figure 4.8). This is the most crownward plausible position for this trackway, and it implies the greatest total duration of ghost ranges. However, the trackway could also represent the sister group of the more inclusive clade that includes Elginerpeton, Obruchevichthys, Ventastega, Metaxygnathus, and more crownward stegocephalians (thus appearing in the most basal position in stegocephalians). This second possible position of

86 / Vertebrate Limb Evolution

the trackway would imply the presence of limbs in the basalmost stegocephalians (Elginerpeton and the three others mentioned above), and it would require a much shorter ghost range of early stegocephalians because a single lineage leading to the Late Devonian stegocephalians needs to be assumed. In any case, these trackways were made in a fully marine, intertidal environment (Niedzwiedzki et al., 2010), and this supports a marine origin of stegocephalians, as discussed in Chapter Three. Another controversial topic is the number of appearances of pentadactyly. A popu lar hypothesis in the 1980s and 1990s suggested that the reduction to five digits per autopod occurred independently in am-

Post-Devonian Stegocephalias

Hynerpeton

Tulerpeton

Ichthyostega

Acanthostega

Metaxygnathus

Obruchevichthys Ventastega

Elginerpeton

Panderichthyids

Tristichopterids

Megalichthys

Osteolepis

Rhizodontids

Dipnoans

Stegocephalians

Appendage type Fin Polydactylous limb Pentaactylous limb Uncertain, fin or polydactylous limb Uncertain, polydactylous or pentactylous limb

Figure 4.8. Appendage evolution in sarcopterygians. This tree emphasizes stegocephalians. Note that the numerous Devonian taxa (from Elginerpeton to Metaxygnathus) represented by fragmentary remains, often described as “tetrapods,” may not have had digits. Modified from Laurin, Girondot, and de Ricqlès (2000).

Vertebrate Limb Evolution / 87

phibians and in reptiliomorphs (the group that includes amniotes and extinct related taxa). The most recent analyses suggest instead that pentadactyly appeared only once, in stem tetrapods, before the appearance of amphibians and reptiliomorphs (Fig. 4.9). This implies that our last common ancestor with lissamphibians (frogs, salamanders, and gymnophionans) already possessed pentadactyl limbs.

Stem tetrapods

Amphibia

“Lepospondyls”

Osteolepiformes Panderichthyidae Acanthostega Ichthyostega Tulerpeton Loxommatidae Crassigyrinus Colosteidae Dendrerpeton Eryops Ecolsonia Tersomius Apateon Amphibamus Doleserpeton Gephyrostegidae Proterogyrinus Archeria Kotlassia Seymouria Ariekanerpeton Westlothiana Aistopoda Adelogyrinidae Nectridea Pantylus Rhynchonkos Brachystelechidae Lysorophia Triadobatrachus Discoglossidae Pipidae Karaurus Hynobiidae Proteidae Sirenidae Eocaecilia Rhinatrematidae Ichthyophiidae Limnoscelis Diadectes Synapsida Captorhinidae Procolophonidae

Temnospondyli Embolomeri

Reptiliomorpha

1&2

1/2

Tetrapoda

Digit number evolution in the hand

Dichotomy closest to what Coates interpreted as the divergence between amphibians and reptiliomorphes.

(0) more than five (1) five (2) four Ambiguous, states 0, 1, or 2 Ambiguous, states 1 or 2

Most recent divergence in which polydactyly may have been lost (reduction to five digits or less). Stegocephali

Figure 4.9. Evolution of digit number in the stegocephalian hand. This tree shows the unique appearance of pentadactyly (in gray) from the ancestral polydactylous condition (in white) in the stegocephalian forelimb. Additional losses of digits yielded tetradactyl hands (in black) in temnospondyls and in amphibians. Modified from Laurin (1998a).

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THE GILLS OF ACANTHOSTEGA AND THE ORIGINAL FUNCTION OF THE TETRAPOD LIMB

The limb with digits was initially considered a terrestrial adaptation. This hypothesis has recently been rejected because it is likely that the first vertebrates with such limbs were fully aquatic. The limb thus appears to be an exaptation (sometimes called pre-adaptation) to terrestrial life because its initial function was not to enable stegocephalians to walk on dry land, even though it fulfi lled that function later when stegocephalians invaded the land. This new hypothesis rests on the inference that the oldest stegocephalians were aquatic. That interpretation was first suggested for Acanthostega, based partly on grooves on the hyobranchial skeleton, which supports the larynx in tetrapods, and gills in other vertebrates. These grooves probably housed arteries that carried blood to the gills, where carbon dioxide would have been released into the water and oxygen would have entered the blood. A bony lamella on a bone of the shoulder girdle (the cleithrum) seems to have formed part of the posterior wall of the branchial chamber. Together, these two characters strongly suggest that functional internal gills were present. Furthermore, the tail retained fin rays (lepidotrichia) similar to those of primitively aquatic osteichthyans (Fig. 4.1). The skeleton of Acanthostega was poorly ossified (much of it remained cartilaginous throughout life), as frequently occurs in aquatic tetrapods. All these clues suggest an aquatic lifestyle in Acanthostega. If all these characters were present only in Acanthostega, we might think that this stegocephalian was atypical and had returned to an aquatic lifestyle, like so many extant tetrapods (seals, whales, marine turtles, etc.). However, all Devonian stegocephalians seem to have been aquatic because the associated fauna is typically aquatic (often marine or coastal), several seem to have retained internal gills (the others are too poorly known to determine if gills were present), and Ichthyostega also retained the fin rays (lepidotrichia) in the tail. Given the aquatic

Vertebrate Limb Evolution / 89

lifestyle of the earliest stegocephalians and their aquatic ancestry, we may conclude that the aquatic lifestyle is primitive for stegocephalians.

BONE MICROANATOMY AND LIFESTYLE

Extant Tetrapods To infer the lifestyle of early stegocephalians, scientists have developed a method based on appendicular long bone microanatomy (especially on the femur, humerus, radius, and tibia) as seen in cross section. These bones initially develop as prechondrogenic condensations (i.e., they form before cartilage appears) that soon start secreting a cartilaginous matrix. Then the membrane that surrounds the cartilage (the perichondrium) transforms into a periosteum that secretes a bony matrix (except at the articulations, which must remain cartilaginous to allow movement between bones). The initial cartilage of vaguely cylindrical shape (it is generally thinner in the midshaft than near the articular ends) is thus encased in a bony cylinder that thickens quickly. This cartilage is often entirely resorbed in ontogeny. Bones elongate mostly through cartilage development at the articular ends, which we call epiphyses, by opposition to the shaft, which we call the diaphysis. We also recognize a transitional zone between epiphyses and diaphysis, which we call the metaphysis. The epiphyses are generally covered in cartilage, but they may have an ossified center, especially in mammals (but not in amphibians). The metaphysis consists of a thin layer of compact bone, called the cortical compacta (or sometimes “cortex”) that surrounds deeper spongy bone (the medullary spongiosa). The diaphysis usually has a thicker cortical compacta and less (if any) medullary spongiosa, at least in most terrestrial tetrapods. We have long known that the cross-sectional aspect of the long bones reflects (among other things) the habitat. Terrestrial tetrapods generally have a moderately thick, compact cortex (Fig. 4.10A), whereas amphibious tetrapods have more compact bones with a thicker cortex (Fig. 4.10B). Aquatic tetrapods may display either very compact bone

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Figure 4.10. Long bones of extant tetrapods of various lifestyles. Mid-diaphyseal cross sections of appendicular long bones. These drawings are not to scale. parts: A, humerus, Cervus elaphus (deer, terrestrial; maximal diameter: 29.2 mm). B,  femur, Ornithorhynchus anatinus (platypus, amphibious; maximal diameter: 6.0 mm). C, humerus, Delphinus delphis (dolphin, aquatic; maximal diameter: 33.3 mm).

with a thick cortex, or spongy bone (Fig. 4.10C). The greatest habitatrelated differences occur in the mid-diaphyseal (midshaft) region, because the metaphysis and the epiphyses nearly always have a thin cortex and an extensive spongiosa. Recent research on a correlation between habitat use and bone microanatomy required thin sections (about 0.05 mm) of long bones in mid-diaphyseal cross sections. These sections were then digitized and analyzed using a custom software application called Bone Profi ler that divides the section surface into thousands of small polygons (Fig. 4.11). The program then measures compactness (the ratio between surface covered by bone and total surface) within each polygon. It then fits a mathematical function to the data (Fig. 4.12); that function represents the compactness profile, which describes compactness (Y ) as a function of position along the section radius (X ), from the center (X = 0) to the periphery (X = 1). The model requires estimating four parameters: Min, the lower asymptote, which generally reflects compactness in the section center; Max, the upper asymptote, which generally reflects compactness in the superficial cortex; P, the position of the inflexion point on the x-axis, which reflects the diameter of the medullary spongiosa; and S, which reflects the width of the transition zone between medullary and cortical regions. This model captures more information from the bone sections than simpler characters that were used in previous

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Figure 4.11. Sampling scheme used by Bone Profi ler to model long bone cross sections. The program delimits 51 concentric zones (Z1 to Z51), which measure 2% of the section diameter, except for the two most superficial zones, which measure only 1% of the diameter, to better model sections with a very thin cortex (as in birds and pterosaurs). Bone Profi ler also delimits 60 radial sectors of 6° width (360°/60). The intersection between these zones and sectors delimits 3060 polygons (51 × 60) whose compactness is calculated. The parameters of the compactness profi le (S, P, Min and Max) can be estimated either on the whole section in a single step (thus yielding a single value for each), or on each radial sector (which yields 60 values per parameter, and allows estimating the variance of the parameters reflecting heterogeneities on the section). Reproduced from Laurin et al. (2004).

studies (Laurin et al., 2006), such as global compactness or the corticodiaphyseal index (which is the ratio between cortical compactness and diameter), or CDI for short. The relationship between CDI and P is simple: CDI = 1 – P, so using the new model allows comparison with results from previous studies. The four parameters of the function (S, P, Min, and Max) and the habitat of many species of vertebrates can then be analyzed through

Compactness

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1.0 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0

Max

∂Y

S = ∂X/∂Y P ∂X 0.0 0.1 0.2 0.3 0.4 0.5

Section center

Min

0.6 0.7 0.8 0.9 1.0

Position

Periphery

Figure 4.12. Compactness profi le model. The x-axis reflects the position on the section (0 is the center, and 1, the periphery). In this hypothetical example, there would be a medullary spongiosa, as in figure 4.10C (Delphinus), but the cortex would be thicker. Modified from Laurin et al. (2004).

statistical tests to determine which combinations of these parameters characterize aquatic, amphibious, and terrestrial species, and more importantly, to show that this relationship is statistically significant. A database on bone microanatomy encompassing more than 200 extant tetrapod species is currently being analyzed (Laurin et al., 2009). These analyses should improve our understanding of bone microanatomy evolution that occurred as a response to habitat shifts in tetrapods. They have already shown statistically significant differences among aquatic, amphibious, and terrestrial species. Flying vertebrates were not studied, because fl ight imposes different constraints and flight capability can usually be assessed from morphology.

Paleozoic Stegocephalians Bone microanatomical data can be used to infer the habitat of early stegocephalians. To do this, we need only obtain bone sections of the species whose lifestyle we wish to infer. A database of such sections encompassing more than 30 species of early stegocephalians has been compiled and is being analyzed (Kriloff et al., 2008). Once the inferences are available, habitat use can be optimized onto a time-calibrated tree, and

Vertebrate Limb Evolution / 93

Figure 4.13. Section of the radius of Ophiacodon. This section comes from an Early Permian specimen (about 290 Ma). Note the thick cortex.

the history of the invasion of land by vertebrates can be analyzed. This phylogeny should be based on the ages of all known stegocephalian fossils, not only on the species whose habitat has been inferred, and molecular ages can also be used (Laurin et al., 2009). This method is necessary to avoid underestimating the geological age of the hypothetical ancestors on the tree, and thus to get an accurate age of the habitat shifts. So far, only preliminary inferences have been obtained. The most interesting are briefly discussed here. One concerns Ophiacodon (Fig. 4.13), one of the oldest known amniotes (Late Carboniferous and Early Permian), which from the 1950s to the early 1960s was considered very similar to the ancestor of all amniotes. At that time, the first amniotes were thought to have retained an aquatic or amphibious lifestyle, and Ophiacodon, whose morphology seemed compatible with these lifestyles (Fig. 4.14), was often cited as the best evidence supporting this hypothesis. The description of the earliest known amniote fauna from Joggins, Nova Scotia, led to the rejection of Romer’s (1957) ideas because Hylonomus, the best-preserved reptile from that locality, was plausibly interpreted as a terrestrial animal (Carroll, 1964). However, Joggins may represent an unusual taphonomic assemblage of terrestrial and

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Figure 4.14. Ophiacodon in its habitat. This amniote, from the Late Carboniferous and Early Permian, was long considered amphibious or even aquatic. Drawing by Douglas Henderson initially published by Czerkas and Czerkas (1990). Reproduced with permission.

amphibious taxa, and this does not preclude the existence of aquatic or amphibious amniotes elsewhere (Canoville and Laurin, 2010). Bone microanatomy supports the hypothesis that Ophiacodon retained an amphibious to aquatic lifestyle (Germain and Laurin, 2005; Kriloff et al., 2008), because the long bones of this amniote were relatively compact (Fig. 4.13) or display an extensive medullary spongiosa, as in many aquatic vertebrates (Fig. 4.10B, C). Microanatomical data suggest an amphibious lifestyle for Captorhinus, a taxon usually considered fairly terrestrial, and various paleobiological inferences suggest that the earliest amniotes may have retained the amphibious lifestyle of their distant ancestors (Canoville and Laurin, 2010), thus adding support for Romer’s (1957) views. Another preliminary inference was obtained for Doleserpeton, an Early Permian stegocephalian that was long considered closely related

Vertebrate Limb Evolution / 95

Figure 4.15. Cross section of a Doleserpeton femur. This section shows the compact, moderately thick cortex (thinner than in Ophiacodon) and the large medullary cavity (A). The corresponding compactness profi le produced by Bone Profi ler is typical of terrestrial vertebrates (B). This section is from an Early Permian specimen (about 290 Ma).

to extant amphibians (Bolt, 1969; Trueb and Cloutier, 1991), although recent research suggests that it is a stem tetrapod (Vallin and Laurin, 2004; Marjanovié and Laurin, 2008). It is generally thought to have been terrestrial (Bolt, 1977), like most other dissorophoids. Again, bone microanatomy confirms previous interpretations because the long bones display a moderately thick, compact cortex and a large medullary cavity (Fig. 4.15) typical of terrestrial vertebrates.

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An example of the ultimate goal of this research is provided by a recent study that inferred the habitat of early stegocephalians based on several characters (Fig. 2.5). These preliminary results include a timecalibrated tree and trace the complex history of the invasion of land by vertebrates. These results provide an initial hypothesis that can be tested as more reliable results are obtained. More than one acquisition of amphibious and terrestrial lifestyles may have occurred, and several taxa independently returned to a more aquatic lifestyle.

. . . The vertebrate skeleton is composed of a dermal portion, which was superficial in the first vertebrates and is largely restricted to the skull and shoulder girdle in extant tetrapods, and an endoskeletal component, which makes up the vertebral column, most of the appendicular bones, and part of the skull. The autopod (hand and foot) is entirely endoskeletal. Work on Hox gene expression in vertebrate appendicular development has been claimed to show that the autopod is a neomorph. Unfortunately, since these data come from few species, their interpretation is difficult, but the latest work casts doubt on these conclusions and suggests that the loss of the metapterygial axis in teleosts is responsible for the differences observed between Danio and tetrapods. Morphologists and paleontologists initially considered that the autotpod was homologous with the fi n tip (early in the 20th century), but later (from the 1940s onwards) concluded that it was probably a neomorph. Recently, some authors reverted to the initial hypothesis of homology between autopod and distal fi n, but the available data are too scanty to allow a definitive conclusion. Digits (fingers and toes) appeared between 380 and 360 Ma ago. This date is imprecise because fragmentary fossils from that period show the presence of close relatives of limbed vertebrates, but the presence of digits in these enigmatic species is uncertain. The oldest skeletal remains of digits are from the Fammenian (360 Ma ago), although stego-

Vertebrate Limb Evolution / 97

cephalian trackways showing digits were recently described from the Middle Devonian. The first limbs were polydactylous and possessed six to eight digits. Pentadactyly appeared in the Carboniferous, probably only once, in stem tetrapods. The first stegocephalians were probably primitively aquatic. Thus, the autopod is not an adaptation to life on dry land; instead, it should be considered an exaptation. New methods to infer the lifestyle of early stegocephalians are under development. One of them uses long bone microanatomy and statistical study of vertebrates (mostly extant) of known lifestyle.

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chapter five

Diversity of Paleozoic Stegocephalians

Among vertebrates, only stegocephalians have an autopod. Thus, stegocephalians include all terrestrial and most amphibious vertebrates. The main invasion of land by vertebrates occurred in the Carboniferous. To understand this event, a survey of the biodiversity and phylogeny of early stegocephalians is useful.

TEMNOSPONDYLS

Temnospondyls form a large group in which more than 150 genera are recognized. They appeared in the Early Carboniferous (about 340 Ma ago) and vanished in the Cretaceous, about 100 Ma ago. They include, among others, Eryops and Mastodonsaurus. Temnospondyls were midsized to large, generally between 30 cm and 3 m in total body length, but at least one species may have reached about 7 m (Steyer and Damiani, 2005). Throughout their history, temnospondyls have colonized various terrestrial and aquatic (salt- and freshwater) habitats. The oldest ones seem to have been amphibious, but in the Permian some species were terrestrial, at least as adults, whereas others were amphibious or aquatic (Fig. 5.1). They had four digits in the hand, and five in the foot. 99

Figure 5.1. Two Early Permian temnospondyls (280 Ma ago). These temnospondyls are shown in their presumed habitat. Eryops (the largest one) lunges to catch a chondrichthyan (a xenacanthid) while Trimerorhachis (smaller) escapes. The hand of Eryops actually had only four digits. Drawing by Douglas Henderson initially published by Czerkas and Czerkas (1990). Reproduced with permission.

Diversity of Paleozoic Stegocephalians / 101

The ribs of temnospondyls are often rather short, and when they are long, as in Eryops, they sometimes overlap. This strengthened the rib cage (as in birds) but prevented costal ventilation of the lungs. This suggests that other structures were responsible for bringing fresh air into the lungs. The large interpterygoid window in the palate of temnospondyls suggests the presence of a buccal pump analogous with that of anurans (Gans, 1970). Muscles may have enabled rhythmic increases in the mouth volume by raising the skin that closed the interpterygoid window, and by depressing the floor of the mouth. After closing the mouth and the nostrils, relaxing these muscles could have forced air into the lungs, through elastic recoil of the buccal skin. (See the box titled “The temnospondyl Iberospondylus schultzei.”)

The Temnospondyl Iberospondylus Schultzei This temnospondyl is the oldest known stegocephalian in the Iberian Peninsula. It dates from the Late Carboniferous (Stephanian C, between 302 and 304 Ma ago) and comes from near Puertollano, in the Ciudad Real province, in the center of Spain (Laurin and Soler-Gijón, 2006). It is a midsized Carboniferous temnospondyl (the skull length is 14 cm). It must have been amphibious because traces of the cephalic portion of the lateral line organ remain. Three well-preserved articulated individuals were found in the locality, and such a preservation mode suggests only a short postmortem transport of the carcasses. It seems to have tolerated salt or brackish water because the locality appears to have been coastal, and unmistakable evidence of marine influence has been found (Soler-Gijón and Moratalla, 2001). Iberospondylus is thus the oldest known temnospondyl in which saltwater tolerance is reasonably well established (the most famous and least disputed examples date mostly from the Triassic). The good preservation of the specimens may explain the presence of an otic lamella that continued

102 / Diversity of Paleozoic Stegocephalians

continued

occluded the otic notch; this indicates that this animal lacked a tympanum (ear drum). It must not have heard high-frequency airborne sounds well, but it probably heard well enough those of low frequency (less than 1000 Hz) and those transmitted in water or in the ground. Iberospondylus seems to occupy a fairly basal place among temnospondyls (Laurin and Soler- Gijón, 2006).

Skull of the temnospondyl Iberospondylus. A dermal ornamentation typical of temnospondyls is visible in dorsal view (left). The palatal view shows the large interpterygoid vacuity, also typical of this group. The scale is in centimeters. Modified from Laurin and Soler- Gijón (2001).

Temnospondyls experienced two extensive evolutionary radiations. The first one occurred from the Early Carboniferous to at least the end of the Early Permian. Temnospondyl diversity seems to have decreased in the Middle and Late Permian, but the low number of fossils from these times is insufficient to determine if this decrease was gradual, or if it occurred suddenly at the end of the Permian, when the biosphere experienced its greatest extinction event, at least in the oceans and seas. The Permo- Carboniferous temnospondyls have often been called

Diversity of Paleozoic Stegocephalians / 103

“rhachitomous,” after their vertebral centrum (the part of the vertebra that located below the spinal cord; it surrounds the notochord and partly replaces it). That centrum is composed of a small, paired, dorsal pleurocentrum that articulates with the neural arches, and a small, crescentic intercentrum. Rhachitomous temnsopondyls form a paraphyletic group, since they include some close relatives of geologically more recent temnospondyls. The second evolutionary radiation of temnospondyls started in the Late Permian and gave rise to a great diversity of forms, most of which belong to the taxon Stereospondyli, also named after the morphology of its vertebral centrum. The stereospondyl centrum is composed of a large, relatively cylindrical intercentrum; the pleurocentrum is either absent, unossified, or very small. Starting with the Triassic, most temnospondyls were aquatic (Fig. 5.2) and fairly large (1.5 m to 3 m in total body length) and belong to the Stereospondyli. Among all early stegocephalians, the ontogeny is best known in temnospondyls, because they are the most abundant Paleozoic stegocephalians in the fossil record. Aquatic larvae with external gills are known for a few temnospondyl species, and they were probably present in most species (Fig. 5.3). These larvae superficially resemble those of urodeles (salamanders and newts), but this does not imply close affinities, since seymouriamorphs also possessed such larvae; this developmental mode is probably primitive for stegocephalians. Temnospondyls played a prominent role in theories about the origin of extant tetrapods because they were long considered to represent the stem group of anurans (Fig. 5.4A) or of all lissamphibians (Fig. 5.4B), and this remains a popular (but controversial) theory today. This may explain why the first reconstruction of the temnospondyl Mastodonsaurus looked like a huge frog, with a stubby body (we now know that it has a long, slender body with proportions more reminiscent of urodeles). These ideas hark back to the works of E. D. Cope, a pioneer of North American paleontology. They prevailed from the 1880s to the end of the 1990s. However, several recent studies that used computer-assisted phylogenetic analyses raise serious doubt about these theories (Laurin, 1998b; Vallin and

Figure 5.2. Metoposaurus, a large aquatic stereospondyl from the Triassic (210 Ma). This temnospondyl belongs to the Stereospondyli, which diversified intensively in the Triassic. Drawing by Douglas Henderson initially published in Long and Houk (1988). Reproduced with permission.

Figure 5.3. Larvae of the temnospondyl Tupilakosaurus wetlugensis. Larvae with external gills are known in a few temnospondyl species. Photo taken by the author in the Paleontological Institute (Moscow).

Urodela Gymnophiona Anura

Amniota io til ha ep p R or m

io til ha ep p R or m m

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Figure 5.4. Phylogenetic hypotheses about the position of temnospondyls. The systematic position of temnospondyls is highly contentious. They have been considered to represent all or part of the stem group of anurans (A) or of all lissamphibians (B), or to be stem tetrapods (C). Temnospondyls are monophyletic only under this latter interpretation (C). Crosses designate extinct taxa. Extant taxa are emphasized in bold type. The name “Lissamphibia” is generally used only if the smallest clade that includes all extant amphibians excludes all currently known Paleozoic stegocephalians, such as temnospondyls (B, C). Amphibians are shown in dark gray, and reptiliomorphs, in light gray.

106 / Diversity of Paleozoic Stegocephalians

Laurin, 2004; Marjanovic´ and Laurin, 2008, 2009); temnospondyls seem to be stem tetrapods (Fig. 5.4C), and as such, are no closer to extant amphibians than to amniotes. This last hypothesis is accepted in this book, although alternatives are discussed. Thus, temnospondyls are not considered amphibians.

EMBOLOMERES

Embolomeres include only 16 genera and extend only from the Carboniferous (around 340 Ma ago) to the Triassic (around 220 Ma ago). Their geographic range comprised what is currently North America and European Russia, regions that were then part of Euramerica. Most measured between 1.5 m and 2.5 m in total length and were aquatic to amphibious, as shown by the frequent presence of grooves for the cephalic portion of the lateral-line organ and their long, deep tail, which was probably used for swimming. However, in the Triassic, some embolomeres found in Russia (the chroniosuchians) included terrestrial species (Fig. 5.5). The skull retains the intertemporal, a bone that had disappeared in most other stegocephalians by the Early Permian. The massive stapes suggests that the otic notch did not support a tympanum. These animals must have had fairly poor hearing on dry land. Palatal fangs suggest that they fed on relatively large prey. The relatively long ribs suggest that they had a good costal lung ventilation capability. Like those of many early stegocephalians, both hand and foot retained five digits. They are characterized by a peculiar type of vertebral centrum composed of two cylinders (Fig. 5.6B). The primitive configuration for stegocephalians, as seen in temnospondyls, Ichthyostega, and other a few other Devonian sarcopterygians, consists of a rhachitomous centrum (Fig. 5.6A). Since their discovery in the 19th century and until the 1990s, embolomeres have been considered to be among the basalmost reptiliomorphs (Fig. 5.7A). The character that initially justified this hypothesis in the 1880s (the presence of a single, median occipital condyle) has long been rejected because we now know that this character is primitive for stego-

Figure 5.5. Chroniosuchian. This embolomere from the Late Permian and the Triassic lived in what is now Russia and was probably terrestrial. Large bony scutes on its back articulated with the neural spines and strengthened its axial skeleton, presumably to improve its ability to support the body weight outside the aquatic environment. Photo taken by the author in the Paleontological Institute (Moscow).

Figure 5.6. Stegocephalian vertebrae in right lateral view. Rhachitomous temnospondyl vertebra (A) showing the primitive morphology for stegocephalians (a ventral, crescentic intercentrum and a paired, dorsal pleurocentrum) and embolomerous vertebra of Eogyrinus, showing a centrum composed of two cylindrical elements (B). The intercentrum is in light gray, and the pleurocentrum, darker. The neural arch, in white, surrounds the spinal cord and is not fused to the vertebral centrum, contrary to most extant tetrapods. Cranial is to the right.

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io til ha ep p R or m m

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Urodela Gymnophiona Anura

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Figure 5.7. Phylogenetic position of embolomeres. Only the main phylogenetic hypotheses are shown. In A, Embolomeres as reptiliomorphs. This hypothesis prevailed from the 1880s to the 1990s. In B, Embolomeres have been placed among stem tetrapods by most computer-assisted analyses from the 1990s onward.

cephalians, but other more convincing characters were proposed. For instance, two bones of the dermal skull roof (parietal and tabular) that are separated from each other in most other stegocephalians share a suture in embolomeres, amniotes, and other presumed reptiliomorphs (Fig. 5.8). Another potential synapomorphy of these taxa is the long posterior stem of the interclavicle (the stem is absent in temnospondyls and more basal taxa). However, most recent computer-assisted phyloge-

Diversity of Paleozoic Stegocephalians / 109

Figure 5.8. Stegocephalian skulls. These skulls show the primitive condition for the relative position of the parietal (P) and the tabular (T), in which these bones are widely separated from each other by intervening bones, as in Ichthyostega (A), and the condition, often considered characteristic of reptiliomorphs (but more likely a synapomorphy of a larger clade), of the presence of a contact between both bones, as seen in embolomeres, seymouriamorphs (B) and amniotes. Parietal and tabular in dark gray; postparietal and supratemporal in light gray. Scale: 1 cm.

netic analyses (e.g., Vallin and Laurin, 2004; Marjanovié and Laurin, 2009) suggest that embolomeres are stem tetrapods (Fig. 5.7B). The characters that have been interpreted as synapomorphies of embolomeres and other presumed reptiliomorphs probably appeared in stem tetrapods. (See the box titled “The embolomere Proterogyrinus scheelei.”) SEYMOURIAMORPHS

Seymouriamorphs have so far been found only in Permian localities, which is surprising given that all plausible phylogenies suggest that this group must have appeared in the Carboniferous (Fig. 5.9). This great gap in their fossil record may result from an erroneous dating of some localities where they occur. Indeed, seymouriamorph-bearing localities in Kazakhstan, Tadjikistan, and Xinjiang (China), which were all on the Kazakhstan plate in the Carboniferous, have been dated as Permian, but

Ural (Eurasia)

Mongolia

Panthalassa

Northern China (North America)

Southern ChinaSima Paleo-Tethys

(South America)

Cimerian block (Africa) Tethys

Glaciation

(Australia)

Figure 5.9. Geograph ical distribution of seymouriamorphs. This map shows the position of continental plates in the Middle Permian (265 Ma ago) and the areas that have yielded seymouriamorph fossils (large black dots). The Kazakhstan continent is framed into a black polygon. Modified from Gradstein et al. (2004).

The Embolomere Proterogyrinus Scheelei This embolomere, among the oldest ones, was found in West Virginia and dates from the Early Carboniferous (Serpukhovian, about 318 to 326 Ma ago). With a skull length of about 12 cm, it was smaller than most later embolomeres, whose skull usually measured between 15 and 35 cm. Grooves for the lateral-line organ on the skull, the weak ossification of the appendicular skeleton, the absence of neurocentral fusion (between neural arch and vertebral centrum), and the long, deep tail, in which the haemal and neural arches may have supported a fi n, suggest a mostly aquatic lifestyle. The otic notch may have housed a spiracle, the fi rst gill slit, which oxygenates blood going to the head. The intercentrum of Proterogyrinus retained the primitive crescentic shape that was lost in later embolomeres, in which this bone became cylindrical. Proterogyrinus is probably a fairly basal embolomere (Holmes, 1984).

Diversity of Paleozoic Stegocephalians / 111

Skull in lateral (A), dorsal (B), and palatal (C) view, and skeleton (D). In dorsal view (B), note the intertemporal (It) and the contact between tabular (t) and parietal (p). The palate (C) shows a very small interpterygoid vacuity (Fi), contrary to temnospondyls. The palatal (C) and lateral (A) views also shows the large palatal fangs. A groove for the lateral-line organ is visible behind and below the orbit (A, B). Reproduced from Holmes (1984, figs. 1, 3) with permission from the Royal Society of London.

Figure 5.10. Skull of Seymouria baylorensis. Cranial reconstruction of Seymouria baylorensis, the fi rst seymouriamorph ever described (Broili, 1904).

Figure 5.11. Skeleton of Seymouria. Skeleton of Seymouria sanjuanensis, from the Early Permian of Germany. Photo provided by D. Berman. Reproduced with permission of the Carnegie Museum of Natural History and the Museum der Natur, Gotha, Germany.

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Figure 5.12. Seymouriamorph vertebra. The pleurocentrum (dark gray) of the vertebral centrum is fi rmly fused to the neural arch (white). The intercentrum is small and crescentic (light gray).

this rests largely on the seymouriamorphs. Phylogenetic analyses suggest that the seymouriamorphs found on this continent were among the oldest, most basal ones. Furthermore, this plate collided with the Euramerican plate (which included European Russia and North America, among other regions) early in the Permian. If seymouriamorphs had first appeared on the Kazakhastan plate in the Carboniferous, the collision between these plates could explain the sudden appearance of seymouriamorphs in Euramerica in the Early Permian. Fewer than 15 genera are recognized (Laurin, 2000; Bulanov, 2003), and most seem to have been terrestrial as adults (Fig. 5.10). This is suggested by the high degree of ossification of their endoskeleton (Fig. 5.11), by the neurocentral fusion (Fig. 5.12), and by the presence of seymouriamorphs in some fossiliferous localities, such as Fort Sill in Oklahoma, in which only fairly terrestrial taxa are encountered. Furthermore, seymouriamorphs may have been among the first stegocephalians with a tympanic middle ear (adapted to hear high-frequency airborne sounds, such as most animal vocalizations). The gracile stapes (the main ear ossicle) was capable of transmitting high-frequency sounds. The otic notch, at the back of the skull (Fig. 5.10), may have supported the tympanum. They were initially considered amniotes (Broili, 1904), because of their presumed terrestrial lifestyle and because of presumed synapomorphies

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Lissamphibia Urodela Gymnophiona Anura

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with amniotes (see “Embolomeres” earlier in this chapter), but the discovery of aquatic larvae with external gills in the 1940s (see the box titled “The seymouriamorph Discosauriscus austriacus”) showed that this hypothesis was false (amniotes lack larvae). Nevertheless, most paleontologists thought that seymouriamorphs were reptiliomorphs at least until the 1990s (Fig. 5.13A). As for embolomeres and temnospondyls, most recent phylogenetic analyses suggest that seymouriamorphs are stem tetrapods (Fig. 5.13B).

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Figure 5.13. Systematic position of seymouriamorphs. Only the main phylogenetic hypotheses about seymouriamorphs are shown. A, Among reptiliomorphs. This hypothesis prevailed from their discovery till the 1990s. B, Among stem tetrapods. This hypothesis is supported by most computer-assisted analyses published from the late 1990s onwards.

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The Seymouriamorph Discosauriscus Austriacus This seymouriamorph found in the Czech Republich dates from the Early Permian (Sakmarian, about 285 to 295 Ma ago). It is represented by growth series documenting its ontogeny, from aquatic larvae with external gills with a weakly ossified endoskeleton to

The seymouriamorph Discosauriscus austriacus. This skull (A, specimen K 13) represents a late larval or metamorphic stage. To the right, the sclerotic ring (that protects the eye) is visible in the orbit. Grooves for the lateral-line organ are visible between the nares and orbits; the temporal ramus of this organ extends to the upper edge of the otic notch. The skeleton (B) is from a young postmetamorphic individual. Reproduced with permission (from the Royal Society of London [A] and from the Royal Society of Edinburgh [B]) from Klembara (1997, fig. 2) and Klembara and Bartík (2000, fig. 1). continued

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continued

postmetamorphic individuals that had lost their external gills. The good ossification of the latter suggests a fairly terrestrial lifestyle. It was long thought that even the largest known individuals were relatively young (less than two years old), but recent skeletochronological study showed that these specimens were sexually mature and about ten years old (Sanchez et al., 2008). For a long time, it was considered a temnospondyl, because it had been confused with branchiosaurs, a group of temnospondyls also represented by growth series including many larvae. The growth series of Discosauriscus show that the relative size of the eye decreases throughout ontogeny, as in most vertebrates. Discosauriscus is one of the few known stegocephalians that seems to have possessed electrosensory organs (Klembara, 1994). The gracile stapes of the closely related taxon Seymouria suggests that the otic notch of Discosauriscus supported a tympanum enabling it to hear high-frequency airborne sounds.

AMPHIBIANS

Amphibians include the lissamphibians (anurans, urodeles, and gymnophionans) and extinct taxa that are more closely related to lissamphibians than to amniotes (see “Are Animals Still Conquering the Land Today?” in Chapter Two). According to this definition, the stegocephalian groups described above are not amphibians, even though they have been (and often still are) considered as such by many authors. Genuine amphibians appeared in the Early Carboniferous (about 340 Ma ago); Paleozoic amphibians include all or most taxa that have collectively been called “lepospondyls” (Fig. 5.14), but since this name probably designates a paraphyletic group, it will not be used below. The term “amphibian” is preferable. Paleozoic amphibians were generally small (from 10 cm to 30 cm in total body length). Several synapomorphies suggest that these taxa are

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Lissam“Lepospondyls” phibia

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Adelogyrinidae Aïstopoda Nectridea

Lysorophia Urodela Gymnophiona Anura

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Figure 5.14. Amphibian phylogeny. The “lepospondyls,” only known from the Paleozoic, have nearly always been considered amphibians, but their relationships to extant amphibians and temnospondyls (often considered amphibians) is fairly controversial. The hypothesis presented here is from Laurin (1998b).

closely related to each other, with the possible exception of adelogyrinids (Ruta and Coates, 2007). For instance, amphibians have lost the complex labyrinthine infolding of the dentine that characterized the teeth of the first stegocephalians (Fig. 5.15) and that gave them the name “labyrinthodonts” (this designates a paraphyletic group, so this name is not used here). The neural arches fused firmly to the vertebral centrum early in ontogeny (Fig. 5.16), contrary to other stegocephalians, whose neural arches fused to the centrum only in adults, if at all. Paleozoic amphibians include several taxa (Fig. 5.17), such as the limbless adelogyrinids and aïstopods; the lysorophians, with diminutive limbs, and a long, slender body that could reach a length of 1 m; and nectrideans, characterized by neural and haemal arches with broadened, crenulated distal ends (Fig. 5.16). Many amphibians are usually classified among “microsaurs,” but this is a paraphyletic group that

Figure 5.15. Labyrinthine infolding of the tooth dentine. This type of tooth characterizes most early stegocephalians (temnospondyls, embolomeres, seymouriamorphs, etc.). Amphibians lack such dentine infolding. Reproduced from Owen (1860).

Figure 5.16. Nectridean vertebra. The shape of the neural (white) and haemal (light gray) arch is unique to nectrideans, but the fusion between the neural arch and the vertebral centrum (dark gray) is a synapomorphy of nearly all amphibians.

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Figure 5.17. Paleozoic amphibians. A lysorophian (with a slender body and tiny limbs) is surrounded by several individuals of the nectridean Diplocaulus of various growth stages. The adults of the latter have a very broad head shaped like a triangle. Drawing by Douglas Henderson initially published by Czerkas and Czerkas (1990). Reproduced with permission.

includes Paleozoic amphibians that do not fit into the other taxa mentioned above (adelogyrinids, aïstopods, etc.). The name “Microsauria” will not be used further in this book. We know almost nothing about the ontogeny of Paleozoic amphibians because their larvae have almost never been fossilized. It has been suggested that Microbrachis (see the box titled “The amphibian Microbrachis pelikani”) had external gills (Carroll and Gaskill, 1978), but more recent study of this taxon has failed to support this claim (Vallin and Laurin, 2004; Milner, 2008). Lissamphibians appear only in the Early Triassic, with the stem anurans (salientians) Triadobatrachus from Madagascar and Czatkobatrachus from Poland. Triadobatrachus retains a short tail, and the bones of

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The Amphibian Microbrachis Pelikani This amphibian was found in the famous locality of Nyrany, in the Czech Republic, and dates from the Late Carboniferous (Moscovian, from 306 to 312 Ma). It is represented by several individuals that represent a growth series, and it was the first taxon previously considered a “microsaur” to be described in detail (in 1883). This amphibian was perhaps neotenic, because it retained lateral-line grooves on its skull into adulthood, its limbs were small, and its endoskeleton was poorly ossified, although these characters may also reflect its aquatic lifestyle. These phenomena are difficult to

The amphibian Microbrachis pelikani. Reconstruction of the skull in dorsal (A), palatal (B), occipital (C), and lateral (D) views. The parietal (p) contacts the postorbital (po); this character is claimed to unite “microbrachomorphs.” The interpterygoid fenestra (fi), visible in palatal view (B), is relatively narrow. The stapes (s) is fairly massive. This animal, like all Paleozoic tetrapods, lacks palatal fangs. Modified from Vallin and Laurin (2004).

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tease apart because in extant amphibians, neoteny is often associated with an aquatic lifestyle. In any case, Microbrachis was probably among the most strictly aquatic, and the most neotenic, of all known Paleozoic amphibians. A few other genera share some or all of these features (lysorophians, adelogyrinids, and some nectrideans also appear to have been aquatic, neotenic forms), but most PermoCarboniferous amphibians were probably amphibious to terrestrial. Microbrachis is the type genus of the monotypic (and redundant) family Microbrachidae (it includes only this genus), and of a larger amphibian taxon called “Microbrachomorpha” (Carroll and Gaskill, 1978), but this group is probably paraphyletic (Anderson, 2001; Vallin and Laurin, 2004). As in the vast majority of other Paleozoic amphibians, its skull lacked an otic notch and its stapes was massive, indicating that the tympanum was absent, as in urodeles and gymnophionans.

its zeugopod (radius and ulna in the arm; tibia and fibula in the leg) have not fused into a radioulna and a tibiofibula, contrary to extant anurans. Urodeles and gymnophionans appear only in the Jurassic, and the oldest representatives of these taxa belong to their stem group, as shown by the retention of several primitive characters. For instance, Eocaecilia, the oldest known gymnophionan, retains diminutive limbs, which are lost in all crown gymnophionans.

DIADECTOMORPHS

As we saw above, some taxa previously interpreted as reptiliomorphs, such as embolomeres and seymouriamorphs, are probably stem tetrapods. On the contrary, diadectomorphs are genuine reptiliomorphs, as studies form the early 20th century already suggested. They were so similar to amniotes (Fig. 5.18) that some authors have even considered them amniotes (Berman et al., 1992) and have suggested that they

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Figure 5.18. Diadectomorphs, amniotes, and seymouriamorphs. The carnivorous amniote Dimetrodon tries to catch a diadectid in the water while two other diadectids and a Seymouria (to the right) rest on a log. Drawing by Douglas Henderson initially published by Czerkas and Czerkas (1990). Reproduced with permission.

laid amniotic eggs (Lee and Spencer, 1997). However, both suggestions represented a minority opinion, and the type of egg laid by diadectomorphs is conjectural (Laurin and Reisz, 1999). Diadectomorphs were initially part of the taxon Cotylosauria, named after the shape of their occipital condyle (the bony structure to which the skull articulates with the vertebral column), but later, the meaning of that name was misinterpreted and cotylosaurs were considered the ancestral group of amniotes. In fact, diadectomorphs are the closest known relatives of amniotes, but they are not their ancestors. This close relationship is supported by the presence of two sacral vertebrae (whose ribs articulate with the hip), instead of a single one, as in most other stegocephalians. This character may reflect the presumably fairly terrestrial lifestyle of diadectomorphs and amniotes.

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Figure 5.19. Diadectomorph skeleton. Skeleton of the small diadectid Orobates as preserved. It was found in Germany and dates from the Early Permian (Berman et al., 2004). Picture provided by D. Berman. Reproduced with permission of the Carnegie Museum of Natural History and the Museum der Natur, Gotha, Germany.

Diadectomorphs were relatively large (1.5 m to 2 m in total body length). Only eight genera are currently recognized, and they date from the Late Carboniferous and the Early Permian. At least some of them (limnoscelids) were amphibious to aquatic and perhaps piscivorous, (see the box titled “The diadectomorph Limnoscelis paludis”) whereas others (diadectids and Tseajaids) were probably more terrestrial (Fig. 5.19). Diadectids were herbivorous, which is exceptional for Paleozoic stegocephalians and is the only case known outside Amniota. Diadectids had very broad molars that seem well suited to chew plants, and their stubby body also suggests a herbivorous diet. No diadectomorph seems to have had a membranous tympanum, but diadectids had a bony plate linked with the ear that may have been used to transmit sounds (either low-frequency airborne sounds or sounds transmitted through water). Their neural arches were strongly convex, as in some early amniotes. The functional significance of this character remains enigmatic.

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The Diadectomorph Limnoscelis Paludis Fossils of this species were found in various sites in the southwestern United States; they date from the Early Permian (Asselian, 295 to 299 Ma). The long, slender body and the weak ossification of its body suggest an amphibious to aquatic lifestyle, as the specific epithet implies. Its sharp fangs suggest that it fed on relatively large prey. This species played a central role in hypotheses on the origin of amniotes. Romer (1957) considered, like many contemporary paleontologists, that Limnoscelis was perhaps the ancestor of amniotes, or at least fairly similar to it. Furthermore, given its relatively old geological age, he suggested that its relatively aquatic lifestyle was more likely to be primitive than to represent a return to the aquatic environment. Thus, he suggested that the fi rst amniotes were primitively aquatic and that they ventured onto land

The diadectomorph Limnoscelis paludis. Cranial reconstruction in dorsal (A), palatal (B), occipital (C), and lateral (D) views. Large fangs are present, but contrary to those of temnospondyls and embolomeres, they do not grow out of the palate; instead, they are located on the premaxilla and maxilla, which also support the upper jaw teeth.

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mostly to lay their eggs. The amniotic egg, which is adapted to being laid on dry ground, would then have preceded the appearance of terrestrial adults (at least among amniotes). On land, these eggs were sheltered from the many aquatic predators, whereas relatively few large predators roamed the land. This hypothesis is no longer largely accepted today, because the oldest known amniotes seem to have been terrestrial, and there is no evidence that the other diadectomorphs (such as Diadectes and Tseajaia) were aquatic.

AMNIOTES

The oldest known amniotes date from the middle of the Late Carboniferous (315 Ma). They were found near Joggins, in Nova Scotia (Canada), and were preserved in fossilized giant lycopsid tree stumps. Various older fossils (from the Early Carboniferous or the early Late Carboniferous), generally poorly preserved or fragmentary, had been interpreted as amniotes (Baird and Carroll, 1967; Smithson and Rohlfe, 1990), but serious doubts have been raised about these interpretations (Laurin and Reisz, 1992, 1999), or their proponents have themselves provided new interpretations (Smithson et al., 1994). The oldest known fossils are of small body size, but this may result from their preservation in the giant tree stumps that may have acted as passive traps. Given their diameter (60 cm or less), they could contain only fairly small vertebrates. When they first appear, amniotes are represented by their two main clades, sauropsids (reptiles and related extinct taxa) and synapsids (mammals and their extinct relatives). Synapsids dominated the terrestrial vertebrate fauna throughout the remainder of the Paleozoic and until the great end-Permian crisis (250 Ma ago) eliminated most of them. Sauropsids then went on to dominate for the entire Mesozoic, until the Cretaceous/Paleogene crisis (65 Ma ago) eliminated many large reptiles, including most (but not all) dinosaurs (birds are dinosaurs, and

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several lineages existed before the end of the Cretaceous). Since then, synapsids (represented exclusively by mammals) have again dominated the terrestrial vertebrate fauna. The oldest synapsids (those from the Carboniferous and the Early Permian) have long been called “pelycosaurs,” but this group is paraphyletic (therapsids are nested within it), and this name will not be used further in this book. (See the box titled “The amniote Haptodus garnettensis.”) Synapsids included the largest terrestrial (or amphibious) herbivores and carnivores in the Paleozoic. One of the most familiar carnivores is the strange sailback Dimetrodon (Fig. 5.18). Herbivorous synapsids include caseids, which reached a fairly large size (Cotylorhynchus reached nearly 3 m in total length), and edaphosaurids, the oldest known herbivorous amniotes, such as Edaphosaurus (Modesto and Reisz, 1992). The oldest known fossil amniotic egg dates from the Triassic, but the amniotic egg is produced in mammals (it is laid only in monotremes) and in reptiles; therefore, parsimony suggests that it must have existed in their last common ancestor (by definition, that was the first amniote). The long gap in the fossil record of amniotic eggs was initially intriguing, because in the Mesozoic, fossilized amniotic eggs are relatively abundant. This gap probably results from the absence of mineralization of the external membrane of the egg of early amniotes (Laurin, Reisz, and Girondot, 2000). Such eggs still exist in monotremes, the platypus and the echidna. A flexible, weakly mineralized outer egg membrane is a synapomorphy of reptiles, but such an egg has a very low fossilization potential. The strongly mineralized egg shell that is so familiar to us (because we eat so many hen eggs) is an archosaur synapomorphy, and it also appeared at least three times within turtles and within squamates. The oldest taxon with a strongly mineralized egg shell (Archosauria) appeared in the Triassic (their oldest fossils date from the Middle Triassic), which explains why no amniotic egg has been found in Permian or Carboniferous localities, despite the relative abundance of skeletal remains of amniotes in these same deposits.

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Figure 5.20. Diadectomorph and amniote skulls. The skulls of the diadectomorph Limnoscelis (A) and of the amniote Captorhinus (B) show the relationship between the frontal bone (gray) and the orbit (lighter gray) in both groups. The position of the prefrontal and postfrontal, between the frontal and the orbit, as seen in diadectomorphs (A), is primitive and very widespread in stegocephalians, whereas the presence of a frontal contribution to the orbit, as seen in most amniotes (B), is derived and rare. Abbreviations: F, frontal. Pf, postfrontal. Prf, prefrontal.

Since the amniotic egg has left no Paleozoic fossils, and since it is difficult to identify the species that have laid the fossilized eggs we have, paleontologists use other characters to identify amniotes in the fossil record. For instance, the frontal bone borders the orbit dorsally in amniotes (Fig. 5.20B), whereas in most other stegocephalians, two other bones (pre- and postfrontal) occupy this position (Fig. 5.20A).

STEGOCEPHALIAN PHYLOGENY

Two Long- Established Phylogenies The first phylogenies of early stegocephalians were produced in the 1880s (see “Temnospondyls” and “Embolomeres” earlier in this chapter), well before the advent of cladistics and phylogenetic analysis software. It is thus not surprising that they were overturned by some (but not all) recent analyses that benefited from the tremendous technological

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The Amniote Haptodus Garnettensis This species comes from near Garnett, Kansas, and dates from the Late Carboniferous (Kasimovian, between 304 and 307 Ma ago). It is one of the oldest known amniotes represented by well-preserved, partly articulated skeletons. Like most early amniotes, it seems to have been fairly terrestrial, and was probably carnivorous, as suggested by its dentition. It is closely related to the sphenacodontids and to therapsids (that group that includes most Middle-Permian and more recent synapsids, such as dicynodonts and mammals). Contrary to at least some therapsids, the back of its mandible was not modified to facilitate hearing airborne sounds. Its massive stapes was still part of the jaw suspension (it braced the upper jaw against the braincase). The transversal row of large teeth on the transverse flange of the pterygoid (Pt, visible in palatal and lateral views) characterizes most early amniotes. The large tooth in the anterior portion of the maxilla (M) is a caniniform tooth, probably homologous with the canine tooth found in mammals. However, contrary to the canine, two caniniform teeth were sometimes functional on the same maxilla, whereas a single canine is functional at any given time. Furthermore, the caniniform tooth was replaced throughout life, like all teeth, in Haptodus. Haptodus thus had a polyphyodont dentition, like most early vertebrates, whereas mammals are diphyodont (they possess two successive dentions, the milk dentition in children and the adult dentition). Diphyodonty must have appeared in synapsids in the Triassic or early in the Jurassic, and this was perhaps linked with the complex molars of mammals, whose occlusal surfaces must interlock closely to ensure efficient chewing. The high metabolism of mammals requires a fast digestion of food (especially of plant matter, which is not very nutritious), and the complex molars allow mammals to break up food into tiny particles, thus increasing the surface-to-volume ratio and speeding up digestion. This complex interlocking would presumably have been difficult to achieve in continuously replacing teeth. Like all

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Permo-Carboniferous tetrapods, Haptodus must have retained a slow metabolism and an ectothermic body temperature regulation system (which relies on behavior and the ambient climate to maintain body temperature near its optimal value). Its skin was probably devoid of fur and it probably laid eggs.

The amniote Haptodus garnettensis. Reconstruction of the skull in dorsal (A), palatal (B), and lateral (C) views, and of the mandible in lateral (D) and medial (E) views. Reproduced from Laurin (1993).

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advances of phylogenetics in the last decades. Nevertheless, they deeply influenced generations of paleontologists and are still widely accepted, in a slightly modified form, by several practicing systematists, and as such, they deserve to be presented here. Most phylogenies published before 1997 implied that all known stegocephalians were either amphibians or reptiliomorphs (Fig. 5.21); in most cases, no limbed vertebrate was considered a stem tetrapod, at least until the discovery of Devonian stegocephalians. Thus, embolomeres, seymouriamorphs, diadectomorphs, and amniotes were considered to be reptiliomorphs, whereas “lepospondyls,” temnospondyls, and lissamphibians were considered amphibians. The “lepospondyls” were sometimes considered polyphyletic because some were classified among reptiliomorphs by a few authors (“lepospondyls” are paraphyletic in Figure 5.21). The position of the Devonian stegocephalians such as Acanthostega and Ichthyostega was more controversial. Most previous studies considered them amphibians, but at least since the 1980s, some authors considered them stem tetrapods. This phylogeny suggested that the invasion of land by vertebrates occurred in parallel in amphibians and in reptiliomorphs (Fig. 5.21). These phylogenies were initially produced by E. D. Cope, who suggested, as early as 1880, that embolomeres were reptiliomorphs and, in 1882, that temnospondyls were amphibians. These hypotheses were initially supported by a few characters. For instance, reptiliomorphs were thought to share the presence of a single occipital condyle, and amphibians displayed a vertebral centrum formed (or dominated) by an intercentrum (this is clearly correct only among temnospondyls). This phylogeny was nevertheless accepted by the vast majority of paleontologists and remains popular today. When the characters used by Cope to justify his hypotheses were refuted (because they are primitive, like the single occipital condyle, or based on an error of interpretation, like the composition of the amphibian vertebral centrum, which is a pleurocentrum in lissamphibians and “lepospondyls”), other characters were proposed, but strangely, the phylogeny was not seriously questioned. This can

Amniota Diadectomorpha Seymouriamorpha Embolomeri Acanthostega Ichthyostega Aïstopoda Adelogyrinidae Nectridea “Microsaurs” Lysorophia Temnospondyli (including Lissamphibia)

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“Lepospondyls”

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m ds Stetrapo e t Figure 5.21. Classical stegocephalian phylogeny (simplified). The position of the Devonian stegocephalians, such as Ichthyostega and Acanthostega, was controversial for most of the 20th century. They were generally considered to be amphibians, and less often, stem tetrapods. The horizontal gray lines indicate the independent acquisitions of an amphibious or terrestrial lifestyle. In some cases (nectrideans, “microsaurs,” temnospondyls, embolomeres), only some species of these groups are amphibious or terrestrial.

perhaps be attributed to the weight of tradition, which plays an important, if seldom acknowledged, role in science (Laurin, 2008a). The weight of tradition may seem inappropriate in science, but it is not always harmful, because it prevents the scientific community from prematurely rejecting good established theories when new alternatives are proposed. Recent stegocephalian phylogenies produced without computers retain a topology compatible with Cope’s suggestions (Panchen and Smithson, 1988). An alternative hypothesis, less widely accepted, implies that extant amphibians are polyphyletic, at least compared with Paleozoic stegocephalians. According to its proponents, anurans are nested within temnospondyls, whereas gymnophionans are nested within “lepospondyls.” The position of urodeles has been more variable; an origin among

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“lepospondyls” was favored by early studies (Carroll and Currie, 1975; Carroll and Holmes, 1980), but an origin among temnospondyls (not the same as for anurans) is favored by more recent studies (Schoch and Carroll, 2003; Carroll, 2007; Fröbisch et al., 2007; Anderson, 2008; Anderson et al., 2008). These phylogenies are incompatible with most recently published phylogenies produced by computer-assisted analyses (Laurin, 2002). Furthermore, the developmental data that have provided much of the support for these hypotheses actually do not support them (Schoch, 2006; Germain and Laurin, 2009). Finally, two of the few data matrices that supported lissamphibian polyphyly actually support a monophyletic origin of extant amphibians among “lepospondyls” when recoded to better reflect the descriptive literature (Marjanovic´ and Laurin, 2008, 2009). Globally, there is very little objective support for extant amphibian polyphyly.

A Recent Alternative The fi rst computer-assisted phylogenetic analyses of Paleozoic stegocephalians (Gauthier et al., 1988; Trueb and Cloutier, 1991) seemed to support Cope’s venerable ideas, but this resulted from a rather restricted choice of taxa. One of these studies included only temnospondyls and lissamphibians, and the other included only embolomeres, seymouriamorphs, diadectomorphs, and amniotes. Given these taxonomic samplings, it was impossible to test which Paleozoic taxa were amphibians and which ones were reptiliomorphs (because to test these hypotheses, lissamphibians and amniotes had to be present in the same analysis). The fi rst analysis that included most relevant higher taxa (Laurin and Reisz, 1997) suggested that lissamphibians derive from “lepospondyls.” Temnospondyls are stem tetrapods, rather than amphibians (Fig. 5.22). According to the same phylogeny, embolomeres and seymouriamorphs are not reptiliomorphs; instead, they are stem tetrapods. All Devonian stegocephalians are also stem tetrapods. This phylogeny requires reevaluating the evolution of most

Acanthostega Ichthyostega Temnospondyli Embolomeri Seymouriamorpha

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Amniota Diadectomorpha Aïstopoda Adelogyrinidae Nectridea “Microsaurs” Lysorophia Lissamphibia

“Lepospondyls”

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S

Figure 5.22. Recent stegocephalian phylogeny (simplified). Reptiliomorphs and amphibians include far fewer taxa than in older phylogenies because many of their presumed members (temnospondyls, embolomeres, and seymouriamorphs) have been transferred to the tetrapod stem. The horizontal gray lines indicate the independent presumed appearances of amphibious or terrestrial lifestyles. In some cases (temnospondyls, embolomeres), only some species of these taxa have become terrestrial, and some species reverted to an aquatic lifestyle (adelogyrinids, and some species among nectrideans, “microsaurs,” amniotes, and lissamphibiens). Synapomorphies of the clades: 1, temnospondyls and tetrapods; pentadactyl limb. 2, embolomeres and tetrapods; presence of a contact between parietal and tabular. 3, seymouriamorphs and tetrapods; fusion of the vertebral centrum to the neural arch in the vertebra. 4, tetrapods; loss of the intertemporal in the dermal skull roof. 5, cotylosaurs; presence of two sacral vertebrae. 6, amphibians; atlantal neural arch fused in the sagittal plane (it is paired in most other taxa). 7, lysorophians and lissamphibians; loss of two of the three coronoids that were present in the mandible of the first stegocephalians and loss of the jugal bone.

characters in early stegocephalians. For instance, it suggests that the fi rst terrestrial stegocephalians were stem tetrapods (Fig. 5.22). Such a radical change in stegocephalian phylogeny could be accepted neither rapidly nor without much resistance. A few studies produced large data matrices that supported a monophyletic origin of lissamphibians among the temnospondyls (Ruta et al., 2003; Ruta and Coates, 2007). However, three theses, including one in progress, have reworked this matrix, and all conclude that Lissamphibia is monophyletic but nested within “lepospondyls” (Marjanovic´ and Laurin, 2009). Furthermore, “lepospondyls” are more closely related to amniotes

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than to temnospondyls in all phylogenies supported by data matrices published after 1996, whereas old phylogenies placed both temnospondyls and “lepospondyls” in an amphibian clade that excludes amniotes. Thus, the old phylogeny is rejected by practically all recent relevant studies, but the debate about lissamphibians continues and will probably not be settled for five or ten more years. This long period of debate is necessary because much time is required to compare the various data matrices, find the characters or taxa responsible for the incompatibilities, and determine the correct coding. This work requires exhaustive literature searches, an examination of many fossils, and new descriptions and analyses, but this painstaking research is the price to pay for progress in paleontology.

. . . Ontogeny is best known only in a few temnospondyls and seymouriamorphs, among Paleozoic stegocephalians. At least a few species of both groups had larvae with external gills. We do not know if embolomeres, diadectomorphs, and Paleozoic amphibians had such larvae. Our ideas about phylogenetic relationships among the main stegocephalian taxa have changed drastically following the fi rst computerassisted phylogenetic analyses that included all the main clades. From the 1880s till the mid-1990s, we thought that most stegocephalians were either amphibians (temnospondyls and “lepospondyls”) or reptiliomorphs (embolomeres, seymouriamorphs, diadectomorphs, and amniotes). Most recent analyses suggest that temnospondyls, embolomeres, and seymouriamorphs are stem tetrapods. Only “lepospondyls” are amphibians, and reptiliomorphs include mostly diadectomorphs and amniotes.

chapter six

Adaptations to Life on Land

When vertebrates ventured onto land, most of their systems (locomotor, respiratory, sensory) and structures (like the skin and axial skeleton) were not optimal for terrestrial life. Life in this new environment must have been fairly difficult for these animals, and the selective pressures leading to adaptation to life on land must have been fairly strong. Adaptation as a process is evolution influenced by selective pressures; the same word also designates the end result of this evolution, namely, a character that improves fitness. Thus, the loss of internal gills early in stegocephalians history can be seen as a terrestrial adaptation. We must distinguish exaptation (often called preadaptation) from the related concept of adaptation. An exaptation is a structure that acquires a new function. Thus, the presence of a limb with digits may not be an adaptation for terrestrial life, because digits appeared in aquatic vertebrates, perhaps to walk underwater in a cluttered environment, such as a mangrove. In terrestrial stegocephalians, the limb acquired a new function, to walk on dry land. It is thus an exaptation. Another well-known example is the feather. It appeared in fl ightless dinosaurs, probably to provide thermal insulation, before adopting an exaptive role for fl ight. This chapter discusses the main adaptations and exaptations for terrestrial life in stegocephalians. 135

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The conquest of land does not necessarily represent an evolutionary trend, which is biased directional evolution. Indeed, although some stegocephalians became terrestrial, some of their descendants reverted to an aquatic lifestyle. Since evolution is not deterministic (it has no purpose), it is usually not directional, at least in the long run. If there was an evolutionary trend towards terrestrial life in some taxa at some times (as in stegocephalians in the Early Carboniferous), there were perhaps trends in the other direction at others (as shown by the frequent returns to an aquatic lifestyle in stegocephalians from the Early Carboniferous to the present). Detecting evolutionary trends requires extensive data and statistical analysis. The conquest of land by vertebrates probably consists of only a few habitat shifts, so it cannot be subjected to such analyses, although transitions between habitats in various taxa have revealed intruiging patterns (Vermeij and Dudley, 2000).

LIMBS AND GIRDLES

Evolution of the Locomotor System Since limbs with digits appeared among aquatic vertebrates in the Devonian, they may not be an adaptation to terrestrial life. However, some characters of more recent (Carboniferous or later) stegocephalians are probably adaptations to terrestrial locomotion. To determine which ones, we need to compare the limbs of primitively aquatic stegocephalians with those of the first terrestrial vertebrates. This is not easy to do, because we cannot observe the lifestyle of early stegocephalians, and any inferences that we make on this topic can be wrong. Furthermore, the primitive or secondary status of an aquatic lifestyle is sometimes difficult to assess, especially for Carboniferous taxa. Finally, the limbs are well known in only a small proportion of early stegocephalians. We will compare the limb of Acanthostega (a Devonian stem tetrapod) with that of Cacops (Fig. 6.1; an Early Permian temnospondyl) and assume that the fi rst genus was primitively aquatic and that the second was terrestrial. Among the differences observed, only

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Figure 6.1. Reconstruction of the temnospondyl Cacops. Cacops is generally thought to have been among the most terrestrial temnospondyls because its limbs were well ossified, and dermal scales on its back may have reinforced its vertebral column. However, this does not imply that it did not occasionally swim, as this reconstruction suggests. Drawing by Douglas Henderson initially published by Lauber (1996). Reproduced with permission.

those that consistently appear between other primitively aquatic and terrestrial stegocephalians are likely to reflect terrestrial adaptations; other differences may reflect only the morphologies of Acanthostega and Cacops and be unrelated to adaptations to terrestrial locomotion.

Limb Evolution After the transition from an aquatic to a terrestrial lifestyle, the limb became more flexible because well-defined articular surfaces allowing a greater range of flexion appeared. In Acanthostega, the relatively flat articular surfaces suggest that the limbs could not flex much at the wrist, elbow, knee, and ankle (Fig. 4.1). Such a limb must have behaved more like a swim paddle (as seen in extant cetaceans) than a typical tetrapod

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limb. In most Permo-Carboniferous stegocephalians, the limb extremities bear curved articular surfaces that suggest an increased mobility compatible with walk on emerged land (Fig. 6.2). In such forms, we see genuine elbows and knees that presumably allowed flexion or extension across a range of about 90 degrees. However, the wrists and ankles still involved articulations between several bones, and their flexibility may have resembled that of urodeles. Highly flexible wrists and ankles, as seen in birds and mammals, appeared much later. The limb also became better ossified in terrestrial stegocephalians. In Acanthostega, the ends of long limb bones must have been covered in a thick layer of cartilage. The carpal and tarsal bones do not articulate closely with each other, which also suggests that a substantial amount of cartilage remained around these bones. In Cacops, the cartilaginous layer around these bones was much thinner, resulting in a stronger limb. Finally, the bones of the palm of the hand and sole of the foot, the metacarpals and metatarsals, became better differentiated. In Acanthostega, they do not differ from phalanges, whereas in Cacops, they are thicker and longer. This differentiation may reflect the appearance of a new flexible joint between the hand and foot proximally and fingers and toes distally. Such flexion is very useful on land, but not in water.

Girdle Evolution The girdles are skeletal structures to which limbs articulate. The shoulder (or pectoral) girdle is composed of dermoskeletal and endoskeletal parts. The latter is called the scapulocoracoid and may be made of three bones—the scapula, coracoid, and precoracoid. The pelvic (hip) girdle is entirely endoskeletal. As with the limb, several changes are probably exaptations. This includes the loss of contact between the shoulder girdle and the skull (Fig. 6.3) through the loss of the dorsal dermal part of the girdle and of bones from the opercular series that covered the branchial chamber. This increased the mobility of the head through the appearance of a mobile neck; thus, shoulder and neck

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Figure 6.2. Skeleton of the temnospondyl Cacops. Each limb segment, as well as dermal and endoskeletal portions of the girdles, are shown in various shades of gray. Modified from Williston (1910).

Figure 6.3. Panderichthys, one of our closest fi nned relatives. The endoskeletal shoulder girdle is not visible in this view because it was very small and located on the internal surface of the dermal shoulder girdle. The bones that were lost in the fi rst stegocephalians and thus increased the neck flexibility are identified by white dots. Modified from Vorobyeva and Schultze (1991).

Figure 6.4. Skeleton of the stegocephalian Ichthyostega. This aquatic stegocephalian dates from the Late Devonian and was found in Greenland. The same gray shades as in Figure 6.2 are used to identify skull, girdle, and limb segments. Modified from Jarvik (1955).

muscles provided a suspension to stabilize the head while the animal walked on land. This is important because head movements can impede both vision and equilibrium. The limbs acquired a new orientation because sarcopterygian fi ns extend posteriorly (Fig. 6.3), whereas in the earliest still-aquatic

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stegocephalians, the limbs extend mostly laterally (Figure 4.1). The new orientation results partly from lateral rotation of the shoulder and hip sockets. Another exaptation is the sacrum, the structure composed of at least one pair of ribs that articulate directly with the pelvic girdle. This contact improves support of the body weight outside the water because it is energetically less costly than the indirect link through muscles and ligaments found in fi nned vertebrates. Adaptations to terrestrial life include a reduction in size of the dermal shoulder girdle and an increase in size of the endoskeletal shoulder girdle (Figs. 6.2 and 6.4). The dorsal portion of the latter (the scapula) provides attachment sites for many of the limb muscles; its increase in size presumably reflects an increased development of these muscles.

VERTEBRAL CENTRUM AND AXIAL SKELETON

Primitively aquatic Devonian sarcopterygians such as Eusthenopteron had neural arches (the part of the vertebra that surrounds the spinal chord) fused in the sagittal plane only at the dorsal tip of the neural spines. The arches lacked well- defi ned articular surfaces for articulation with each other. The vertebral centra (which surrounded the notochord) were composed of a variable number of bony elements— in Eusthenopteron, a median or paired intercentrum and a paired pleurocentrum—that were presumably linked to each other and to the neural arches through cartilage and connective tissues. The vertebral centra formed rings that surrounded a functional notochord retaining an important mechanical role. This was adequate in an aquatic environment, but it was probably not stiff enough to support the body outside water. The vertebrae of the first stegocephalians were barely sturdier. In Acanthostega, the neural arches were slightly more firmly fused in the sagittal plane than in Eusthenopteron. The zygapophyses— articular surfaces between successive neural arches— appeared, but they were poorly developed. The vertebral centrum was a little thicker but retained a configuration reminiscent of Eusthenopteron, and the intercen-

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Left lateral view

Anterior view

A Neural arch

B

C

Intercentrum

D

E Pleurocentrum (three configurations)

Figure 6.5. Diversity and evolution of vertebral centra. Vertebrae are orga nized from the most primitive (A) to the most recent (E), but they form two morphoclines. The fi rst goes from Permo- Carboniferous temnospondyls showing the rhachitomous morphology consisting of a large, crescentic, ventral intercentrum and small, dorsal, paired pleurocentra (A) to Triassic stereospondyls (B) with a centrum composed of a cylindrical intercentrum. The second shows the progressive development of the pleurocentrum along the tetrapod stem from the primitive rhachitomous position (A) through embolomeres (D), which had cylindrical pleuro- and intercentra, and more crownward stegocephalians, such as seymouriamorphs and tetrapods (E), which had a large, cylindrical pleurocentrum and a reduced, crescentic intercentrum (the latter disappeared early in amphibian evolution and later in amniotes). The Early Carboniferous form Whatcheeria (C) does not belong to any of these main taxa but fits on the tetrapod stem between Ichthyostega and temnospondyls. It has crescentic intercentra and pleurocentra (one each per centrum).

trum sometimes remained paired. This axial skeleton reflects a primarily aquatic lifestyle. The axial skeleton of Early Carboniferous stegocephalians was better adapted to terrestrial locomotion, even though many were probably amphibious rather than truly terrestrial. In these forms, the neural arch halves are firmly fused at the sagittal plane and the zygapophyses are well developed. The composition of the vertebral centrum was variable (Fig. 6.5). In temnospondyls, the centrum retains the same composition as in Eusthenopteron and Ichthyostega (Fig. 5.6A). In embolomeres, pleurocentra and intercentra are cylindrical (Fig. 5.6B). The subsequent evolution of the vertebral centrum depends on the phylogeny. Under the recent alternative favored here (Fig. 5.22), the

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pleurocentrum becomes cylindrical and the intercentrum becomes very small and crescentic in the smallest clade that includes seymouriamorphs and tetrapods (Batrachomorpha). This morphology has been retained in some extant amniotes. The neural arch of batrachomorphs is firmly fused to the vertebral centrum, which reinforces the axial skeleton. Only in Batrachomorpha is the axial skeleton fully adequate for terrestrial locomotion. Under the classical hypothesis of a monophyletic Lissamphibia nested within temnospondyls (Fig. 5.21), the increase in size of the pleurocentrum and its fusion with the neural arch along with the dwindling of the intercentrum have to be assumed to occur convergently among reptiliomorphs and in amphibians. The few apparently terrestrial temnospondyls have strengthened their axial skeleton through dermal scales that articulate with each other and with neural arches (DeMar, 1968) or through flanges on the ribs that overlap the next posterior rib and strengthen the rib cage, as in birds. Dermal scales articulating with each other and with neural arches also appeared in the most terrestrial embolomeres, found in the Late Permian and Triassic of Russia (Golubev, 1998). No comparable axial skeleton exists in extant tetrapods.

BREATHING

Lung Evolution Our aquatic ancestors were already able to breathe air since they had inherited lungs from the first osteichthyans (see “Homology and Analogy: Lungs, Swim Bladders, and Gills” in Chapter One). This suggests that some of our aquatic ancestors lived in poorly oxygenated water and used their lungs to extract oxygen from the air. For such animals, adapting to breathe only air on emerged land was far easier than it was for teleosts that have more recently become amphibious and which had transformed their lungs into a swim bladder (see “Homology and Analogy: Lungs, Swim Bladders, and Gills” in Chapter One).

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In terrestrial vertebrates, the lung became more complex. Evolution of this complexification is poorly documented because the lung does not fossilize. Alveoli— small subdivisions of the lung— are present in primitively aquatic osteichthyans (all actinopterygians and dipnoans), but the alveoli are more numerous and smaller in tetrapods, expanding surface/volume ratio and improving lung efficiency. An indirect clue about lung complexity and its increasing importance in breathing is provided by relative rib length. In primitively aquatic vertebrates, ribs are generally very short, whereas in tetrapods that use costal ventilation, as in many amniotes, they are long and curved because they, along with the cartilaginous sternal ribs on the ventral surface, have to encircle the thorax. Relative rib length suggests that pulmonary ventilation was not accomplished primarily through the ribs in Devonian stegocephalians. Predominant costal lung ventilation may have appeared in the smallest clade that includes temnospondyls, embolomeres, seymouriamorphs, and tetrapods. This includes most post-Devonian stegocephalians and may have disappeared in some temnospondyls (which is not surprising, given that many of them returned to an aquatic lifestyle, especially in the Triassic) and in amphibians very early in their history. Thus, the buccopharyngeal breathing of lissamphibians, which does not involve ribs, is probably not a primitive feature; it presumably represents an autapomorphy of this taxon. The history of the lissamphibian buccopharyngeal pump is difficult to reconstruct because it leaves even less fossil evidence than costal ventilation. Nevertheless, a few clues suggest that most early stegocephalians lacked such a pump (Gans, 1970), except for temnospondyls, whose large interpterygoid vacuities may have been involved. In such taxa, air enters the mouth when the gular pouch (between the lower jaws) expands. Then, the mouth and nares are closed and air is forced from the mouth into the lungs by contraction of the gular pouch. Expiration is simpler; trunk muscles contract and expel the air. Such a buccal pump also exists in many reptiles, but it has only an olfactory role.

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The stegocephalian choana (internal naris) was originally the posterior external naris found in most other osteichthyans. This naris was initially located on the lateral surface of the snout. It provided an outlet for the water that entered the nasal cavity through the anterior naris when the animal swam. The motion of a swimming animal creates a water current in the nasal cavity, which allows the animal to perceive odors, but such animals cannot voluntarily inhale water through the nose because the nasal cavity lacks a connection with the buccal cavity. In the first tetrapodomorphs (the largest clade that includes tetrapods but neither dipnoans nor actinistians) from the Early Devonian, the posterior external naris had migrated ventrally and was located on the lower edge of the snout, next to the mouth. In all other tetrapodomorphs, this opening has migrated onto the palate. This allows direct inhalation of air or water and, thus, the ability to smell without having to move or open the mouth. This may have been especially useful if our ancestors were aquatic ambush predators. We think of the choana as a respiratory structure, but its first function may have been primarily olfactory. The choana was never important as an underwater breathing structure because water is more viscous than air; a much larger opening is needed to efficiently ventilate the gills.

Loss of Gills One of the main adaptations to life on emerged land was the loss if the internal gills. These structures can breathe in air, but they dehydrate rapidly because the branchial chamber is largely open to the external environment through the gill slits. It is thus not surprising that they were quickly lost towards the end of the Devonian or the Early Carboniferous. And yet, much information (taphonomic, presence of a lateralline organ, low degree of ossification of the endoskeleton) suggests that most stegocephalians remained mostly aquatic. Thus, the internal gills may have been lost even before stegocephalians became terrestrial.

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Figure 6.6. Shoulder girdle of Acanthostega. Postbranchial lamina of the cleithrum (dark gray) of Acanthostega, one of the last stegocephalians that possessed internal gills. The dermal shoulder girdle is shaded a little lighter, and the endoskeletal girdle, lighter still. Scale: 1 cm. Modified from Coates and Clack (1991).

This paradox raises the possibility that stegocephalians lived in oxygendepleted water, in which case the gills may have been disadvantageous because the oxygen could have flowed from the gills into the water, rather than the other way around. The habitat of Paleozoic stegocephalians remains partly hypothetical, but the loss of internal gills is suggested by the disappearance of the postbranchial lamina of the cleithrum (Fig. 6.6), a structure of the dermal shoulder girdle that normally contributes to the posterior wall of the branchial chamber. This structure was present in the fi rst sarcopterygians and persisted among several Devonian and a few Carboniferous stegocephalians. Another osteological character suggesting an early loss of internal gills is the disappearance of grooves on the ceratobranchials (part of the visceral skeleton; Fig. 6.7). These probably housed arteries that carried blood to the gills, where it was oxygenated. These grooves are present in Acanthostega and Ichthyostega

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Figure 6.7. Branchial skeleton of Acanthostega. Acanthostega ceratobranchials showing the grooves that must have housed branchial arteries. All visceral skeletal elements are shaded. Scale: 2 mm. Modified from Coates and Clack (1991). parts: A, dorsal view of the skull and associated branchial elements. B, ventral view. C, transversal section of a ceratobranchial the groove that sheltered the branchial artery.

(both from the Devonian), but they are absent from most post-Devonian stegocephalians.

Skin Breathing Many extant amphibians breathe through the skin. This often provides a substantial amount of gas exchange in addition to the gills and lungs, but in some taxa, such as many plethodontid salamanders, both lungs and gills have disappeared and the skin is solely responsible for gas exchange. Exclusively cutaneous respiration is possible only in organisms of small body size because the surface/volume ratio decreases with body size. Thus, most amphibians with exclusively cutaneous breathing are less than 10 cm in total body length, with the exception of the only known lungless gymnophionan, Atretochoana eiselti, which reaches more than 70 cm in length (Wilkinson and Nussbaum, 1997). Since many

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Paleozoic stegocephalian species measured much more than 10 cm (Laurin, 2004), this mode of breathing must not have been widespread. Romer (1972) had already concluded that cutaneous breathing was not important in early stegocephalians, because dermal scales, present in many early stegocephalians, prevented cutaneous gas exchange. In fact, these scales are usually located in the dermis, under the skin, and vascular canals may have been present on the external surface of such scales, thus facilitating gas exchange.

THE SKIN AND WATER EXCHANGE

Primitively Aquatic Vertebrates The skin of primitively aquatic vertebrates provides a partial barrier to water exchange because vertebrates living in fresh water are hypertonic compared with their environment, whereas marine vertebrates are generally hypotonic compared with sea water. The integument in most primitively aquatic osteichthyans possesses various features to reduce permeability, such as dermal scales covering most the body and a thick layer of connective tissue (Bond, 1979). Thus, eel skin is fairly waterproof, but it represents 10% of the animal’s mass. In these vertebrates, most water exchange takes place at the gills; these cannot be waterproofed, since this would prevent gas exchange. Freshwater vertebrates must eliminate the excess water that keeps seeping into the body. This is accomplished through the glomerula in the kidneys. Ions and other substances that the organism must keep are then resorbed by the kidney tubules and the bladder. Osmoregulation has been intensively studied in several actinpterygian species. In marine vertebrates, water tends to move out of the body because sea water is hypertonic relative to the body. These vertebrates drink seawater. This is absorbed by the digestive tract, and such animals excrete monovalent ions (for instance, Na+, Cl-, etc.), especially through the gills and, to a lesser extent, through specialized cells in the skin on the anterior part of the body. Divalent ions (like Ca2+) are eliminated mainly

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by the kidneys. Glomerula are smaller and less numerous (if present at all) in marine vertebrates because the body does not have to eliminate excess water. They thus produce much less urine than their freshwater relatives, but it has a much higher concentration of divalent ions. This osmoregulatory mode characterizes most marine actinopterygians. However, chondrichthyans and the coelacanth retain urea in the blood, which increases its osmotic pressure to match (and even exceed slightly, in chondrichthyans) that of sea water, which greatly facilitates osmoregulation and helps maintain water balance. The taxonomic distribution of urea retention does not enable us to determine if our marine ancestors ever possessed it. The habitat of our aquatic ancestors is still controversial, but many paleontological data suggest a marginal marine origin for stegocephalians. This would have facilitated the invasion of land because marine vertebrates produce little urine, which enables water conservation on land.

The First Terrestrial and Amphibious Vertebrates The skin adaptations of early stegocephalians to face the relative aridity of the terrestrial environments are poorly known because skin does not fossilize, except for the ossified scales. We know that many stegocephalians retained ossified scales on the ventral surface of the body, but fewer species had such scales also on the flanks and the back. By the end of the Devonian, stegocephalians had greatly reduced the dermal scale covering of the body. To study other aspects of water-balance evolution, we must turn to extant taxa. Lissamphibians are often considered incompletely adapted to a terrestrial lifestyle, but this is an oversimplification. Lissamphibian skin is often highly permeable, but this is not necessarily disadvantageous. Indeed, lissamphibians absorb most of the water they need through specialized surfaces of the skin. Other lissamphibians, such as the treedwelling anuran Phyllomedusa sauvagei, produce waxy secretions that

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waterproof their skin (Pough et al., 2004). Other anurans, such as Cyclorana (Hylidae), Limnodynastes, and Neobatrachus (Myobatrachidae), can secrete a mucous cocoon to prevent water loss in the dry season. These lissamphibains can resist dehydration as well as most reptiles and mammals. Their adaptations differ greatly from those of amniotes, which suggests that they appeared convergently. Consequently, the first tetrapods may have had fairly permeable skin. The glomerula are generally well developed in extant amphibians, which produce much urine, but this may be linked with their frequently amphibious lifestyle. In some desert-dwelling ampibians, urine is retained in a huge bladder and can be reabsorbed in the dry season to meet the animals’ water requirements.

Amniotes Amniote skin is generally more waterproof than amphibian skin. The main barrier against dehydration is provided by lipid layers. In this respect, there is little difference between mammalian and reptilian skin. It is often wrongly stated that mammals have a more permeable skin than reptiles because they can lose much water in the form of sweat. However, sweating is an active thermoregulatory mechanism— evaporation of sweat cools off the body—and sweat is produced by specialized glands. Sudation is thus not to be confused with passive water evaporation through the skin; such evaporation also occurs in mammals, of course, but at about the same rate as in reptiles. Most reptiles produce little urine and have poorly developed glomerula. This is probably linked with their excretion mode of nitrogenous waste products as uric acid, which is fairly insoluble and precipitates in the urine. Excreting nitrogenous wastes thus requires less water in reptiles than in urea-producing mammals. In most mammals and in some birds, glomerula are well developed and produce copious urine, but most of it is reabsorbed in a new portion of the kidney tubules called Henle’s loop. This minimizes water loss linked with nitrogenous

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waste excretion. Since the kidney does not normally fossilize, and since it evolves quickly in response to habitat shifts, it is difficult to reconstruct its history.

SENSORY ORGANS

Lateral- line Organ This organ is composed of neuromasts (ciliated cells), generally located in canals in the dermis, along the flanks and in canals or grooves of some cranial bones. It is present in all primitively aquatic craniates except hagfishes (Janvier, 1996). In lampreys and aquatic lissamphibians, the neuromasts of this organ are located on the skin surface. These cells are used to detect motion in water. They help predators to detect their prey, and the prey to avoid predators. They also facilitate schooling behavior in teleosts; they can stay grouped and avoid collision even if blinded because of the information provided by the lateral-line organ. A lateral-line system works only in water, and since it dehydrates quickly, it was probably quickly lost in terrestrial and amphibious tetrapods. In lissamphibians, the organ is present in aquatic larvae and in the adults of several aquatic taxa, but it disappears at metamorphosis in species that have terrestrial or amphibious adults. It has never been observed in amniotes, even in early development. Fossils show that the organ of the first tetrapodomorphs was located in canals in dermal bones and in flank scales, but it migrated to a more superficial position, in grooves at the surface of dermal bones, in early stegocephalians. This migration may be explained by the function of the canals in which the organ is located in most other gnathostomes; they seem to filter the noise generated by the animal as it swims. In teleosts, a similar superficial migration is often associated with neoteny and is generally disadvantageous, but the problem can be minimized by adopting an ambush hunt strategy (Montgomery and Clements,

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2000). As long as the animal is immobile, the superficial position of the neuromasts is not disadvantageous. It is thus possible that early stegocephalians were ambush predators. Since the lateral-line organ does not always leave traces on the skeleton, we can follow only part of its evolution in stegocephalians. We know that it persisted in many temnospondyls (including the last species in the Cretaceous) in various embolomeres, in seymouriamorph larvae, and in the adults of a few Paleozoic amphibians. We have no evidence that it ever existed in reptiliomorphs, even though it was probably present in the first, yet undiscovered, members of this clade.

Ear anatomy and function The ear is comprised of three distinct parts that do not have the same taxonomic distribution (or geological age). The oldest, found in all craniates, is the inner ear. The middle ear is unique to stegocephalians, and the external ear is found only in mammals. The inner ear was initially involved mostly in equilibrium, a function that it retains in all craniates; in all except tetrapods, this remains also its main function. In tetrapods (and convergently in ostariophysean teleosts), the inner ear acquired a new auditory function without losing its equilibrium function. But without a middle ear, it is sensitive mostly to sounds traveling in water and in the ground; in air, only relatively low-frequency (less than 1000 Hertz) sounds are easily heard. As for the lateral-line organ, its sensory cells are neuromasts. The middle ear is composed of one ossicle (the stapes) or more (in mammals, there are three). This structure facilitates reception of airborne sounds to the inner ear. It results from the transformation of the hyomandibular, which is involved in jaw suspension in most gnathostomes, into an ear ossicle (the stapes). To understand its evolution, we must first survey the types of jaw suspensions.

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jaw suspension We recognize three main types of jaw suspension (Fig. 6.8): amphistylic, hyostylic, and autostylic. Amphistylic suspension is probably the most primitive because it is found in the first chondrichthyans and osteichthyans, and it persists in gymnophionans and urodeles. It was also found in Paleozoic amphibians and in the first amniotes. In these taxa, the palatoquadrate (the element that composes the dorsal part of the mandibular arch) articulates directly with the neurocranium (braincase) through the basicranial articulation, which is often located close to the orbit, and indirectly with the neurocranium through the hyomandibula (or stapes). Primitively, both articulations may have been slightly mobile. They were involved in, among other things, the buccal pump of actinopterygians and primitively aquatic sarcopterygians. The hyostylic suspension appeared through the disappearance of the basicranial articulation, resulting in a greater mobility of the palatoquadrate and, hence, of the upper jaw. It is found in most elasmobranchs (sharks and rays). In this type of mandibular suspension, as in amphistyly, the hyomandibular plays an essential role in mandibular suspension, which imposes mechanical constraints preventing this structure from evolving in response to evolutionary pressures to improve hearing. In the third kind of mandibular suspension, autostylic, the palatoquadrate articulates with (and often fuses to) the neurocranium only through the basicranial articulation. This frees the stapes from its support function, which was probably crucial to allow the appearance of middle ear. To efficiently transmit high-frequency airborne sounds, the stapes must be very light, which is incompatible with a role in mandibular suspension. All stegocephalians with a tympanum or ear drum (a tympanic ear), such as extant reptiles, mammals, and anurans, possess an autostylic suspension. Mammals are a partial exception because the stapes retains an articulation with the posterior part of the palatoquadrate, the incus, but these minute elements form part of the middle

Adaptations to Life on Land / 153

Amphistylic

Hyostylic

Autostylic

Neurocranium Mandibular arch Hyomandibular Articulations between mandibula arch and neurocranium or hyomandibular Orbit

Figure 6.8. Mandibular suspension. The three types of jaw suspension (amphistylic, hyostylic, and autostylic) are defi ned by the number and position of the articulations (not necessarily mobile) between the palatoquadrate (element of the upper part of the mandibular arch) and the neurocranium.

ear and not the functional jaw. A tympanic ear enables all these animals to hear high-frequency (over 1000 Hertz) airborne sounds well. tympanic ear The tympanic ear is necessary only in the air because sounds transmitted in water can easily reach the water-filled inner ear when the animal is submerged. However, the bulk of the sound waves transmitted in air would be reflected at the air/water interface (the vertebrate inner ear is always filled with water) without a force-amplification mechanism, because water is about 1000 times more dense than air. This means that the animal would be nearly deaf. For sound waves to be transmitted efficiently into the inner ear, their force is amplified through two mechanisms (Fig. 6.9). The first is a great size ratio (between 10 × and 40 × ) between the surface of the tympanum and the oval window, into which the footplate of the stapes rests. Vibrations of the stapes induced by airborne sounds are transmitted to the fluid-filled inner ear through the oval window. The second is a lever system, which decreases movement amplitude and increases its strength by the same factor. The lever

154 / Adaptations to Life on Land

Skin

Pars superior Internal ear (water)

Extracolumella

Oval window

Neurocranium (braincase)

External environment (air)

Stapes

Middle ear cavity (air)

Pars inferior

Tympanum

2 mm

Figure 6.9. Middle ear. Middle ear of a gecko (squamate) Ptyodactylus guttatus. Modified from Werner and Igic (2002).

is different (not homologous) in several taxa, which is not surprising given that the tympanum appeared several times (Fig. 6.10). In squamates, the extracolumella (which is generally cartilaginous) plays this lever role. The distal end of its pars inferior (ventral part) is located in the center of the tympanum and moves with it when sound waves reach it. The extracolumella is fi xed to the skull at the tip of its pars superior (upper part), which is immobile. The pars inferior is usually three times longer than the pars superior (Werner and Igic, 2002, which means that the motion amplitude is decreased by a factor of about 4. Between this lever effect and the amplification provided by the ratio between the surface of the tympanum and of the oval window (10 × to 40 × ), the total amplification factor is from 40 to 160. This allows adequate transmission of sounds from air to the aqueous solution that fills the inner ear. It is fairly advantageous for terrestrial vertebrates to hear highfrequency airborne sounds—these include sounds emitted by predators, potential prey, and the vocalizations of conspecific individuals, such as calls emitted by males to call females or to delimit their territory. It

Adaptations to Life on Land / 155

Approximate age (Millions of years)

Geological eras and periods

Salientia

"Microsaures" Lysorophia Apoda Urodela

"lepos." Lissamphibia

Amniota Diadectomorpha Aïstopoda

Temnospondyli

Salientia

Urodela

Apoda

Apateon

Doleserpeton

Ecolsonia

Aïstopoda Dendrerpeton

Seymouriamorpha

Reptiliomorpha Amphibia

Embolomeri

Amphibia

"lepos." "temno." Lissamphibia Embolomeri

Seymouriamorpha

Amniota

Reptiliomorpha

(3)

Jur 213 Tri

Mesozoïc

144

248

Tympanum absent Tympanum present

Classical hypothesis

Recent alternative

Mis Pen

286 320 360

Dev

(?) (?)

Paleozoic

Per

(3)

408

Figure 6.10. Middle ear evolution. Evolution of the middle ear in stegocephalians according to an old phylogeny (to the left) and to a recent one (to the right). Modified from Laurin (1998b).

is  thus not surprising that the tympanum appeared fairly quickly in terrestrial taxa (Fig 6.10). These include anurans and mammals, which acquired the tympanum convergently, probably in the Triassic, or perhaps as late as the Jurassic in anurans. Among reptiles, the tympanum appeared at least once, but more likely twice, if turtles are not diapsids (their phylogenetic position is controversial). The appearance of the tympanum in reptiles probably occurred in the Late Permian (Müller and Tsuji, 2007; Senter, 2008). There was probably another appearance in seymouriamorphs in the Late Carboniferous, and perhaps one in some terrestrial temnospondyls at about the same time. The tympanum may thus have appeared up to six times in stegocephalians. The tympanum does not fossilize, but middle ear evolution is fairly well known because the stapes, despite its slenderness, is often preserved. When it is preserved, the stapes gives indirect clues about the presence of a tympanum because the latter can vibrate efficiently only if the stapes

156 / Adaptations to Life on Land

Figure 6.11. Stapes. Massive stapes of the temnospondyl Iberospondylus schultzei (Late Carboniferous), which probably lacked a tympanum (A to E), and of Rhinella marina (formerly known as Bufo marinus), one of the largest anurans (F to J). Both are left stapes, in anterior (A, F), dorsal (B, G), posterior (C, H), ventral (D, I), and medial (E, J) views. Note that the stapes is much more gracile in R. marina, which has a tympanum, than in I. schultzei. Modified from Laurin and Soler- Gijón (2006).

is light and has low inertia. Thus, in most extant vertebrates, a tympanum is associated with a stapes with a diameter less than 1 mm. On the other hand, tetrapods lacking a tympanum usually have a massive stapes involved in mandibular suspension (Fig. 6.11). The skull usually has an otic notch that supports the tympanum, whenever the latter is present (Fig. 6.12). However, the presence of such a notch is insufficient to infer the presence of a tympanum because, in some cases, the notch is associated with a massive stapes. By combining both criteria (size of stapes and presence of the notch), the presence of a tympanic middle ear can be inferred.

Eye The eye probably evolved less than the lateral-line organ when vertebrates invaded land because it did not require drastic modifications to

Adaptations to Life on Land / 157

Tympanum

Figure 6.12. Otic notch and tympanum. Seymouria baylorensis skull showing the otic notch, which probably supported a tympanum. Modified from Laurin (1996).

work in air. The main innovations that improved its performance on land are the lachrymal glands that keep the eye wet and a change in shape. The latter is required because the refraction index of air is 1, but that of water is 1.33. Without changes, an eye adapted to underwater vision gives a fuzzy image on land, and vice versa (as we experience when we dive without goggles). Another change, which probably occurred later, is the appearance of an eyelid to protect the eye from dehydration and dust. In amniotes, the main eyelid (the most mobile one) is the upper eyelid, whereas in lissamphibians, it is the lower eyelid. This suggests that eyelids appeared convergently in these taxa (or at least its mobility did). Its evolution is difficult to reconstruct because it generally does not fossilize. Its presence seems to be strongly linked with habitat (at least in lissamphibians) because gymnophionans, which are aquatic or fossorial, and pipids, which are aquatic, lack eyelids.

Olfactory Organ Migration of the posterior external naris into the mouth, thus becoming the choana, facilitated olfaction as well as breathing. Another noteworthy change is the disappearance of many taste buds, which cover much of the skin in aquatic vertebrates. In tetrapods, taste buds have become restricted to the mouth because they work only in water.

158 / Adaptations to Life on Land

Electrosensory Organ Various primitively aquatic vertebrates can detect electrical fields. This is useful to detect prey and predators alike. Thus, sharks can detect immobile prey, even if buried under sediment. This perception rests on special cells, called the ampullae of Lorenzini, which can also measure ambient temperature. They resemble neuromasts, but lack large cilia. Similar structures persist in some aquatic urodeles and gymnophionans, but are absent in anurans, in amphibious or terrestral lissamphibians, and in amniotes. The taxonomic distribution of these ampullae in early stegocephalians is poorly known because they leave few traces, but small solated pores on the skull of the seymouriamorph Discosauriscus have been interpreted as traces of these ampullae (Klembara, 1994).

. . . The transition from an aquatic to a terrestrial lifestyle was facilitated by several exaptations, as early as the Late Devonian. The shoulder girdle became detached from the skull through the loss of opercular bones, and this gave a new flexibility to the neck, which could thus stabilize the head while the animal walked. The sacrum transmitted the weight of the animal on land at a lower energetic cost and with less muscle fatigue than would have been possible without it. The axial skeleton was reinforced by zygapophyses, new articular surfaces between successive neural arches. The choana appeared by migration of the posterior external naris into the mouth. This habitat shift also triggered adaptations that appeared in the Carboniferous or, in some cases, later still. Limbs became more flexible, with better-defined articular surfaces, especially in the knee and elbow and later in the wrist and ankle. The axial skeleton was reinforced through consolidation of the vertebral centrum and its fusion with the neural arches. Internal gills, which dehydrate quickly on land, were lost. Costal pulmonary ventilation appeared in stem tetrapods

Adaptations to Life on Land / 159

and was subsequently lost in lissamphibians. The lateral-line and electrosensory organs were lost and the tympanum appeared, in both cases several times. The tympanum seems to have appeared well after the terrestrial lifestyle. Lachrymal glands and eyelids appeared (for the latter, probably convergently in lissamphibians and amniotes). Several of these characters leave little or no fossil evidence, which hampers evolutionary studies.

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chapter seven

Synthesis and Conclusion

CONQUEST OF LAND AND THE FIRST RETURNS TO THE AQUATIC ENVIRONMENT

The data summarized here can be used to present a preliminary reconstruction of the history of the conquest of land by vertebrates (Fig. 7.1). This synthesis suggests that all known Devonian stegocephalians were primitively aquatic. Some Carboniferous taxa, such as Crassigyrinus, baphetids, and colosteids, which were not described in this book, were probably also primitively aquatic, even though they probably had better terrestrial locomotion capabilities than those of Devonian stegocephalians. It is also possible that embolomeres were primitively aquatic, but this is uncertain because their last common ancestor with temnospondyls may have been amphibious. Some of the small-body and longer-legged temnospondyls were probably terrestrial, at least as adults (aquatic larvae are known in some of them, and may have been present in all temnospondyls). A terrestrial lifestyle probably evolved independently several times in some temnospondyls and in batrachomorphs, and within the latter, probably convergently in seymouriamorphs and in some tetrapods (Fig. 7.1). 161

Lissamphibia

Mammalia

Diapsida

Chelonia Sauropsida Amniota

Adelogyrinidae Aistopoda Urocordylidae Scincosauridae Keraterpetontidae Microbrachis Pantylus Brachystelechidae Lysorophia

Captorhinidae Caseidae Varanopidae Ophiacodontidae Edaphosauridae

Protorothyrididae

Nectridea Proganochelys

Procolophonidae

65

Limnoscelis paludis Mesosauria

Temnospondyli Embolomeri Seymouriamorpha

Colosteidae

Baphetidae

Tulerpeton Crassigyrinus

Panderichthys Tiktaalik Acanthostega Ichthyostega

Periods Cenozoic

Cretaceous 146 Jurassic 200 Triassic 251 Permian 299 Carboniferous

Synapsida Tetrapoda

Amphibia

Aquatic

Amphibious

Uncertain, amphibious or terrestrial

Uncertain, aquatic or amphibious

359 Devonian

Inferred or observed lifestyle Stegocephali

Geological time scale

Terrestrial 416

Figure 7.1. Conquest of land by vertebrates. This preliminary synthesis summarizes the works evoked in this book. Considerable uncertainty remains concerning the habitat of many taxa, such as aïstopods and caseids, and habitat evolution is ambiguous in some parts of the tree (hatching). Modified from Laurin (in press).

Synthesis and Conclusion / 163

A presumed return to an aquatic environment occurred very early in the evolution of stegocephalians because some Early Carboniferous amphibians, such as adelogyrinids, were aquatic. However, we cannot be certain if this was a primitive or a secondary condition because of uncertainty regarding the habitat of several taxa, of the complexity of habitat use evolution, and even phylogenetic affinities (some recent phylogenies suggest that adelogyrinids were stem tetrapods). There seems to have been at least two appearances of an amphibious lifestyle (in some temnospondyls and in batrachomorphs). If this is correct, and if adelogyrinids are amphibians, a return to an aquatic lifestyle occurred by the Early Carboniferous, and others occurred in the Late Carboniferous (in some nectrideans, Microbrachis, lysorophians, etc.). In amniotes, the earliest return to an aquatic environment occurred among mesosaurs (Modesto, 2006). An amphibious or terrestrial lifestyle may even have evolved five times in stegocephalians— among temnospondyls, seymouriamorphs, amniotes, and at least twice among amphibians (Fig. 7.1). Aquatic to terrestrial lifestyles thus evolved in a complex way that we are only beginning to decipher. Many more years of research will be necessary to gather sufficient data to propose a robust reconstruction of habitat preference in stegocephalians.

WHY COME ONTO LAND?

We do not know which and how many selective pressures pushed vertebrates to venture onto land. Several hypotheses have been formulated, but they are difficult to test. As we saw in Chapter Three, paleontologists abandoned years ago the old idea that seasonal aridity pushed our ancestors to walk onto land to seek more permanent bodies of water. More plausible alternatives include venturing onto land to forage, as an escape from the many aquatic predators, and even to facilitate (or enhance) thermoregulation. These possibilities deserve some explanation. An abundant arthropod fauna had inhabited the terrestrial realm from at least the Early Devonian. This fauna was a potential food resource

164 / Synthesis and Conclusion

for sarcopterygians, provided they could invade this environment. To do this successfully, sarcopterygians would have to have acquired a suite of new features not the least of which was a locomotor system allowing them to capture land-dwelling prey. Consider also the present-day observation that obligatorily aquatic animals (including vertebrates) are sometimes trapped in shallow intertidal ponds. These constitute easy prey for animals capable of walking from one pool to the next. It is possible that our first amphibious ancestors fed partly on such trapped prey in coastal regions. During the Devonian and Carboniferous periods, both marine and freshwater environments were inhabited by large predators, including chondrichthyans (sharks and their kin), placoderms (the armored gnathostomes of which Dunkleosteus, a giant form measuring about 6 m long, is one of the best known examples), some huge sarcopterygians, and even eurypterids (giant marine scorpions that could reach a length of up to 2 m; Fig. 7.2). It seems likely that land was much safer for small or midsized sarcopterygians. In the extant fauna, a similar phenomenon is observed: young individuals of many actinopterygian species inhabit shallow water, where they are sheltered from potential predators, such as other piscivorous species of larger size, or even larger, more mature individuals of the same species (cannibalism is not rare among animals). Large predators are excluded from shallow water because they risk becoming stranded and/or unable to hide from predatory reptiles, birds, and mammals that can venture into shallow water. In the Paleozoic Era, dry land may have provided an ideal shelter for some sarcopterygians. Recently, it has been suggested that our ancestors crawled onto the shores to raise their body temperature by basking in the sun (Carroll et al., 2005). Since air temperature is generally higher than water temperature in the afternoon, an animal can raise its body temperature by getting out of the water. If it is sufficiently large, its body temperature will drop relatively slowly when it gets back into the water. Ichthyostega reached about 1 m in length, and even though Acanthostega was slightly smaller, other more recent stegocephalians (such as the Early Carbon-

Synthesis and Conclusion / 165

Figure 7.2. Eurypterid. Some of these sea scorpions (two species are shown here) reached a length of 2 m and featured strong pincers with which they could attack most contemporary animals, including vertebrates. Reproduced from Haeckel (1904).

iferous Crassigyrinus) or other finned tetrapodomorphs (such as Panderichthys) were larger than Ichthyostega. The last common ancestor of stegocephalians must have been fairly large (Laurin, 2004), with a skull about 13 cm long (slightly smaller than in Ichthyostega). Animals in this size range benefit from basking in the sun. The advantage of raising the body temperature is that it accelerates metabolism, which gives more speed to the animal, and this may be advantageous to catching prey and escaping predators. These three hypotheses as to why vertebrates ventured landward (i.e., to seek prey, to escape predators, or to raise body temperature) are difficult to test, but paleontologists continue to attempt to discover ways in which they could be tested. Keep in mind that these hypotheses are not mutually exclusive. It is possible that these three, and probably more, selective pressures played a role in the evolution of land-dwelling vertebrates.

166 / Synthesis and Conclusion

MODERN PALEONTOLOGY AND THE “INDIANA JONES” STE REOTYPE

In the public imagination, paleontologists are like “Indiana Jones,” spending much of their time in the field looking for fossils. This romantic image is a reality for some paleontologists, but for most it is far from their daily experience. A paleontological field trip requires a great deal of planning. One must begin by knowing exactly where to go to find the sedimentary rocks of the right age in which the fossils being sought might occur, then one has to secure sufficient funding, obtain visas (if applicable), receive permission from local or national governments to bring back the fossils that were discovered to the laboratory for preparation, get the necessary vaccinations, and plan all the other practical aspects (who will participate, what equipment will be brought and how, etc.). If the field trip is expensive, which is often the case if a large skeleton is quarried in a remote area or if it requires the use of heavy equipment, it is often necessary to get a grant especially for this purpose. Following the expedition, an order of magnitude more time will usually be needed to prepare the fossils (i.e., to extract them from the sediments in which they were entombed). To prepare a single skeleton might require one or more years of full-time work by a qualified technician (or by a scientist, if not enough technicians are available). The fossil must then be photographed, illustrated, and often reconstructed (to correct for distortion, to put back into place disarticulated elements, and to infer the plausible size and shape of missing bones) before it is described. Further functional and phylogenetic analyses are often carried out, with all resulting data being incorporated into a scientific paper that is submitted for publication in a paleontological journal. The paper is typically sent to colleagues for evaluation and improvement before it is published. Therefore, it is easy to imagine that a successful field trip typically requires months of planning and many more months, often years, to extract the data provided by the fossils that were found. This is why most natural history museums have storage

Synthesis and Conclusion / 167

rooms filled with large blocks that await preparation, sometimes for decades after they were brought back from the field. This book is an attempt to show how much paleontological, paleobiological, and evolutionary research relies on data compiled from fossils that were previously described (Laurin, 2004). Many recent studies rely on sophisticated analyses or new statistical methods. These works can also be based on observations made on extant faunas, in which it is far easier to establish a correlation between function and morphology (Laurin et al., 2006). Most of that kind of work is done in libraries and at computers, where data are gathered and analyzed. In some cases, we must observe live animals in their environment, or prepare histological sections, or use other techniques to extract new data on extant forms. Thus, a research program on what bone microanatomy can tell us about an organism and the habitat in which it lived, be it aquatic or terrestrial (as detailed in Chapter Three), has required the accumulation of a large number of extant and fossil bones. These were either collected in the field (which was done by colleagues who collected the material for other purposes) or studied in various natural history museums (in the United States, Canada, Mexico, France, Germany, Austria, Sweden, Russia, and South Africa). Paleontologists and systematists often use sophisticated software to analyze their data, to produce phylogenies showing how organisms are related, to determine the age of taxa (through molecular or paleontological dating), to infer the function of ancient structures (modeling), or simply to produce illustrations (by editing pictures, drawing, or processing 3-D images from a high-end scanner). Paleontology remains unique in providing observations on extinct species, which constitute the vast majority of the Earth’s biodiversity (between 99% and 99.9% of the species that have inhabited this planet are now extinct, according to various estimations). Because of this, it still has a central role to play in documenting the history of life on Earth.

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GLOSSARY

Actinopterygians: group of vertebrates that possess fi ns with welldeveloped rays (lepidotrichia) and, generally, a diminutive fi n endoskeleton. It contains more than 24,000 species, including teleosts (trout, pike, herring, swordfish, etc.), sturgeons, and the paddlefish. Adaptation: character that was selected to fulfill a function that it retains, or the evolutionary process that gives rise to this character. Amniotes: group of vertebrates that includes mammals and reptiles (these include birds). Most are terrestrial. A key feature of this group is the “amniotic” egg, characterized by extra-embryonic membranes unique to this group, such as the amnios and the chorion. Amphibians: group of vertebrates that includes lissamphibians (Anura, composed of frogs and toads; Urodela, which includes salamanders and newts; and Gymnophiona, also known as caecilians or apodans) and several extinct taxa (aïstopodes, adelogyrinids, nectridiens, lysorophiens, etc.) that are more closely related to lissamphibians than to amniotes. Amphibians include several aquatic, amphibious, and terrestrial species. Analogy: relationship between two organs that fulfi ll the same function but which have different evolutionary origins. For instance, the gills of sharks and tetrapod lungs are both respiratory structures, but have distinct origins; the lung is not a transformed gill. The wings of bats and those of birds are also analogous (they represent two independent modifications of a walking forelimb). 169

170 / Glossary

Anura: taxon that includes frogs and toads; it is one of the three main lissamphibian taxa. The vernacular term “anuran” is equivalent. Apomorphy: derived (recent) character; it is an evolutionary innovation. Autapomorphy: derived (recent) character unique to a taxon. For instance, mammary glands are an autapomorphy of the taxon Mammalia (which includes mammals). Autotrophic (adj.): capable of producing organic substances (often sugars) from simpler substances, using an energy source, like sunlight in photosynthesis. A few examples of autotrophic organisms include cyanobacteria, red and brown alga, and green plants. batrachomorpha: the smallest clade that includes tetrapods and seymouriamorphs. Branch: segment of an evolutionary tree that separates two nodes (terminal taxa, at the tip of the tree, are also nodes). Usually, branch length reflects evolutionary time, but it can also represent observed evolutionary change (e.g., in nucleotide sequences or in morphological characters). Chondrichthyans: group of aquatic vertebrates with an entirely cartilaginous endoskeleton. It includes chimera (ratfish) and elasmobranchs (sharks, skates, and rays; the latter two are sharks that acquired a flattened body shape). Clade: monophyletic group, such as birds, mammals, or tetrapods. Cladistics: technique that can be used to reconstruct evolutionary relationships by using shared derived (evolutionarily unique) characters. Cladogram: diagram showing the evolutionary relationships between taxa. It shows only a topology (branch lengths are not illustrated). Cladograms do not show the absolute age of taxa. Crown group: smallest clade that includes two extant taxa. For instance, amniotes form a crown group composed of the smallest clade that includes mammals and reptiles. Dipnoans: group of primitively aquatic vertebrates (also known as lungfishes); they possess paired fi ns, gills, and lungs. Dipnoans are the closest extant relatives of tetrapods. Euramerica: continent that included Laurentia (which itself corresponds with most of North America), Baltica (plate that included the territory now occupied by Baltic countries), and other plates that represent much of Europa. It formed in the Devonian through the collision between Laurentia and Baltica) and became integrated into Pangea in the Permian. Euramerica is also known as Laurussia or the Old Red Sandstone Continent.

Glossary / 171

Exaptation: character that was selected for a function that it no longer has, or that is no longer its main function. Fossil: remains (usually of a mineralized structure, bone, shell, etc.) or trace of activity (tracway, burrow, etc.) of ancient organisms (generally older than 12,000 years). Gnathostomes: jawed vertebrates. This taxon includes, among others, chondrichthyans and osteichthyans. Gymnophiona: taxon that includes extant limbless amphibians. They are tropical and poorly known because many species are fossorial (i.e., subterranean; the others are aquatic). Homology: relationship between two organs or structures that have a common evolutionary origin, even though their function and aspect may differ (for instance, the tetrapod lung and the teleost swim bladder). Lepidotrichia: dermal fi n rays. They are composed of long, slender bony elements, primitively segmented, branched, and paired, although in some taxa, they may fuse to each other to form spiny structures (as in the perch) that are unsegmented, not ramified, and median (not paired). Lissamphibia: taxon (whose members are called “lissamphibians”) that includes the three large clades of extant amphibians (anurans, urodeles, and gymnophionans) but not Paleozoic amphibians. Metapterygial axis: axis that appears in embryonic fi ns and along which structures homologous with arm and leg bones develop. Monophyletic (adj.): includes all the descendants of an ancestor (for instance, the taxon Mammalia, which includes all extant mammals, is monophyletic). Monotypic (adj.): redundant. Applies to a taxon (under rank-based nomen clature) that includes a single taxon of the immediately lower rank. For instance, a family that includes a single genus, or a genus that includes a single species, is monotypic. Neoteny: retention of larval or juvenile characters in adults (defi ned as individuals that have reached sexual maturity). Neural arch: part of the vertebra that surrounds the spinal chord. Node: either end of a branch of a phylogenetic tree. Internal nodes are most often discussed; these occur at the meeting point of two branches, but the tips of terminal branches (which may represent species) are also nodes. Osteichtyans: group of vertebrates whose internal skeleton is largely ossified. It includes aquatic (actinopterygians, dipnoans) and terrestrial (tetrapods) taxa.

172 / Glossary

Outgroup: taxon related to a group whose phylogeny we want to study (the latter is the ingroup). Generally, the outgroup must be closely related to the ingroup, but it must not be part of it. Thus, to study tetrapod evolution, dipnoans are the most appropriate extant outgroup. Paraphyletic (adj.): includes only a subset of the descendants of the last common ancestor of its members (for instance, the taxon Reptilia under rank-based nomenclature, when excluding birds). Phylogeny: diagram that represents the evolutionary relationships between taxa (or more rarely, genes or organisms). It includes a topology (which indicates only a nested or hierarchical pattern of relationships) and branch lengths (which represent the evolutionary distances between taxa). Reptiliomorphs: taxon that includes amniotes (mammals and reptiles) and all extinct groups (such as diadectomorphs) that are more closely related to amniotes than to lissamphibians (extant amphibians). Sarcopterygians: taxon that includes the coelacanth, dipnoans, and tetrapods, in addition to various extinct taxa. Squamates: taxon that includes “lizards” (a paraphyletic group), snakes, and amphisbaenians (small squamates with reduced limbs, if any). Stegocephalians: taxon that includes all limbed vertebrates and a few closely related species which may have retained paired fi ns. Stem group: paraphyletic group that includes all extinct species which are more closely related to one crown group than to another crown group. For instance, stem tetrapods include extinct species that are more closely related to tetrapods (a crown group) than to dipnoans (the most closely related crown group). It is a purely phylogenetic concept. Thus, some stem tetrapods had digits, such as Acanthostega, whereas others had paired fi ns, such as Eusthenopteron. Stem tetrapods: paraphyletic group that includes all organisms which are more closely related to tetrapods (without being part of the crown group) than to their closest extant relatives (dipnoans). This group includes animals with digits, such as Acanthostega, and others with paired fi ns, such as Eusthenopteron. Stromatolite: a layered, pillow-shaped structure formed by the trapping and binding of sedimentary particles by the biofi lms of various microorganisms, especially of cyanobacteria (photosynthetic bacteria). Synapomorphy: derived (recent) character (an evolutionary novelty) shared by at least two taxa. Synapomorphies are usually taken as evidence of close relationships. For instance, digits are present in most tetrapods and show

Glossary / 173

that they are closely related, whereas the coelacanth, salmon, and sharks, which retain fi ns (an older character), are more distantly related to each other and to tetrapods. Systematics: science that studies the diversity and evolution of biological organisms. It includes taxonomy. Taxon: group of closely related biological organisms. Taxonomy: field in systematics concerned with the recognition, naming, and delineation of taxa. Taxonomy may also designate a classification of biological organisms. Teleosts: group of primitively aquatic vertebrates (a few amphibious species exist) that possess fi ns with dermal rays (lepidotrichia) and a swim bladder. It includes several commercially important species (trout, herring, salmon, tuna, swordfish, etc.). Tetrapoda: smallest clade that includes lissamphibians (frogs, salamanders, and gymnophionans) and amniotes (mammals and reptiles). Tetrapodomorphs: group that includes tetrapods and stem tetrapods (all extinct sarcopterygians that are more closely related to tetrapods than to dipnoans). This taxon includes all stegocephalians as well as some fi nned sarcopterygians, such as Eusthenopteron. Topology: relative position of taxa in a phylogeny as shown by a cladogram or a similar diagram. A topology includes data only on the relative kinship of taxa, not their evolutionary distance. Urodela: taxon (whose members are called “urodeles”) that includes salamanders and newts; this is one of the three main lissamphibian groups. Vertebral centrum: the part of the vertebra located under the spinal chord, which partly replaces and surrounds the notochord.

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INDEX

Note to readers: Bold page numbers indicate illustrations and their captions. Acanthostega appendicular skeleton, 80, 83 branchial skeleton, 146 fossils, 42 gills, 88– 89 lateral-line organ, 69 limb evolution, 83, 85, 136–140 neural arches, 140 shoulder girdle, 145 skeleton, 74, 85 in stegocephalian phylogeny, 130–131 thermoregulation, 164 acarians, 60 Acipenser, 77, 80 actinistians appendicular skeleton, 80 evolution, 49 lung evolution, 144 time span, 47 actinopterygians appendicular skeleton, 80 breathing evolution, 143 defi ned, 169 endoskeleton, 79

as fodder, 64, 164 Hox gene expression, 78 Hox genes, 76 jaw suspension, 152 metapterygial axis, 78–80 phylogeny, 20 skin and the water exchange, 148 adaptation overview, 135–136 of amphibians, 52, 54 aquatic, 70 of arthropods, 60 defi ned, 169 digit evolution, 88 adelogyrinids amphibians and, 117, 119, 121 land, freshwater, or sea?, 163 phylogeny, 132 age of taxa, 6, 21, 26–37 aïstopods, 117, 119 algae, 56 Amia, 38 ammonites, 62 amnios, 169

187

188 / Index

amniotes, 122 ancestor of all, 93 bone microanatomy and habitat, 93– 94 breathing evolution, 143 compared with amphibians, 51 dating, 32–33 defi ned, 169 diadectomorphs and, 121 divergence from lissamphibians, 32 ears, 152 egg, 51 electrosensory organ, 158 eyes, 157 fossils, 40, 42 land, freshwater, or sea?, 163 lateral-line organ, 150 Ophiacodon, 94 in the Paleozoic, 125–129 phylogeny, 18, 127–134 skin and the water exchange, 149–150 skull, 127 as terrestrial, 51 vertebral centrum, 142 Amphibia, 9 amphibians age of taxa, 25 defi ned, 169 land, freshwater, or sea?, 163 lifestyle evolution, 53 misnomer, 66 in the Paleozoic, 116–121 phylogeny, 105, 117, 127–134 polydactyly, 86– 87, 87 reproduction, 51–54 skin and the water exchange, 149 temnospondyls and, 106 the term discussed, 116 as terrestrial, 51–52 amphioxus, 75, 76 amphiumids, 54 analogy, 37–39, 169 ancestors, 17 overview, 16–21 of amphibians, 52

freshwater theory, 64 jaw structure, 48 marine origins, 67 taxon designation, 6 annelids, 31, 62– 63 Anura, 30, 170 anurans aquatic, 54 dating, 32 divergence from gymnophionans, 32 ears, 152, 155–156 electrosensory organ, 158 phylogeny, 105, 131–132 reproduction, 52 skin and the water exchange, 148–149 stapes, 156 taxonomy, 9 temnospondyls and, 103 apomorphy, 14, 15, 23, 170 appendicular skeleton of osteichthynas, 80 of Proterogyrinus, 110 of tetrapodomorphs, 83 aquatic environment, return to, 161–163 arachnids, 57– 61, 61 archosaur, 126 Aristotle, 2 arthropods overview, 57– 61, 59 becoming herbivorous, 60 becoming terrestrial, 46 nomenclature, 3 phylogeny, 20, 58 autapomorphy, 170 autopods digit evolution, 85– 86 exclusive to stegocephalians, 99 fi n endoskeleton, 79– 81 origin of, 75–79 autotrophic, 170 autotrophic organisms, 55–57 Avalonia, 41 axial skeleton, 140–142

Index / 189

bacteria, 56, 172. See also cyanobacteria baphetids, 161 batrachomorphs, 142, 161, 163 Bayesian age determination, 36 Bible, 2 biodiversity, 9 birds breathing evolution, 142 character evolution, 23 divergence from mammals, 32 limb evolution, 138 nomenclature, 10 phylogeny, 20 skin and the water exchange, 149 bivalves, 62 bone microanatomy compactness profi le model, 92, 95 lifestyle and, 89– 96 Bone Profiler, 90, 91, 95 bones in amniotes, 127 aquatic adaptation, 70, 71 in coelacanths, 47 electrosensory organ, 158 in embolomeres, 106, 108–109 fi n endoskeleton, 79 lateral-line organ, 69, 150 limb evolution, 77, 85, 138–139 in Triadobatrachus, 119 in the vertebrate skeleton, 73–75 branch length, 21, 33, 36, 37, 58, 170 branches, 15, 21, 170 branchial skeleton, Acanthostega, 146 Branchiostoma, 76 breathing, 146–147. See also gills; lungs Bufo, 156 Cacops, 136–138, 137, 139 caecilians, 9, 52 calibration dates overview, 31–35 branch lengths and, 37 fossil record, 32 Captorhinus, 94, 127

Carboniferous, 36, 40, 41, 53, 67, 162 conquest of land, 45, 47, 50 cartilage, 73–75, 89, 138, 140 CDI (cortico-diaphyseal index), 91 Cenozoic, 53, 162 centipedes, 57, 60 centrum, 103, 107. See also vertebral centrum cephalopods, 62, 62 Cervus, 90 characters overview, 16–21 in adaptation, 169 age and polarity, 18–20 in apomorphy, 170 in autapomorphy, 170 in cladistics, 170 defi ned, 16–17 dipnoan, 50 evolution, 21–24, 23 in exaptation, 171 polarity, 19 in synapomorphy, 172 choana, 144, 157 chondrichthyans, 100 defi ned, 170 Iberian habitat, 65– 66 jaw suspension, 152 phylogeny, 20 predator, 164 skin and the water exchange, 148 chorion, 51 chroniosuchian, 107 chronology of relevant events, 39–40 clade, 170 cladistics, 21, 24, 170 cladogram, 20, 170 classification. See nomenclature; taxonomy clitellates, 63 coelacanths overview, 47–49 appendicular skeleton, 80 evolutionary tree, 24–26 fi n endoskeleton, 79

190 / Index

coelacanths (continued) freshwater theory, 64 phylogeny, 18 skin and the water exchange, 148 skull, 48 taxonomy, 8 colosteids, 161 comparative analyses, 1 Cope, E. D., 103, 127–132 cortico-diaphyseal index (CDI), 91 Cotylorhynchus, 126 cotylosaurs, 122, 132–133 crabs, 46–47, 57– 61, 59 Crassigyrinus, 161, 164 credibility interval, 36 Cretaceous, 30, 36, 53, 162 crown group, 170 cryptobranchids, 54 cyanobacteria, 56 Cyclorana, 149 Czatkobatrachus, 119 Danio, 77–78 dating taxa comparison, 34–37 molecular, 31–34 paleontological, 26–30 Delphinus, 90, 92 Delta, Iowa, USA, 41 dermal skeleton, 73–74, 74 Devonian, 36, 40, 41, 67, 162 conquest of land, 45, 49–50 plant evolution, 56–57 Diadectes, 125 diadectids, 122, 123, 123 diadectomorphs, 121–125, 122, 123, 127, 127–134 diaphysis, 89 digit evolution overview, 75– 87 pentadactyly, 83, 86– 87 polydactyly, 81– 87, 106 Dimetrodon, 122, 126 dinosaurs, 125, 135 Diplocaulus, 119

dipnoans overview, 49–50 appendicular skeleton, 80 breathing evolution, 143–144 defi ned, 170 fi n endoskeleton, 79 freshwater theory, 64 lung and swim bladder, 38 metapterygial axis, 78–80 phylogeny, 18 Discosauriscus, 115, 115–116, 158 dissorophoids, 95 Doleserpeton, 94– 95, 95 Dunkleosteus, 164 Dutuitosaurus, 70, 71 ears. See also otic notch adaptation to land, 151–156 in diadectomorphs, 123 gecko, 154 in Haptodus, 128 in Iberospondylus, 102 in seymouriamorphs, 113 skeletal support, 74 stapes compared, 156 earthworms, 16, 18, 62– 63 East Kirkton, Scotland, 41 echidna, 126 Edaphosaurus, 126 eels, 50, 147 eggs of amniotes, 126–127 amniotic, 51, 169 amphibian reproduction, 51–54 diadectomorph, 122 of Limnoscelis, 125 nomenclature, 10 Elginerpeton, 84, 84– 86 Ellesmere Island, Canada, 41 Elpistostege, 42 embolomeres land, freshwater, or sea?, 161 lateral-line organ, 151 lung evolution, 143 in the Paleozoic, 106–109, 110–111

Index / 191

phylogeny, 108 in stegocephalian phylogeny, 127–134 vertebral centrum, 141, 141–142 endoskeleton of Acanthostega, 71 breathing evolution, 144 fi ns, 77, 79– 82 of Microbrachis, 120 of seymouriamorphs, 113 in vertebrates, 73–75 Eocaecilia, 121 Eogyrinus, 107 epiphyses, 89– 90 Erpetoichthys, 38 Eryops, 81, 99–101, 100 Erythrinus, 38 eukaryotes, 56 Euramerica, 106, 170 euryhaline, 50 eurypterids, 164, 165 Eusthenopteron appendicular skeleton, 80, 83 fossils, 41–42 limb evolution, 81, 81– 82 phylogeny, 9 vertebral centrum, 140–141 evolution. See also limb evolution actistinian, 49 of amphibians, 54 of appendages, 86 of appendicular skeleton, 80 of bones, 92 ears, 155 eyes, 157 irreversible nature of, 47 lateral-line organ, 151 skin and the water exchange, 148 in stegocephalians, 86 of terrestrial ecosystems, 55 trends, 136 vertebral centrum, 141 evolutionary trees overview, 1, 2, 24–26 Anura supertree, 30

bone microanatomy and habitat, 92– 93 metazoan, 58 phylogeny, 17–18 exaptation, 88, 135, 139–140, 171 exoskeleton, 73–74 eyes overview, 156–157 in arthropods, 59 in Discosauriscus, 115, 116 in Periophthalmus, 46 skeletal support, 74 fangs. See teeth and fangs feathers, 23, 135 fi ns in Acanthostega, 74, 88 aquatic adaptation, 71 in coelacanths, 47–48 in dipnoans, 50 evolution into limbs, 81 fossils, 41–42 freshwater theory, 64 Hox gene expression, 75–80 monobasal, 79 in Panderichthys, 139 in Periophthalmus, 46 phylogeny, 19, 20 in Proterogyrinus, 110 sarcopterygian, 79– 83 fish, 3, 6–10, 8 Florence, Nova Scotia, Canada, 41, 41, 43 food, availability on land, 163–166 fossil record calibration dates, 31–35, 32, 36, 37 conquest of land, 45, 45–50 dating, 34–37 evolutionary trees, 24 limb evolution, 82–87 paleontological dating, 26–30, 27 phylogeny, 16–18, 21 fossilization, 16, 65, 126–127

192 / Index

fossils of amniotes, 125, 126–127 of amphibians, 119, 121 defi ned, 171 of dipnoans, 50 of Elginerpeton, 84 freshwater theory, 65– 67 hunting and recording, 166–167 lacking, 16 lateral-line organ, 150 of Limnoscelis, 124 living: coalacanths, 47–48 locations, 39–41 of onychophorans, tardigrades, 63 of Ophiacodon, 93 of plants, 55–56, 60 red beds, 63– 68 of seymouriamorphs, 109–113, 111 of temnospondyls, 102–103 freshwater habitat, 50, 52, 62– 68, 71–72, 99, 147–148, 164 freshwater sharks, 64– 67 fungi, 57 Gallus, 77 gastropods, 62, 62 gecko, 154 geologic time scale, 39–40, 40 ghost range, 27 gills in Acanthostega, 88– 89 in arthropods, 58–59, 60 in dipnoans, 49 in Discosauriscus, 115–116 homology and analogy, 37–39 loss of, 135, 144–146 in Microbrachis, 119 in mollusks, 62 in Periophthalmus, 46 in Proterogyrinus, 111 in seymouriamorphs, 114 skeletal support, 75

in temnospondyls, 103, 104 water exchange, 147 girdles in Acanthostega, 88, 145 defi ned, 138 evolution, 136–140 fi n endoskeleton, 79 limb evolution, 85 skeletal support, 74 glomerula, 147–149 gnathostomes, 171 gobiids, evolutionary radiation, 46 Gogo Formation, Western Australia, 42 Gondwana, 41 green plants, 56–57 Greenland, 41 gymnophionans body shape, 71 defi ned, 171 divergence from anurans, 32 electrosensory organ, 158 eyes, 157 jaw suspension, 152 in the Jurassic, 121 phylogeny, 9, 132 polydactyly, 87 reproduction, 52 skin breathing, 146 habitat, 89– 90, 92– 93 Haptodus, 126–128, 129 hearing. See ears Hennig, Willi, 21, 24 herbivores, 126 Hominidae, 4 Homo sapien classification, 4 homology overview, 37–39 among appendicular skeletons, 80 defi ned, 171 synapomorphy and, 82 Hox genes, 75–79, 78 Hynerpeton, 85

Index / 193

Iberospondylus, 66, 101–102, 102, 156 Ichthyostega fossils, 42 gill loss, 145 limb evolution, 83, 85 skeleton, 139 skull, 109, 139 in stegocephalian phylogeny, 130–131 tail, 88 taxonomy, 10 thermoregulation, 164–167 vertebral centrum, 106, 141, 141 insects, 57, 60 International Code of Botanical Nomenclature, 56 International Society for Phylogenetic Nomenclature, 15 intracranial articulation in coelacanths, 48 jaw suspension, 152–153, 153 Joggins, Nova Scotia, Canada, 41, 41–43, 93, 125 Jurassic, 30, 36, 41, 53, 67, 162 Karaurus, 71, 71 lachrymal glands, 157 land, conquest of, 45–54 land, freshwater, or sea?, 161–166 larvae in amphibians, 119 in arthropods, 59 in Discosauriscus, 115–116 lateral-line organ, 68– 69, 150 neoteny and, 171 in seymouriamorphs, 114, 151 in temnospondyls, 103, 104, 161 in tetrapods, 51–52 lateral-line organ overview, 150–151 in Discosauriscus, 115 in Dutuitosaurus, 70 in embolomeres, 106

in Microbrachis, 120 in Proterogyrinus, 110–111 in stegocephalians, 68–72 Latimeria, 47, 80 Laurasia, 41 leeches, 62– 63 Lepidodendron, 43 lepidoptrichia, 171 Lepidosiren, 38, 49–50 Lepisosteus, 38 lepospondyls, phylogeny, 130–134 lichens, 57 lifestyle evolution, metazoan, 58 likelihood, 26, 34, 43 limbs in amphibians, 117 in amphiumids, 54 aquatic adaptation, 70 evolution, 12, 73– 97, 81, 136–140 as exaptation, 135 fossils, 40, 42 in Microbrachis, 120, 121 phylogeny, 16, 18, 19, 20 in sarcopterygians, 68 in stegocephalians, 69 in Triadobatrachus, 119 Limnodynastes, 149 limnoscelids, 123 Limnoscelis, 124, 124–125, 127 Linnaean (rank-based) nomenclature, 2– 6 Linnaeus, 3– 6, 10 Linton, Ohio, USA, 42 lissamphibians age, 29, 32–33 defi ned, 171 divergence from amniotes, 32 diversification, 36 in the Early Triassic, 119 electrosensory organ, 158 evolution, 53–54 eyes, 157 freshwater habitat, 64– 66 Karaurus, 71

194 / Index

lissamphibians (continued) lateral-line organ, 69, 150 lung evolution, 143 phylogeny, 105, 130–134 relatives, 171 skin and the water exchange, 148 temnospondyls and, 103 living fossils, 47–48, 50, 54 locomotion, 136–140. See also walking long bones, 91 lungfish, 25, 38. See dipnoans lungs absent in Periophthalmus, 46 in arthropods, 58, 60 in coelacanths, 48 in dipnoans, 49, 54 in embolomeres, 106 evolution, 38, 142–144 homology and analogy, 37–39 in mollusks, 62 in temnospondyls, 101 lycopods, 43 lysorophians, 117, 119, 163 Mammalia, 10, 11, 12 mammals, 25, 32 mandibular suspension, 152, 153, 156 Mastodonsaurus, 99, 103 mesenchyme, 74 mesomeres, 79, 80 metaphysis, 89– 90 metapterygial axis defi ned, 171 Hox gene expression, 77–80 limb evolution, 81 in osteichthyans, 80 in sarcopterygians, 79– 82 of tetrapodomorphs, 83 Metaxygnathus, 65, 85– 86 metazoans, phylogeny, 58 Metoposaurus, 104 Microbrachis, 119, 120, 120–121, 163 microsaurs, 117 MIG (Minimum Implied Gap), 27 Miguasha, Quebec, Canada, 41, 41, 42

Minimum Implied Gap (MIG), 27 molecular clock, 31–32 molecular dating, 31–34, 32, 93 mollusks, 3, 20, 62, 62– 63 monophyletic, 6–10, 8, 105, 173 monophyly, compared with paraphyly and polyphyly, 7 monotypic, 171 Mus, 77 myriapods, 57, 60 names, vernacular, 3 nectrideans, 117–119, 118, 163 Neobatrachus, 149 Neoceratodus, 49, 80 Neogene, 30, 36 neomorphs, 77–78, 81 neoteny, 150, 171 neural arches adaptation to land, 140–142 in amphibians, 117 defi ned, 171 in diadectomorphs, 123 in Proterogyrinus, 110 in seymouriamorphs, 113 in stegocephalians, 107 in temnospondyls, 103 neurocranium, 74, 152, 153 neuromasts, 150–151, 158 New South Wales, Australia, 41 Ningxia Hui Autonomous Region, China, 41 nodes, 8, 15, 24, 171 nomenclature overview, 1–15 defi ned, 5 phylogenetic, 14 phylogenetic nomenclature, 10–15 rank-based (Linnaean), 2– 6 vertebrate taxonomy, 6–10 notochords, 75, 103, 140 Nýqany, Czech Republic, 41 Obruchevichthys, 85 Old Red Sandstone. See red beds

Index / 195

ontogeny in amphibians, 51, 119 bone microanatomy, 89 in Discosauriscus, 115–116 in seymouriamorphs, 115–116 in stegocephalians, 75, 103, 117 onychophorans, 62– 63 Ophiacodon, 93, 93– 95, 94 Ornithorhynchus, 90 ostariophysean, 151 osteichthyans, 80, 143–144, 171 otic notch. See also ears in Discosauriscus, 115, 116 in embolomeres, 106 in Microbrachis, 121 in Proterogyrinus, 110 in Seymouria, 157 in seymouriamorphs, 113 in temnospondyls, 102 outgroups, 20, 24–25, 172 Paleogene, 30, 36 paleontological dating, 27 paleontology, modern, 166–167 Panderichthys, 141, 164 Pangea, 41, 170 paraphyletic, 6–10, 172 paraphyly, compared with monophyly and polyphyly, 7 parsimony overview, 21–24, 22 analysis of arthropod evolution, 57 character evolution, 23 in dating taxa, 27 evolutionary trees, 24–26 in lissamphibian habitat, 54 regarding the fi rst amniote, 126 pelycosaurs, 126 Penalized Likelihood (PI), 34 pentadactyly, 83, 86– 87, 87 Periophthalmus, 46, 54 Permian, 36, 40, 53, 67, 164 photosynthetic organisms, evolution, 55–57 Phyllomedusa, 148

PhyloCode, 15 phylogenetic nomenclature, 10–15, 14 phylogenetics overview, 1–2, 16–37 ancestors and characters, 16–21 dating comparison, 34–37 evolutionary trees, 24–26 molecular dating, 31–34 paleontological dating, 26–30 parsimony, 21–24 phylogeny amphibian, 117 Anura supertree, 30 character polarity and, 19 defi ned, 172 embolomere, 108 hypothetical, 5 metazoan, 58 middle ear evolution, 155 sarcopterygian, with taxonomy, 9 stegocephalian, 127–134, 131, 133 with taxonomy, 8 temnospondyl, 105 vertebral centrum, 141 the weight of tradition, 130–132 phylology, 6–10. See also monophyly; paraphyly; polyphyly PL (Penalized Likelihood), 34 pipids, 52, 54, 69, 157 placoderms, 64, 164 plants, 55–57 platypus, 90, 126 plesiomorphy, 23 plethodontid, 146 polydactyly, 81– 87, 87, 106 Polyodon, 78 polyphyletic, 6–10 polyphyly, compared with monophyly and paraphyly, 7 Polypterus, 38, 76 preadaptation. See exaptation predators, escaping, 163–166 Prosalirus, 30 Proterogyrinus, 110–111

196 / Index

Protopterus, 38, 49–50 Ptyodactylus, 154 Puertollano, Spain, 66, 101 Puertollanopus, 66 quartet dating method, 33 rank-based (Linnaean) nomenclature, 2– 6, 12–14 red beds, 63– 68, 170 Red Hill, Pennsylvania, USA, 41 reptiles, 25 Reptilia, 9, 9, 10 reptiliomorphs defi ned, 172 diadectomorphs as, 121 embolomeres as, 106, 108 lateral-line organ, 151 pentadactyly, 87 phylogeny, 105 seymouriamorph phylogeny, 114 stegocephalian phylogeny, 130, 133 vertebral centrum, 142 rhachitomous, 103, 106, 107, 141 Rhinella, 156 rhizodontids, 80, 82 Romer, A. S., 94, 124, 147 Romer’s gap, 42, 93 saltwater tolerance, 52, 64– 66, 67, 101 sandstone, 63– 65, 170 sarcopterygians appendicular skeleton, 83 defi ned, 172 Devonian, 63– 64 fi ns and Hox gene expression, 80–83 as fodder, 164 freshwater habitat, 64 Hox genes, 76 jaw suspension, 152 land’s attraction, 163–164 limb evolution, 86, 139–140 metapterygial axis, 78–80 phylogeny, 20 phylogeny and taxonomy, 9

red bed habitat, 68– 69 reproduction in the Paleozoic, 52 similarity to coelacanths, 47 similarity to dipnoans, 50 sauropsids, 125 scorpions, 60, 164, 165, 165 sensory organs. See individual organs Seymouria, 122 otic notch, 116, 157 skeleton, 113 skull, 112, 157 seymouriamorphs, 122 compared with temnospondyls, 103 ears, 151, 155, 158 geographic distribution, 110 land, freshwater, or sea?, 161, 163, 165 lung evolution, 143 in the Paleozoic, 109–116 phylogeny, 114, 127–134 skull, 109 vertebral centrum, 141, 141–142 sharks, freshwater, 64– 67 Sigillaria, 43 Sinostega, 66 sirenids, 54, 69 sister groups, 16, 17 skeleton. See also skull appendicular, 80, 83, 110 axial, adaptation to land, 140–142 branchial, Acanthostega, 146 Cacops, 139 chroniosuchian, 107 dermal, Acanthostega, 74 dermal skeleton, 71, 73–74 diadectomorph, 123 Discosauriscus, 115 exoskeleton, 73–74 Ichthyostega, 139 Proterogyrinus, 111 Seymouria, 113 vertebrate, 73–75 visceral, 74, 75, 145, 146 skin and the water exchange, 147–150 skin breathing, 146–147

Index / 197

skull amniotes, 127 Cacops, 141 Captorhinus, 127 diadectomorphs, 127 Dutuitosaurus, 70 Haptodus, 129 Iberospondylus, 102 Ichthyostega, 139 Karaurus, 71 Limnoscelis, 124, 127 Microbrachis, 120 Proterogyrinus, 111 Seymouria, 112, 155 snakes, 9, 12, 20, 71 species, 104 sphenacodontids, 126 squamates, 9, 126, 154, 172 stapes, compared, 156 stegocephalians amniotes, 125–127 amphibians, 116–121 appendicular skeleton, 80, 83 aquatic in the Devonian, 88– 89 bone microanatomy, 92– 96 breathing evolution, 143–147 defi ned, 172 dermal skeleton, 74 diadectomorphs, 121–125 diversity in the Paleozoic, 99–135 Dutuitosaurus, 70 ears, 151–155 electrosensory organ, 158 embolomeres, 106–109, 110–111 endoskeleton, 75 evolution of osmotic tolerance, 67 freshwater theory, 64– 67 land, freshwater, or sea?, 161–165 lateral-line organ, 68–72, 150–151 limb evolution, 82–85, 86, 136–140 middle ear evolution, 155 phylogenies compared, 155 phylogeny, 127–134, 131, 133 polydactyl evolution, 87 red bed fossils, 63– 64

red bed habitat, 68 seymouriamorphs, 109–116 skin and the water exchange, 147–150 skull, 109 temnospondyls, 99–106 thermoregulation, 164–165 vertebral centrum, 141, 141 stem group, 172 stem tetrapods. See also tetrapods defi ned, 172 Doleserpeton, 95 embolomeres, 108, 109 fi n endoskeleton, 79 limb evolution, 136 pentadactyly, 87 seymouriamorph phylogeny, 114 seymouriamorphs, 116 in stegocephalian phylogeny, 127–134 temnospondyls, 105, 106 stereospondyls, 103–104, 141, 141 stromatolite, 172 stylopod, 75, 77 swim bladder, 37–39, 38 synapomorphy character evolution, 23 defi ned, 82, 172, 173 of eggs, 126–127 Hox gene expression, 78 saltwater intolerance, 66 of stegocephalian clades, 133 synapsids, 10, 125–126, 128–129 systematics, 173 tails in Acanthostega, 88 in amphibians, 52 in embolomeres, 106, 110 in Ichthyostega, 88 in Periophthalmus, 46 in Proterogyrinus, 110 in stegocephalians, 71, 75 in Triadobatrachus, 118, 119 tardigrades, 62– 63

198 / Index

taxa, taxon dating, 26–37 defi ned, 173 delimitation, 5, 6 names, 14 taxonomy overview, 2, 6–10 defi ned, 173 with phylogeny, 8 sarcopterygian, with phylogeny, 9 teeth and fangs in amphibians, 117 dentine, 118 in diadectomorphs, 123, 124 in dipnoans, 50 in embolomeres, 106 in Haptodus, 128–129 in Limnoscelis, 124 in Proterogyrinus, 111 teleosts defi ned, 173 ears, 151 Hox gene expression, 77 Hox genes, 76 lateral-line organ, 150 lung and swim bladder, 38 Periophthalmus described, 46 temnospondyls, 100 ears, 151, 155–156 land, freshwater, or sea?, 161, 163 limb evolution, 136–137, 139 lung evolution, 143 in the Paleozoic, 99–106 phylogeny, 105, 127–134 polydactyly, 87 stapes, 156 vertebrae, 107 vertebral centrum, 141, 141–142 tetrapodomorphs appendicular skeleton, 83 defi ned, 173 lateral-line organ, 150 limb evolution, 83 lung evolution, 144 thermoregulation, 164

tetrapods. See also stem tetrapods body shape, 71 bones compared, 89– 90 breathing evolution, 142–144 defi ned, 173 digit evolution, 78, 80–87 ears, 151, 156 evolutionary tree, 24–25 extant, bone microanatomy, 89– 92 eyes, 157 false identification, 85 Hox gene expression, 78 land or sea?, 161 lateral-line organ, 150 limb evolution, 137–138 long bones, 90 lung and swim bladder, 38 origin of, 32 pervasiveness of, 46 phylogeny, 18, 20 reproduction among, 51–54 skeletal structure, 75 skin and the water exchange, 149 taxonomy, 8 vertebral centrum, 141, 141–142 therapsids, 126 thermoregulation, 163–166 Tiktaalik, 42, 80, 82, 83 time span, 39–40 topology, 80, 173 Triadobatrachus, 119, 121 Triassic, 36, 53, 67, 162 trilobites, 59 Trimerorhachis, 100 tristichopterids, 9, 80, 83 Tseajaia, 125 tseajaids, 123 Tula, Russia, 41, 41–42, 83 Tulerpeton, 42, 66, 83, 83, 85 turtles aquatic adaptation, 70, 88 body shape, 71 ears, 155 eggs, 126–127

Index / 199

phylogeny, 20 taxonomy, 9 tympanum in amphibians, 116 in diadectomorphs, 123 ear evolution, 152–156 in embolomeres, 106 evolution, 153–156 of Microbrachis, 121 in Seymouria, 157 stapes and, 156 types, 5 Undichna, 66 urodeles aquatic, 54 compared with other stegocephalians, 71 compared with temnospondyls, 103 defi ned, 173 electrosensory organ, 158 evolutionary tree, 25 jaw suspension, 152 in the Jurassic, 121 limb evolution, 138 phylogeny, 131–132 reproduction, 52 uterus of amniotes, 51

Ventastega, 85 vertebrae, 74–75, 107, 118 vertebral centrum adaptation to land, 140–142 in amphibians, 117 defi ned, 173 diversity and evolution, 141 in embolomeres, 106–107 in Proterogyrinus, 110 in seymouriamorphs, 113 in stegocephalian phylogeny, 130–131 in temnospondyls, 103 visceral skeleton, 74, 75, 145, 146 vision. See eyes walking in arthropods, 60 in coelacanths, 48 limb evolution, 73, 82, 88, 136–140 in onychophorans, 63 in stegocephalians, 66 in tardigrades, 63 whales, 3, 70, 88 Whatcheeria, 141 xenacanthids, 65, 65– 66, 100 zeugopod, 75, 77

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