2Phylogenetic Systematics and the Origins of Amphibians and Reptiles

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Phylogenetic Systematics and the 2 Origins of Amphibians and Reptiles

he extant amphibians and reptiles are a diverse collection of animals with evolutionary histories dating 2.1  Principles of Phylogenetics Tback to the Early Carboniferous period. A phylo- and Taxonomy genetic perspective helps us visualize the relationships among these organisms and interpret the evolution of Phylogenies are the basis of the taxonomic structure of rep- their physiological, morphological, and behavioral char- tiles and amphibians. A taxon (plural taxa; from the Greek acteristics. To gain this perspective, it is important to un- tax, “to put in order”) is any unit of organisms given a for- derstand how phylogenies are created and used. Thus, mal name. For example, the common five-lined skink (Ples- we begin with a brief review of phylogenetic systematics tiodon fasciatus) from eastern North America is a taxon, as is and taxonomy and then use this framework to examine its entire genus (Plestiodon), the group containing all skinks the transition from fi shlike aquatic vertebrates to the ear- (Scincidae), and several more inclusive, larger taxonomic liest terrestrial tetrapods (from the Greek tetra, “four,” + groups (Squamata, Reptilia, Tetrapoda, Vertebrata, etc.) to podos, “foot”) and the origins of modern amphibian and which it belongs. A monophyletic taxon, or clade, is made reptile groups. up of a common ancestor and all of its descendant taxa. Taxonomy is the science of categorizing, or classify- Phylogenies can be depicted in a variety of styles (Figure ing, Earth’s living organisms. A phylogeny is a hypothesis 2.1). A node is the point at which a common ancestor gives of the evolutionary relationships of these categories of rise to two sister lineages, or branches. The region of a organisms, usually presented in the form of a branching phylogeny between two nodes is called a stem. The stem is diagram. Phylogenies, sometimes called cladograms or an important concept because the term is often used when phylogenetic trees, are similar to human family trees in discussing extinct lineages. Depending on the type of anal- that they show the splitting of an ancestor and its de- ysis used to infer the phylogeny, the length of branches may scendants through time, but instead of several familial represent the amount of genetic change or be scaled with generations, these splitting events cover millions to hun- time and accompanied by a timescale. Such a timescale is dreds of millions of years. usually depicted in terms of the geological eras and periods The appearance in 1966 of an English translation of of Earth’s evolutionary history (Table 2.1; Figure 2.2). the work of the German biologist Willi Hennig was the A phylogeny is one of the most powerful tools in biology. start of a revolution in the way evolutionary relationships With knowledge of a group’s phylogeny, we can track the are analyzed. Hennig’s method, known as phylogenetic evolution of morphology, behavior, and ecology among the systematics or cladistics, emphasizes the importance of organisms in that group. For example, both the mantellid monophyletic groups and shared derived characters. The frogs of Madagascar and the dendrobatid frogs of Central many terms used in phylogenetic systematics can be con- and South America are small, leaf-litter dwelling anurans fusing, but the concept of monophyly (from the Greek that are brightly colored and have evolved the ability to mono, “one” or “single,” + phylon, “tribe”) is critical to secrete powerful defensive alkaloid toxins in their skin understanding any discussion of modern phylogeny and (see Chapter 15). Both groups sequester many of the same taxonomy. types of alkaloids (Clark et al. 2005), and both groups de-

Figure 2.1 Common formats and termi- (A) Taxon 1 nology for presenting a phylogeny (clado- Node gram). This simple phylogeny of four hypo- Clade Sister taxa thetical taxa is shown in three different styles. B Taxa 1 and 2 form a clade, as do Taxa 3 and Taxon 2 4 and all four taxa together. Not shown are A numerous stem lineages between nodes A and Taxon 3 B (and others between A and C). These lin- C eages may be extinct or simply were not sam- Clade Sister branches pled in the phylogenetic analysis. (A) Squared (lineages) Stem branch Taxon 4 horizontal presentation, read from left to right with terminal taxa on the right. This is the style used most frequently in this book. (B) Squared vertical presentation, with terminal (B) (C) taxa at the top. (C) Diagonal presentation. Taxon 1 Taxon 2 Taxon 3 Taxon 4 Taxon 1 Taxon 2 Taxon 3 Taxon 4

B C rive these alkaloids from their prey, usually B C ants. With no phylogenetic information, A we would assume that these two groups are more closely related to each other than A to other frog groups, and that the ability to sequester defensive alkaloids from ar- thropod prey evolved once in their common ancestor. However, phylogenetic analysis shows that atics, Reptilia without birds is paraphyletic (from the Greek mantellids and dendrobatids are only distantly related, and para, “beside” or “except”) because it contains only some, that both groups have close relatives that do not secrete de- not all, of the descendants of the common ancestor of the fensive alkaloids (Figure 2.3). Thus, sequestration of toxins traditional reptiles (Figure 2.4). evolved independently in mantellids and dendrobatids, a A similar concept is polyphyly (from the Greek poly, phenomenon known as convergent evolution. “many”), the situation in which a taxonomic group does not In phylogenetic systematics, only clades—monophyletic contain the most recent common ancestor of all the mem- taxa—are formally recognized and given names. Follow- bers of that group. For example, a hypothetical taxonomic ing this convention produces taxonomic groups that also group comprising the endothermal (“warm-blooded”) ver- represent evolutionary history. For example, precladistic tebrates—mammals and birds—would be polyphyletic be- taxonomy recognized birds and reptiles as separate taxa. cause it would not include the most recent common ances- However, modern phylogenetic analysis has shown that tor of each group, birds and mammals having arisen from birds share a common ancestor with all the other reptile different common ancestors (diapsids and synapsids; see taxa (crocodiles, lizards, snakes, tuatara, and turtles). In Section 2.5). Paraphyletic and polyphyletic groups are not other words, if we exclude birds from Reptilia, then Reptilia given formal taxonomic names but are sometimes named is not monophyletic; in the context of phylogenetic system- informally, in which case the taxonomic name is put in quo-

Paleozoic Mesozoic Cenozoic

Cambrian Ordovician Silurian Devonian CarboniferousPough 4ePermian Triassic Jurassic Cretaceous Tertiary Sinauer Associates 541 500 450 400 350 Morales300 Studio 250 200 150 100 50 Pough4e_02.01.ai 02-22-15 Million years ago (mya) Quaternary: Holocene Pleistocene

Pliocene Figure 2.2 The geological time scale. Paleocene Eocene Oligocene Miocene This graphic rendering of the time scale in Table 2.1 will be used with time-scaled 66 60 50 40 30 20 10 Present cladograms throughout this book. Million years ago (mya)

Pough 4e Sinauer Associates Morales Studio Pough4e_02.02.ai 03-10-15 2.1  Principles of Phylogenetics and Taxonomy 21

Other ranoid frogs Ranoidea Mantellidae (taxon origin ~65 mya) Rhacophoridae

Microhylidae

Common Other ranoid frogs ancestor Other hyloid frogs Mantella laevigata Lineages Dendrobatidae diverge Hyloidea (taxon origin ~65 mya) ~170 mya

Mesozoic Cenozoic

Jurassic Cretaceous Tertiary

200 150 100 50 Present Millions of years ago (mya) Dendrobates tinctorius

Figure 2.3 Phylogeny reveals convergent evolution. ability evolved a single time in their common ancestor. How- Both the Neotropical Dendrobatidae and the Madagascan ever, phylogeny reveals that these frogs belong to two distinct Mantellidae comprise small, brightly colored frogs that live evolutionary lineages—Hyloidea and Ranoidea—that sepa- in leaf litter on the tropical forest floor, as seen in these photos rated some 170 mya, and the defensive use of toxins evolved of typical species. Both dendrobatids and mantellids obtain independently in the two taxa. Solid triangles are shorthand alkaloid toxins from the insects they eat and sequester these for multiple taxa; the complete anuran phylogeny is shown toxins in their skin as a defense against predators. These in Figure 3.22. (Photographs: Mantella © All Canada Photos/ similarities could logically lead to the hypothesis that dendro- Alamy; Dendrobates © Dirk Ercken/Alamy.) batids and mantellids are sister taxa, and that sequestration

a tation marks (as “Reptilia” in Figure 2.4B). Many research- Table 2.1  The geological time scale ers do not make a distinction between para- and polyphy- Era Period Epoch letic and simply use the term non-monophyletic. Holocene ~11 kya Because only monophyletic groups are given formal tax- Quaternary 2.6 mya onomic names, many changes in the names of taxonomic Pleistocene 2.6 mya groups such as genera and species are the results of phy- Pliocene 5.3 mya logenetic analysis showing that an existing named taxon Cenozoic Miocene 23.0 mya is not monophyletic. As with all scientific hypotheses, the 66.0 mya relationships depicted by a phylogenetic tree are subject to Tertiary 66.0 mya Oligocene 33.9 mya falsification by new evidence or a better analysis of existing Eocene 56.0 mya evidence. Alternative hypotheses about evolutionary rela- Paleocene 66.0 mya tionships are common, as we will see in this and the next two chapters. Pough 4e Cretaceous 145 mya In some cases, groups that are clearly monophyletic SinauerMesozoic Associates Jurassic 201 mya can be defined by shared derived characters (see below), Morales252 mya Studio but it has not yet been possible to determine the sequence Pough4e_02.03.aiTriassic 05-05-15 252 mya in which the descendant lineages separated (e.g., neoba- Permian 299 mya trachian frogs or pleurodont lizards; see Figures 3.22 and Carboniferous 359 mya 4.12, respectively). When the branching sequence of three or more lineages cannot be determined, that situation is un- Devonian 419 mya Paleozoic resolved and is called a polytomy (from the Greek tom, a 541 mya Silurian 444 mya “cut” or “slice”). For example, iguanian lizards, anguimorph Ordovician 485 mya lizards, and snakes form a polytomy because the phylogenetic interrelationships of these major clades remain unclear Cambrian 541 mya (see Figure 4.12). a Dates are from Geological Society of America (2012) and represent the Before we discuss how phylogenies are constructed, starting times of the intervals shown. we wish to emphasize that the branching pattern of life is

(A) Reptilia An ancestral character is also called a plesiomorphy Crocodylia (from the Greek ples, “close to” + morph, “form”). A derived character is an apomorphy (from the Greek ap, “away Aves from”). In other words, an apomorphy is a structure that Testudines has moved away from the ancestral form. A derived character shared by two or more taxa is called a synapomorphy Rhynchocephalia (from the Greek syn, “together”), or shared derived char- Squamata acter. Synapomorphies are evidence that taxa share a common ancestor—that is, they form a clade. The amniotic egg Mammalia is a synapomorphy supporting the monophyly of Amniota. Additional examples of synapomorphies defining a clade (B) “Reptilia” include the presence of a shell in turtles and the absence Crocodylia of lungs that is characteristic of plethodontid salamanders. Sometimes, as we saw in Figure 2.3, the same derived Aves character evolves independently in different groups; that Testudines is, the character appears in two groups that do not share a recent common ancestor. Derived characters arising from Rhynchocephalia such convergent evolution are called homoplasies (from the Squamata Greek homo, “alike,” + plastos, “moulding”). For example, ectothermy—relying on the environment rather than internal Mammalia mechanisms to regulate body temperature—is the ancestral Figure 2.4 Definitions of Reptilia. (A) Modern phylogenetic condition for all tetrapods. Both mammals and birds are en- systematics includes Aves in a monophyletic Reptilia. (B) The dotherms, which is a derived state. However, endothermy antiquated paraphyletic definition of Reptilia excludes Aves. is a homoplastic trait in the context of tetrapod phylogeny because it evolved convergently (i.e., separately and independently) in birds and mammals—it is a derived character continuous whether a phylogeny includes extinct or extant in both groups, but it is not a shared derived character. taxa, and there are numerous lineages that are not shown in Although plesiomorphies do not provide any informa- a phylogeny simply because we do not have any fossil evi- tion about evolutionary relationships, this does not mean dence of those lineages. Thus, for every branch of a phylog- they are unimportant. On the contrary, ancestral characters eny, there are countless other branches for which we have can be profoundly important in how an animal lives. Ec- no information, so no phylogeny can completely capture the tothermy is plesiomorphic for amphibians and reptiles and true diversity of life over Earth’s enire history. has ramifications in many aspects of their ecology and behavior. Thus, it is essential to understand the mechanisms Building phylogenies and implications of ectothermy to understand the biology Deciphering the phylogenetic histories of taxa is a surpris- and ecology of salamanders and lizards, even though the ingly complex task. Profound advances in how we construct fact that both salamanders and lizards are ectotherms does phylogenies have been made since Hennig’s development not provide any information about the evolutionary rela- of cladistics. The use of DNA data and increasingly sophis- tionship of these two groups. ticated statistical methods of phylogenetic analysis (e.g., To further confuse matters, a given character may be maximum likelihood and related Bayesian methods) have seen as either a plesiomorphy or a synapomorphy, depend- been especially influential. In general, however, phyloge- ing on the taxonomic scale. For example, the shell is a sy- neticPough systematics 4e uses characters to identify clades and to napomorphy of turtles, evidence that turtles form a clade discoverSinauer Associates the order in which they branched over evolution- relative to all other reptiles. However, if one is interested Morales Studio aryPough4e_02.04.ai time. A character 05-05-15 is simply any heritable trait and can in the interrelationships of the different turtle lineages, the include morphology, behavior, physiology, DNA sequences, presence of a shell is not informative because all turtles and virtually anything else observable about organisms. A have the ancestral condition of a shell; in this case, the shell derived character is a character that differs in form from its is a plesiomorphy. ancestral character. For example, all amniotes (mammals The examples of characters given above are all aspects of and reptiles) possess a specialized amniotic egg, which is an organism’s physical phenotype and are called morpho- characterized by a tough shell and four structures called logical or phenotypic characters. Before scientists had the extraembryonic membranes (see Chapter 9). This type of ability to collect biochemical data such as DNA, morpho- egg is unique to amniotes, and because it evolved from an logical characters were the only data used for phylogenetic egg that lacks a shell and extraembryonic membranes (the construction. Morphological data—typically features of the ancestral state seen in fish and amphibians), the amniotic skeleton—are usually the only data available from fossils egg is a derived character. of extinct taxa. The collection of morphological data has

uncorrected page proofs © 2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 2.1  Principles of Phylogenetics and Taxonomy 23 been greatly aided by X-ray microtomography that allows ern taxonomy to use rank-free taxonomic names above the the scanning of three-dimensional images of skeletons and genus level. Thus, instead of referring to the Class Reptilia, even of fossils embedded in rock. we simply say Reptilia. Just as the morphology of organisms changes over time There are multiple reasons for adopting rank-free tax- and leaves signatures of evolutionary history, so too does onomy. The first is that Linnean ranks are not comparable DNA. The vast majority of phylogenetic analyses of extant with respect to either diversity or time. For example, the taxa today rely on differences in DNA characters among amphibian lineage Cryptobranchidae (giant salamanders) taxa. Mutations in DNA that substitute one nucleotide for is approximately 175 million years old and contains 3 extant another (e.g., adenine for guanine) occur in all lineages of species, but the lineage Bufonidae (true toads) is less than life. Modern phylogenetic analysis tries to determine the 50 million years old and contains almost 600 species. In this sequence in which these substitutions occurred over evolu- case, to rank both these lineages as families has no mean- tionary time, and therefore the sequence in which lineages ing in terms of biological diversity. Second, because we now split from other lineages.* have substantial amounts of phylogenetic information (in- The most obvious advantage to using DNA data for phy- cluding DNA sequences) for many organisms, especially logenetic reconstruction is the number of characters one vertebrates, taxonomists can make highly detailed taxono- can analyze. With the vast numbers of genes for which mies, to the point of naming every node on a phylogeny. DNA sequences are available, and the ever increasing num- Using the more inclusive Linnean ranks in this situation ber of organisms for which complete genomes have been quickly becomes cumbersome because of the proliferation sequenced, it is now easy to obtain thousands or hundreds of rank prefixes such as magnaorder, infraclass, superfam- of thousands of characters rather than the tens to hundreds ily, and so on. In other words, the meaningful part of a taxo- of characters used in phylogenetic analyses based on mor- nomic name is the name itself, not the Linnean rank. phological data. The use of DNA also allows a researcher This book uses a mostly rank-free taxonomy, although to study evolutionary questions that would be difficult to we do refer to families and subfamilies, primarily because answer with only morphological data. For example, DNA these terms have long been used for higher-level taxonomy sequence analysis allows one to study the phylogenetic his- and continue to be used extensively in scientific literature. tory of species that have few visible phenotypic differences As in all taxonomic literature, whether Linnean or rank- (known as cryptic species). Analysis of DNA can also de- free, we specify genus and species. termine whether two populations of a species have recently The proliferation of phylogenetic information has also or are currently exchanging genes, or if both populations changed how we define taxonomic groups, specifically the are reproductively isolated from each other, and thus may use of node-based and stem-based definitions of taxonomic be on the road to becoming distinct species. DNA data can names. A node-based definition names a group that in- rarely be collected from fossils, however, so studies incor- cludes the most recent common ancestor of at least two taxa porating extinct taxa must rely on morphological data col- (called specifiers) and all of its descendants. This type of lected from fossil specimens. group is also sometimes called a crown group. For example, the name Tetrapoda defines a taxonomic group that con- Rank-free taxonomy and phylogenetic tains the common ancestor of mammals, reptiles, lissam- nomenclature phibians, and the extinct Acanthostega, and all of its descen- Many students may recall having memorized the hierarchi- dants (Figure 2.5). This group contains all extant taxa, plus cal Linnean ranks (kingdom, phylum, class, order, family, genus, and species), but there is an increasing trend in mod- Reptiles * The details of how phylogenies based on DNA data are constructed are fascinating but beyond the scope of this brief overview. Specialized cover- age can be found in a number of sources, including Felsenstein 2003, Hall Mammals 2011, and Baum and Smith 2013.

Amphibians

Figure 2.5 Node-based versus stem-based Node age ~400 mya taxonomic names. The node-based name Ichthyostega Tetrapoda (red) is a crown group defined by the Stem, including Tetrapoda node that represents the common ancestor of all extinct lineages; Acanthostega and all extinct and extant tetrapods stem age ~420 mya Acanthostega (the amphibians, mammals, and reptiles). The Tetrapodomorpha stem-based name Tetrapodomorpha (blue) includes Eusthenopteron the crown group (i.e., Tetrapoda) and all taxa— including extinct lineages—that are more closely related to Tetrapoda than to lungfish. Lung sh

Pough 4e Sinauer Associates Morales Studio Pough4e_02.05.ai 02-22-15 24 Chapter 2  Phylogenetic Systematics and the Origins of Amphibians and Reptiles any extinct relatives of extant lineages (e.g., fossil reptiles A large measure of subjectivity remains in the species and mammals). It does not include any stem lineages (see description process, and can be summed up by the ques- below) that diverged before the split between Acanthostega tion “How much difference is enough to call the organism and other tetrapods. a new species?” The answer is left up to the researchers The alternative to a node-based definition is a stem- and can depend on which of several definitions of species, based definition. In phylogenetic terms, stem lineages or species concepts, they use (see Coyne and Orr 2004). are those that diverge before the crown group. Stem-based It is useful to think of a species as a testable hypothesis definitions also use specifier taxa, but instead of identi- subject to falsification by further data rather than as an fying a specific node in the tree, a stem-based definition immutable form. Species are sometimes no longer recog- defines a group more closely related to at least one taxon nized when additional data, especially DNA data, reveal than another. For example, Tetrapodomorpha is a stem- that a recognized species is not consistently different from based name defining all organisms more closely related to other species. extant tetrapods (Tetrapoda) than to lungfish (see Figure Some lineages do not fit comfortably into binomial tax- 2.4). It includes Tetrapoda and all lineages that arose on onomy. For example, some Ambystoma salamanders, as this branch of the phylogeny after it split with the ancestor well as several genera of lizards, are composed entirely of of extant lungfish. In other words, a stem-based definition females that reproduce clonally (i.e., as matrilineages). In includes the crown group and lineages that diverged before practice, they are named as species (e.g., Aspidoscelis neo- the crown group. mexicana, a tetraploid hybrid between two species of whip- There is a third type of taxonomic definition, called an tail lizard; see Figure 9.5), but they do not fit the biological apomorphy-based definition, that includes members of a species definition of a group of actually or potentially in- group that all share a specific apomorphy. However, this terbreeding organisms. Each individual reproduces parthe- definition is rarely used. nogenetically, and there is no exchange of genetic material among the members of this unisexual species. Discovering and describing new species A fundamental goal of taxonomy is discovering and de- Molecular data and species identification scribing new species, and this continues to be an active Since the advent of DNA sequencing in the late 20th cen- field of herpetology. For example, approximately 1,800 tury, DNA data have profoundly changed how we identify species of amphibians were described between 2004 and new species. Researchers can compare DNA sequences to 2013 (see amphibiaweb.org), representing about 25% of all determine whether an organism is similar to an existing named, extant species. Much of this biodiversity has been named species. This can be a complex process, and a thor- discovered in tropical forests, especially in South America, ough discussion is beyond the scope of this chapter (see equatorial Africa, Southeast Asia, and Madagascar (see Fujita et al. 2012; Leaché et al. 2014), but researchers typi- Chapter 5). cally use a phylogenetic analysis of the DNA to determine Both historically and today, the species discovery process if individuals from a putative new species are part of clades often begins when a researcher finds a group of organisms formed by other known species. in the wild that differs in some way from existing species. For example, a researcher may discover one or more Most often these are morphological differences; in reptiles populations of lizards with a unique brown body coloration they can be such characters as color or scale patterns. For that differs from the green body coloration seen in another, frogs, advertisement calls are important because they are physically similar and presumably closely related, species. strong predictors of reproductive isolation (see Chapter 13). If a phylogenetic analysis of DNA shows that the brown The researcher then compares the potential new species to lizards are a lineage derived within the clade of already other presumably closely related species to assess whether described green species, the researcher may conclude that there are enough consistent, distinctive differences to war- the brown animals are not a new species but represent a rant recognizing a new species. If so, the species is officially color polymorphism of the existing green species (Figure described using a strict set of rules governed by the Interna- 2.6A). However, if the phylogenetic analysis of DNA shows tional Code of Zoological Nomenclature (ICZN). A single that the brown and green populations are genetically dis- specimen is designated as the holotype, and it serves as tinct and form reciprocal monophyletic groups, then the re- the individual that possesses all the characters of that spe- searcher may describe the brown morphs as a new species cies. The holotype, and any other individuals collected with (Figure 2.6B). it, must be deposited in a museum that other researchers DNA data may also show large genetic differences be- can access in the future. The species must be described in tween populations of an already described species, but a scientific journal in an article that defines the holotype there may be no diagnosable morphological characters that and that provides a unique binomial species name (typically distinguish them. Are these morphologically indistinguish- Greek or Latin), the meaning of the name, a morphological able animals multiple cryptic species rather than a single description of the new species, and an explanation of how species? A growing consensus holds that DNA data alone this new species differs from other species. can be used to delimit species because genetic divergence

Figure 2.6 Discovering (A) (B) new species using phylogenetic data. (A) The newly discovered populations of brown lizards are Species 1 derived from within the green species phylogeny and could be interpreted as Species 1 simply color variants of the green species. (B) The brown and green lizards form reciprocal monophyletic groups and are good candidates to Species 2 be described as two species.

is evidence of the reproductive isolation of populations. In The numerous taxonomic names are the most frustrating other words, although we humans may not be able to tell aspect of discussing both extinct and extant diversity. We two species apart, each species recognizes individuals of its have limited our discussion to those groups that are criti- own species as distinct from those of other species. cal to understanding amphibian and reptile diversity (Table 2.2). It is useful to visualize these groups on the phylogenetic tree to understand how they are related (Figure 2.7). 2.2  Evolutionary Origins and Processes of Amphibian and The ecological transition from water to land Reptile Diversity Before discussing the origins of terrestrial tetrapods, it is necessary to understand the many challenges of transi- In this section we discuss the origins of terrestriality from tioning from an aquatic to terrestrial mode of life and how aquatic ancestors and the subsequent diversification of morphological and physiological adaptations to land were amphibian and reptile groups, many of which are extinct shaped by natural selection. A major difference between and have left no descendants living today. Throughout this living in water and on land is the effect of gravity on the discussion, you may find it useful to refer to Figure 2.2 and skeletal system. Changes in the body forms and propor- Table 2.1, which describe the geological time periods we tions of early tetrapods are coincident with changes in the frequently refer to. It is also important to understand that, skeleton and reflect increasing support for life on land. for every group of animals that we discuss here and in Fish have a comparatively weaker skeleton than tetra- Chapters 3 and 4, there are countless extinct stem lineages pods because a fish’s buoyancy counteracts the down- that we do not discuss. ward force of gravity and there is little selective pressure As we noted in Chapter 1, inclusion of organisms as dif- to evolve robust skeletons, even in large fish. In contrast, ferent as frogs and crocodiles in the discipline of herpetol- terrestrial animals must support their entire mass against ogy is partly historical accident and partly recognition that the force of gravity, and thus the most obvious adaptations the shared ancestral character of ectothermy creates impor- to living on land are seen in the skeleton and associated tant functional similarities among the groups. Although we musculature, especially in the vertebrae, limbs, and pec- discuss taxonomic groups separately, remember that many toral and pelvic girdles—the bony structures that support of these extinct groups, or ancestors of extinct groups, were the forelimbs and hindlimbs (see Figure 2.8). Terrestrial contemporaneous and formed ecological communities that animals have robust, interlocking vertebrae that can bear were functionally equivalent to those we see now. If you the weight of the entire axial skeleton, organs, and muscles wade through a swamp today, youPough will 4e see a variety of am- of the trunk. These limb girdles must be large enough to phibians and reptiles, includingSinauer some Associates that are fully aquatic support the body mass and configured to allow the limbs or terrestrial; small, gracile insectivores;Morales Studio and large, plodding to move. Finally, one or both sets of limbs must have the Pough4e_02.06.ai 03-12-15 herbivores. You might hear amphibians calling and watch strength to move the animal. lizards aggressively defending their territory. If you could The evolution of terrestrial feeding modes need not have made the same walk in a Late Carboniferous forest, have involved radical reorganization of the ancestral feed- you would have experienced the same phenomena, but you ing apparatus, but only the addition of components associ- would have been watching the earliest relatives of modern ated with terrestriality. Some modern tetrapods (e.g., some amphibians and reptiles, along with organisms from lin- salamanders) migrate annually between a terrestrial and an eages that subsequently became extinct and have no direct aquatic medium, using the tongue to acquire food on land descendants today. and suction feeding in water. Experiments show that the

Table 2.2  Major extant taxonomic groups in the evolution of amphibians and reptiles

Sarcopterygii: Bony fish with fins or limbs supported internally by bones and intrinsic musculature. Sarcopyterygii arose in the Late Silurian and includes Actinistia, Dipnoi, and Tetrapoda.

Actinistia: A diverse group of fish extending back to the Paleozoic, now represented by only two species of coelacanths (genus Latimeria). Dipnoi: Three genera of extant lungfish in Africa, South America, and Australia, as well as diverse fossil species extending well back to the Paleozoic. Tetrapoda: Vertebrates with four limbs. Includes Lissamphibia, Amniota, and the extinct Acanthostega and all of its descendants.

Lissamphibia: Anura (frogs), Caudata (salamanders), and Gymnophiona (caecilians). We use Lissamphibia for the clade name and informally refer to them by the more common term amphibians. Amniota: Vertebrates with (ancestrally) a shelled egg and four extraembryonic membranes.

Synapsida: Mammalia (mammals) and extinct non-mammalian fossil species Diapsida: Includes all extant Reptilia as well as several extinct lineages.

Archosauria: Testudinesa (turtles), Crocodylia (alligators, crocodiles, and gharials), and Avesb (birds). Lepidosauria: Squamata (lizards and snakes) and Rhynchocephalia (tuatara). a The inclusion of Testudines in Archosauria is debated (see Section 2.7). b Aves is included because this clade is nested deep within the archosaur branch of Reptilia. Among extant amniotes, birds are the closest relatives of crocodylians. Neither birds nor mammals are subjects of this textbook.

mechanics of this transition in feeding mode are quite sim- terrestrial hearing, including a stapes associated with a ple. Terrestrial adult salamanders retain the basic structural tympanum, seems to have occurred later in land vertebrate and functional components of their larval feeding system evolution than in Acanthostega and Ichthyostega, two early and simply add components (such as a tongue) for feed- aquatic tetrapods. By the time temnospondyls appeared ing on land (Lauder and Reilly 1994). Both feeding modes some 30 million years later (see Figure 2.7), the structure are possible for adult salamanders that passed through an of the hearing apparatus approached that of extant sala- aquatic larval stage. manders (Christensen et al. 2015). Preventing desiccation is critically important in the dry- It is important to note that these suites of morphological ness of the terrestrial environment. While this challenge and physiological adaptations did not have to evolve at the can be met by staying close to water (as many modern am- same time. The earliest tetrapods would have made very phibians do), other adaptations are necessary for an animal brief forays out of water, and thus any of the above adapta- to remain terrestrial for extended periods of time. This has tions would have conferred a small selective advantage. Ac- been achieved by the evolution of wax-producing glands in cumulation of small changes over millions of years would the skin of amphibians and increased keratinization and have ultimately allowed tetrapods to occupy terrestrial lipids in the skin of amniotes. environments. Gills are not suitable for terrestrial life because the gill filaments collapse onto each other when they are not sup- The transition from fish to tetrapods ported by water, drastically reducing the surface area avail- Morphological, paleontological, and molecular phylogenetic able for gas exchange. Terrestrial gas exchange occurs via studies show that tetrapods arose from sarcopterygian fish the skin, buccopharynx, and lungs. We know from examin- ancestors. Sarcopterygian (from the Greek sarc, “fleshy,” + ing modern lungfish that it is possible to possess both func- pterys, “fin” or “wing”) fish, including modern lungfish and tional gills and lungs, and lungs are an ancestral character of tetrapods. Many other functional and anatomical changes re- Figure 2.7 Phylogeny of Tetrapodomorpha. This phylo-  quired for the evolution of terrestriality have left no evi- geny includes the lineages discussed in the chapter text; count- dence in the fossil record. Sensory systems, in particular less extinct stem lineages are not depicted. Node ages are esti- the eyes and ears, would have changed to accommodate mates derived from Ruta and Coates 2007, Anderson et al. 2008, differences in the transmission of sensory signals through Shedlock and Edwards 2009, Sigurdsen and Bolt 2009, Jones et air and water (e.g., Fritzsch et al. 2013). The evolution of al. 2013, and Benton 2014.

Squamata (lizards and Lepidosauria snakes)

Rhynchocephalia (tuatara) Lepidosauromorpha Plesiosauria

Ichthyosauria

Saurischia Aves (birds)

Dinosauria Diapsida Other saurischians Avemetatarsalia Ornithschia Archosauria Pterosauria Reptilia Crocodylia

Other crurotarsians Crurotarsi Amniota Testudines Archosauromorpha (turtles) Non-diapsid reptiles

Synapsida Mammalia (mammals) Non-mammalian synapsids Lepospondyli Batrachia Lissamphibia Caudata (salamanders) Anura (frogs)

Gymnophiona (caecilians) Dissophoroidea

Tetrapoda Other temnospondyls Temnospondyli

Ichthyostega

Acanthostega

Tetrapodomorpha Tiktaalik

Panderichthyes Sarcopterygii Eusthenopteron

Dipnoi (lung sh)

Actinistia (coelocanths)

Paleozoic Mesozoic Cenozoic Quaternary Silurian Devonian Carboniferous Permian Triassic Jurassic Cretaceous Tertiary

400 350 300 250 200 150 100 50 Present Million years ago (mya) Pough 4e Sinauer Associates Morales Studio Pough4e_02.07.ai 05-05-15 uncorrected page proofs © 2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 28 Chapter 2  Phylogenetic Systematics and the Origins of Amphibians and Reptiles coelacanths, have fins that articulate with the limb girdles over, the middle-ear architecture of Panderichthys shows via a single bone. In tetrapods this same bone develops into modifications that may represent the early transition to a the humerus of the arm and the femur of the leg. In evolu- tetrapod-like middle ear (Brazeau and Ahlberg 2006). tionary terms, we call these structures homologous because The elpistostegalid Tiktaalik (Figure 2.8C) has been pro- they are both derived from the same fundamental struc- foundly important to interpreting the transition from water ture. Although tetrapods, lungfish, and coelacanths share to land in early tetrapodomorphs (Daeschler et al. 2006). Al- a common ancestor, neither of the latter two fish groups though distinctly a fish that inhabited shallow water bodies, resembles the earliest ancestors of tetrapods because both Tiktaalik possessed a suite of morphological characters that have undergone more than 400 million years of independent represents a transitional stage between aquatic and terres- evolution and developed their own unique traits. Thus, fossil trial modes of living. Tiktaalik lacks the bony sheath (opercu- data provide the strongest clues to the origin of tetrapods lum) that covers the gills in other fish. This change is func- and the ecological context in which they evolved. tionally important because loss of the operculum eliminates Before continuing, recall the distinction between stem- the rigid connection between the body and head, creating and node-based taxonomic names (see Section 2.1). The a flexible neck. Thus, Tiktaalik could probably raise its head stem-based clade Tetrapodomorpha includes all taxa that out of the water and turn it from side to side. Perhaps more are more closely related to modern amphibians, reptiles, important, the pectoral and pelvic girdles were stronger than and mammals than to lungfish (see Figure 2.5). This clade those of other tetrapodomorph fish, thus allowing Tiktaalik to includes modern tetrapods and their more fishlike fossil prop itself up on its fins, use them for aquatic propulsion, and ancestors. The definition of Tetrapoda has changed over maybe even make brief terrestrial forays along the water’s the years (see Laurin 2002; Laurin and Anderson 2004) edge (Shubin et al. 2006, 2014). but is now most commonly used as a node-based name for the clade containing the ancestor of Acanthostega and Early tetrapods all descendants of this common ancestor: modern-day am- Even casual observation reveals that the skeletons of Acan- phibians, reptiles, and mammals, including extinct lineages thostega (Figure 2.8D) and Ichthyostega (Figure 2.8E), ani- such as Ichthyostega. mals that lived during the Late Devonian (~365 mya), were Interest in tetrapod origins has generated a rich litera- far more like our own terrestrially adapted skeletons than ture with the identification of numerous extinct lineages the skeletons of fish. They had well-developed pectoral and and hypotheses of their phylogenetic relationships. Below pelvic girdles and distinct neck regions that allowed move- we discuss only a selection of fossil taxa most relevant to ment of the head independent of the trunk. They also pos- the origin and evolution of tetrapods (see Schoch 2014 for sessed limbs with bony digits—seven on the hindlimb of a comprehensive review). Ichthyostega (the forelimb of Ichthyostega is unknown) and eight on both the forelimb and hindlimb of Acanthostega Early tetrapodomorphs (Coates and Clack 1990). Ichthyostega had additional skeletal Tristopterid and elpistostegalid fish are the most important modifications that suggest partially terrestrial habits (Pierce extinct lineages for understanding the evolution of early et al. 2013). For example, the pectoral and pelvic girdles of tetrapodomorphs. Eusthenopteron, a tristopterid, was a large Ichthyostega were far more robust than those of Acanthostega (up to 1.8 m) predatory fish that inhabited shallow marine (Coates 1996), the elbow was bendable (Pierce et al. 2012), or estuarine waters in the Late Devonian (385–380 million the vertebral column was reinforced by strong connections years ago). Eusthenopteron is notable because its teeth have between vertebrae (zygopophyses), and the ribs were ex- extensive folding of enamel (labyrinthodont dentition) like panded and overlapping, thereby forming a distinct rib cage. those of other early tetrapods. More important, its pectoral All of these features suggest that Ichthyostega could drag and pelvic fins contain bones homologous to the radius, itself out of the water with its forelimbs (the hindlimbs were ulna, tibia, and fibula of modern tetrapods (Figure 2.8A). smaller and more paddlelike) and support its weight in ter- Eusthenopteron was probably fully aquatic (Clack 2002; Lau- restrial environments, although it not possible to know how rin et al. 2007). long it could remain out of the water. Like lungfish today, The Late Devonian (~385 mya) elpistostegalid fish these genera probably had lungs, but they also retained Panderichthys (Figure 2.8B) was contemporaneous with fishlike internal gills and were primarily aquatic (Coates Eusthenopteron and displayed more tetrapod-like features and Clack 1991; Clack et al. 2003). (Boisvert 2005; Boisvert et al. 2008). Its body was dorso- In summary, a 20-million-year time span in the Late laterally flattened and lacked dorsal and anal fins, and the Devonian saw a dramatic transition from fully aquatic fish tail fin was greatly reduced. Its pectoral girdle was more to animals with structures found in all tetrapods today. Al- robust than that of Eusthenopteron, and Panderichthys may though these features initially evolved in response to selec- have walked on the bottom of shallow water bodies. Its eyes tive pressures specific to inhabiting shallow water bodies, were located dorsally on a rather crocodile-like skull, and they provided the basic building blocks that eventually al- Panderichthys may have foraged at the water surface. More- lowed tetrapods to invade and diversify on land.

(A) Eusthenopteron 2.3  Three Hypotheses for the Origin of Extant Amphibians

Extant amphibians (caecilians, frogs, and salamanders) form a clade named Lissamphibia (see the diphyly hypothesis below for a different interpretation). The origin of Lissamphibia has been debated for decades and continues to produce copious literature. The debate centers around whether caecilians, frogs, and salamanders are derived from one or both of two early tetrapod lineages, temnospondyls and lepospondyls (Figure 2.9). As with tetrapod (B) Panderichthyes origins, we do not discuss the many other stem amphibian lineages (see Schoch 2014 for an extensive review). The temnospondyl hypothesis The most widely accepted hypothesis for the origin of extant amphibians is that they form a clade (Lissamphibia; see Section 2.4) and are derived from temnospondyl ancestors (Milner 1988, 1993), specifically the Dissorophoidea (C) Tiktaalik (see Figure 2.9A) (e.g., Ruta and Coates 2007; Sigurdsen and Bolt 2009, 2010; Sigurdsen and Green 2011). Temnospondyls (from the Greek temn, “cut,” + spondyl, “vertebra”) are so named because the centrum (body) of their vertebrae consists of two distinct regions that sur- round the notochord (Figure 2.10A). The intercentrum is a (D) Acanthostega wedge-shaped ventral structure, and the pleurocentra are two wedge-shaped dorsal structures. Temnospondyls are represented by almost 200 genera from the Early Carboniferous to the Middle Cretaceous (~330–130 mya). They ranged in length from a few centi- meters to a few meters. Many species were crocodile-like, with large, flat skulls and dorsally positioned eyes. Mast- odonsaurus, which grew to 6 m and had two massive fangs on the mandible, is an extreme example of this phenotype (Figure 2.11A). The teeth of temnospondyls are labyrinthodont, a condition seen in other tetrapodomorphs (e.g., Eusthenopteron). Temnospondyls inhabited both freshwater and marine habitats. (See Ruta et al. 2007 and Schoch 2013 (E) Ichthyostega for information about the phylogenetics of Temnospondyli.) Numerous characters support a temnospondyl origin of Lissamphibia. Both groups have, among other characters, pedicellate teeth (see Section 2.4), wide openings in the Fibula palate that permit retraction of the eye into the skull, two occipital condyles on the skull that articulate with the first Humerus cervical vertebra (the atlas), and short ribs. Femur Radius Tibia Ulna The lepospondyl hypothesis Some phylogenetic studies support the origin of a mono- Figure 2.8 Reconstructed skeletons and limbs of extinct phyletic Lissamphibia within lepospondyls, usually within tetrapodomorphs and tetrapods. The reconstructed dorsal a paraphyletic assemblage of small, lizardlike animals called view of the forelimb of each species is shown, except for Ichthyo- “microsaurs” (see Marjanovicˇ and Laurin 2009, 2014). Unlike stega (E), whose hindlimb is shown (the forelimb is unknown the divided three-part vertebrae of temnospondyls, the verte- for this genus). Homologous bones are color-coded. (A,D after brae of lepospondyls consist only of a centrum (derived from Coates et al. 2008; B after Boisvert 2005; C after Coates et al. the pleurocentrum) fused with the neural arch into a single 2008, Shubin et al. 2014; E after Coates and Clack 1990.) unit (Figure 2.10B). Lepospondyls comprise about 60 genera

Pough 4e Sinauer Associatesuncorrected page proofs © 2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, Morales Studio manufactured or disseminated in any form without express written permission from the publisher. Pough4e_02.08.ai 02-22-15 30 Chapter 2  Phylogenetic Systematics and the Origins of Amphibians and Reptiles

(A) Frogs (A) Temnospondyl (B) Lepospondyl Lissamphibia Salamanders Anterior Posterior Anterior Posterior Caecilians Neural arch Dissorophoidea Temnospondyli Nerve cord Pleurocentrum Amphibia Other temnospondyls Notochord

Intercentrum Centrum Lepospondyli Figure 2.10 Amniota Vertebrae distinguish temnospondyls and lepospondyls. (A) The vertebrae of temnospondyls consist of a wedge-shaped ventral structure, the intercentrum, and two (B) Temnospondyli dorsal pleurocentra (the second pleurocentrum is behind the Lissamphibia Frogs notochord in this view). (B) In lepospondyls, the intercentrum, pleurocentra, and neural arch are fused into a single structure. Amphibia Salamanders

Caecilians from the Early Carboniferous to the Early Permian (~340–275 “Microsauria” mya). Aïstopods and lysorophids were nearly or entirely limbless, nectrideans were aquatic with strongly compressed tails, and “microsaurs” had a variety of body forms. In con- Other lepospondyls trast to many temnospondyls, lepospondyls were small animals with skulls typically no longer than 5 cm (Figure 2.11B). Lepospondyli However, one of them—Diplocaulus—is famous for its large Amniota (~35 cm) boomerang-shaped head and large body (up to 1.5 m). Probably a flap of skin extended from the head to the sides of the body. This unusual structure maySeveral have been references a that I found (Carroll and (C) Frogs hydrofoil to aid swimming, or a way to increaseother the sources) surface show this in various ways. I will attach these to an email. Salamanders area for cutaneous gas exchange (Cruickshank and Skews 1980), although these and other hypotheses, such as sexual Dissorophoidea I’m thinking that we might want to show Temnospondyli selection, are not mutually exclusive. (See Andersonthis in 2001 a fairly for generic way, not showing a information on the phylogenetics of Lepospondyli.)particular animal? Both lissamphibians and lepospondyls lack numerous Other temnospondyls bones of the skull, including the ectopterygoid and post- Amphibia orbital bones, as well as the cleithrum from the pectoral Pough 4e Caecilians Sinauergirdle. Associates These losses may be interpreted as synapomorphies Moralesthat support Studio inclusion of both groups in a clade. A study “Microsauria” Pough4e_02.10.aithat included morphological 03-12-15 data for both extinct and extant taxa and molecular data for extant taxa also supports the lepospondyl hypothesis (Vallin and Laurin 2004; Pyron Other lepospondyls 2011). However, it is worth noting that only Vallin and Lau- rin’s (2004) data support the lepospondyl hypothesis, and it Lepospondyli is unclear whether Pyron’s (2011) results would differ if al- Amniota ternate data sets that support the temnospondyl hypothesis were used. Moreover, loss of skull bones is often correlated Figure 2.9 Three hypotheses for the origins of modern amphibians. (A) The temnospondyl hypothesis followed with the evolution of miniaturization, a common phenom- in this book postulates that modern amphibians—salaman- enon in numerous groups of amphibians (see Section 2.4). ders, frogs, and caecilians—form the monophyletic clade Lis- The diphyly hypothesis samphibia and are derived from temnospondyl amphibian ancestors, most likely the Dissorophoidea. (B) The lepospondyl The diphyly (from the Greek di, “two”) hypothesis of lis- hypothesis states that Lissamphibia is derived from lepospondyl samphibian origin is a hybrid between the temnospondyl amphibian ancestors, most likely “microsaurs.” (C) The diphyly and lepospondyl hypotheses and proposes that Lissam- hypothesis states that Lissamphibia is not monophyletic and phibia is not monophyletic (Carroll 2007, 2009; Anderson Pough 4e Sinauerthat frogs Associates and salamanders are derived from temnospondyls 2008). It proposes that frogs and salamanders are derived Moraleswhereas Studio caecilians are derived from lepospondyls. from dissorophoid temnospondyls and that caecilians are Pough4e_02.09.ai 02-22-15 uncorrected page proofs © 2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 2.3  Three Hypotheses for the Origin of Extant Amphibians 31

(A) Temnospondyls (B) Lepospondyls

Mastodonsaurus, 6 m

Diplocaulus, 1.2 m 2 m (6’5”)

Cacops, 45 cm

Microbrachis, 14 cm

Figure 2.11 Temnospondyls and lepospondyls of the Late brachis may have appeared similar to some modern salaman- Paleozoic. (A) Two representative temnospondyls. Mastodon- ders. The graph, keyed to the colored bars beneath the skel- saurus was huge and superficially resembled a crocodylian. The etons, shows the relative sizes of the animals compared with a much smaller Cacops was a more typical size temnospondyl. (B) very tall adult human. (After Bolt 1977; Schloch 1999.) Two lepospondyls. The unique head shape of Diplocaulus may have helped the animal glide through the water. The tiny Micro- derived from lepospondyl “microsaurs” (see Figure 2.9C). Carboniferous stem tetrapods, and early lissamphibians An important fossil supporting the diphyly hypothesis is from the Permian–Jurassic boundary is extremely poor. that of the caecilian Eocaecilia. Some studies have sug- As a result, relationships at these regions of the phylogeny gested that Eocaecilia, and therefore modern caecilians, are may be ambiguous or highly variable across studies simply derived from lepospondyl ancestors (e.g., Carroll 2007; An- due to lack of data. derson et al. 2008). However, a recent X-ray microtomogra- There is discrepancy between molecular and paleonto- phy analysis of the skull of Eocaecilia (see Figure 3.65) has logical age estimates of Lissamphibia. Molecular divergence revealed additional characters that reject the diphyly hy- age estimates generally support a Late Carboniferous age pothesis and instead support a monophyletic Lissamphibia of Lissamphibia (~315–300 mya) (San Mauro 2010; Pyron derived from temnospondyls, a hypothesis also supported 2011). However, divergence ages based on fossil data sug- by inner ear structure and other phylogenetic analyses gest a much younger age, in the Late Permian (~260–255 (e.g., Sigurdsen and Green 2011; Maddin and Anderson mya) (Marjanovicˇ and Laurin 2014). However, there is a 2012; Maddin et al. 2012). Thus, the diphyly hypothesis is frustrating 30-million-year gap (called Romer’s Gap) be- not widely accepted. tween the appearance of Acanthostega, Ichthyostega, and Tik- These alternative hypotheses do not affect our concept taalik in the Late Devonian and the explosion of tetrapod of relationships among extant tetrapods; they apply only diversity in the Early Carboniferous. This period is critical to interrelationships among extant and fossil taxa. None- for understanding early amphibian and amniote evolution, theless, these alternative phylogenetic hypotheses bear for it is when several tetrapod groups—including temno- critically on the interpretation of evolutionary processes spondyls, lepospondyls, and the earliest amniotes—appear involved in the evolution of lissamphibians (Bolt 1977, in the fossil record. 1979; Laurin 1998). The wildly varying quality of fossil preservation is another factor that accounts for different results from phyloge- Why do different analyses support different netic studies of fossil taxa. While there are some exception- hypotheses of lissamphibian origins? ally well preserved fossils with fully articulated skeletons, Perhaps the most important cause of the lissamphibian fossil specimens are usually incomplete, or the skeleton is originsPough 4e debate is also a frustrating aspect of almost all crushed and in multiple pieces. Therefore, not all relevant phylogeneticSinauer Associates analyses of paleontological data—the in- morphological characters may be identified in every speci- Morales Studio completePough4e_02.11.ai fossil record. 05-05-15 The fossil record of early caecilians, men, and researchers may disagree in their identification

uncorrected page proofs © 2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 32 Chapter 2  Phylogenetic Systematics and the Origins of Amphibians and Reptiles of certain characters that affect phylogenetic reconstruc- 1. The teeth are pedicellate and bicuspid (Figure 2.12A). tion (e.g., McGowan 2002; Marjanovicˇ and Laurin 2008). In Each tooth crown sits on a base (pedicel), from addition, researchers must determine whether a fossil has which the crown is separated by a fibrous connec- enough identifiable characters to be included in an analysis, tion. Moreover, the teeth have two cusps, one on the and the choice of specimens, taxa, and characters strongly lingual (inner) side of the jaw and one on the labial influences phylogenetic results. As with the origins of tet- (outer) side. Such a tooth structure is unique to Lis- rapods, a better resolution of the origin of Lissamphibia samphibia and some temnospondyls. awaits more fossil discoveries. 2. The sound-conducting apparatus of the middle ear consists of two elements: the stapes (columella), which is the usual element in tetrapods, and the 2.4  Relationships among Extant operculum. The operculum (not homologous to the Lissamphibian Lineages operculum in fish) consists of a bony or cartilaginous structure that attaches to the ear capsule and is con- Given the controversy concerning the relationships be- nected to the suprascapula via the opercular muscle tween lissamphibians and Paleozoic amphibians, it should (Figure 2.12B). Functionally, this allows ground not be surprising that relationships among frogs, salaman- vibrations to be transmitted from the forelimb to ders, and caecilians have also been debated extensively. the inner ear. Inside the inner ear are two sensory Although most morphological studies support the sister epithelial patches (not shown), the papilla basilaris, relationships between frogs and salamanders (Batrachia), found in other tetrapods, and the papilla amphibio- researchers have also found putative derived morphological rum, unique to lissamphibians. The papilla basilaris characters that support salamander + caecilian or frog + receives relatively high-frequency sound input via caecilian clades (Trueb and Cloutier 1991; Jenkins and the stapes. The papilla amphibiorum receives rela- Walsh 1993; McGowan and Evans 1995; Laurin 1998a). tively low-frequency input via the opercular appa- Because of the highly derived morphology of the three liss- ratus. The opercular apparatus is lost in caecilians, amphibian groups, it is often difficult to apply morphologi- perhaps as a result of limb loss, and is reduced in cal characters across all three groups. salamanders by the loss of one or more components However, three or more decades of molecular phylo- in various groups. genetic analyses have converged on a phylogeny of Liss- 3. The stapes is directed dorsolaterally from the fenestra amphibia that supports the sister relationship between ovalis, a character shared by some of the lissamphib- frogs and salamanders (Batrachia) that together are sister ians’ presumed Paleozoic relatives. to caecilians. The presence of an opercular apparatus is a synapomorphy for Batrachia (see Figure 2.12B). True der- 4. The fat bodies develop from the germinal ridge mal scales are absent in frogs and salamanders (whereas (which also gives rise to the gonads), a developmen- they are present in caecilians and in Paleozoic tetrapods), tal origin unique among tetrapods. and ectopterygoid and postfrontal bones are absent from 5. The skin contains both mucus and poison (granular) their skulls (see Figure 2.13). Finally, two developmental glands that are broadly similar in structure. characters—absence of segmentation of the sclerotome and 6. Specialized receptor cells in the retina of the eye, reduction or loss of male Müllerian ducts—are shared by called green rods, are present in frogs and salaman- frogs and salamanders but not caecilians. ders. Caecilians apparently lack green rods, perhaps For the purposes of further discussion, we follow most because of their highly reduced eyes. phylogenetic studies and assume that Lissamphibia (caeci- 7. A sheet of muscle, the levator bulbi muscle, lies lians, frogs, and salamanders) is monophyletic and derived under the eye and permits lissamphibians to elevate from temnospondyl ancestors (see Figure 2.9A). The earliest the eye. fossil that can clearly be assigned to an extant lissamphibian clade is Triadobatrachus from the Early Triassic (~245 mya; 8. All extant amphibians employ cutaneous and buc- see Figure 3.21). Triadobatrachus was thus an early ancestor copharyngeal respiration. of frogs (although it is unclear whether Triadobatrachus had 9. The ribs are short, straight, and do not encircle the the ability to jump; Sigurdsen et al. 2012), and therefore the body. The ribs of Paleozoic stem tetrapods (other earliest ancestors of Lissamphibia must be older than 245 than some temnospondyls) are long, robust, and million years. encircle the viscera. Monophyly of Lissamphibia 10. Two occipital condyles at the base of the skull articulate with two cotyles on the first cervical vertebra Numerous morphological synapomorphies support lissam- (the atlas). Most other extant tetrapods have a single phibian monophyly (Schoch 2014). The following characters occipital condyle, but two condyles are found in are some of the derived features that are shared by, and in some temnospondyls. many cases are unique to, extant amphibians:

(A) Lingual cusp 12. Lissamphibians share similar reductions in skull Labial cusp Crown bones and fenestration patterns compared with Paleozoic tetrapods (Figure 2.13). These shared Outer margin of jaw derived characters include loss of the supratemporals, intertemporals, tabular, postparietals, jugals, and postorbitals. Other elements, such as the pterygoid and parasphenoid bones in the palate, Pedicel are reduced, producing a similar configuration of bones among the three modern amphibian groups. Nonetheless, the skull morphology of caecilians is highly unusual compared with that of frogs and salamanders, reflecting the caecilians’ very different life history. Replacement crown growing within pedicel Some of these characters (e.g., characters 4–8) are difficult or impossible to evaluate in extinct taxa because soft Tympanic membrane anatomy is rarely preserved in fossils. Moreover, not all of Stapes these characters are unique to Lissamphibia. Nonetheless, Footplate the preponderance of morphological evidence supports lis- (B) samphibian monophyly. Although molecular studies cannot sample extinct taxa, no recent molecular phylogenetic analyses reject lissamphibian monophyly. In summary, the Operculum Opercular muscle most comprehensive molecular and morphological analyses support the hypothesis that salamanders and frogs are more closely related to one another than to caecilians. Suprascapula Paedomorphosis in lissamphibian evolution Although the contrasting hypotheses of lissamphibian ori- Opercular muscle gins (see Section 2.3) affect our interpretation of lissam- Tympanic phibian evolution, miniaturization and heterochrony have Scapula membrane probably been a pervasive influence on the evolution of the highly derived skeletal morphology of lissamphibians regardless of their origins (Bolt 1977, 1979; Laurin 1998b). Heterochrony (from the Greek hetero, “different,” + chro- nos, “time”) is a change in the timing of embryonic and juvenile development that affects the sexually mature adult phenotype. Paedomorphosis (from the Greek paed, “child,” + morph, “form”) is a type of heterochrony and refers to the Figure 2.12 Two shared derived characters of Lissam- retention of juvenile characters in adult stages of an organ- phibia. (A) Pedicellate teeth. Each tooth crown sits on a base ism (see Chapter 8). For example, some salamanders re- (pedicel); the two elements are separated by a fibrous connec- tain the juvenile conditions of having gills and being fully tion. The teeth are bicuspid, with one cusp (point) on the lingual aquatic in adulthood despite being sexually mature, and (inner) side of the jaw and a second on the labial (outer) side. we infer that these salamanders are derived from ancestors (B) The opercular apparatus is part of the lissamphibian sound- with the ability to transform to the adult form. In essence, conducting system, allowing ground vibrations to be transmit- these salamanders have arrested metamorphosis and re- ted from the forelimb to the inner ear. This apparatus is a syn- tain some juvenile features, despite the sexual maturation apomorphy of frogs and salamanders (Batrachia), although it is of their gonads. reduced in salamanders; it has been secondarily lost in caecilians. If lissamphibians are derived from temnospondyls, then (A after Parsons and Williams 1963.) paedomorphosis can explain many of their unusual shared morphological characters. One common result of paedomorphosis is size reduction (juveniles are smaller than 11. The radius and ulna articulate with a single structure adults), and extant amphibians are very small (~5–15 cm) on the humerus called a radial condyle. This char- compared with many Paleozoic tetrapods. Temnospondyls acter has been lost in caecilians, which are limbless show an astounding diversity of body sizes (see Figure 2.11), Pough(Sigurdsen 4e and Bolt 2009). but there is a striking evolutionary trend toward size reduc- Sinauer Associates Morales Studio Pough4e_02.12.ai 05-07-15 uncorrected page proofs © 2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 34 Chapter 2  Phylogenetic Systematics and the Origins of Amphibians and Reptiles

(A) Temnospondyl (B) Salamander (C) Frog

Sphenethmoid Premaxilla Premaxilla Nasal Premaxilla Maxilla Frontoparietal Maxilla Nasal Lacrymal Nasal Maxilla Pterygoid Prefrontal Frontal Frontal Postfrontal Parietal

Postorbital Prootic- Jugal exoccipital (fused) Parietal Quadrate Squamosal Supratemporal Squamosal Exoccipital Prootic Squamosal Quadratojugal Postparietal Tabula Quadrate

Sphenethmoid Premaxilla Premaxilla Premaxilla Vomer Vomer Vomer Palatine Maxilla Maxilla Palatine Pterygoid

Squamosal

Pterygoid Quadrate Parasphenoid Parasphenoid Quadrate Parasphenoid

Figure 2.13 Skulls of lissamphibians and a temnospondyl. Compared with Dendrerpeton, the two lissamphibians have lost Dorsal views are shown above and ventral views below. (A) many skull elements and evolved larger orbits, both manifes- Dendrerpeton, an edopoid temnospondyl from the Paleozoic. tations of paedomorphosis. (After Duellman and Trueb 1986; (B) The salamander Phaeognathus hubrichti (Caudata: Plethod- Carroll 1998.) ontidae) (C) The frog Gastrotheca walkeri (Anura: Hylidae).

1. Skull bones such as the supratemporals, postfrontals, tion, of which dissorophoids and lissamphibians are simply prefrontals, jugals, postorbitals, and ectopterygoids the end point. In other words, lissamphibians may be min- were the last to appear during the development of iaturized temnospondyls. branchiosaur temnospondyls. It is precisely these The heterochronic process left many other imprints on bones that are absent from lissamphibian skulls, thePough morphology 4e of lissamphibians. In fact, some of the suggesting that frogs, caecilians, and salamanders mostSinauer characteristic Associates features of lissamphibians can be in- have arrested their development at a stage before Morales Studio these bones form. All of the skull bones appearing terpretedPough4e_02.13.ai as paedomorphic 05-06-15 features (Schoch 2009, 2010). We give just three examples here, made possible by the early in the development of branchiosaurs (nasals, remarkable preservation of developmental sequences, in- frontals, parietals, lacrimals, etc.) are present in cluding larvae, juveniles, and adults, of some dissorophoid lissamphibians. temnospondyls known as branchiosaurs from the Early 2. The eye orbits of lissamphibians and dissorophoids Permian of Germany. Ontogenetic series of branchiosaurs are large relative to those of other Paleozoic forms. are so well preserved that it is possible to examine the Sensory organs, such as the eyes, form relatively sequence in which the bones of the skull ossified during early in development and are relatively large in early development. developmental stages. As a result of paedomorpho-

time in certain groups (Gauthier et al. 1988). For example, a sis, lissamphibians and derived dissorophoid tem- penis with erectile tissue is found among male crocodylians, nospondyls have large eyes compared with those of mammals, turtles, and some birds. However, the single penis many other Paleozoic temnospondyls. was secondarily lost in the ancestor of Lepidosauria (tuatara, 3. The bicuspid, pedicellate teeth of lissamphibians may lizards, and snakes) as well as most birds. Tuatara reproduce be a retained juvenile condition observed in dissoro- by cloacal apposition without the assistance of an intromit- phoid temnospondyls. Tooth development in disso- tent organ. Squamates (lizards and snakes) evolved paired rophoids and lissamphibians undergoes a sequence hemipenes, but it remains unclear whether the hemipenes in which larvae have nonpedicellate, monocuspid are completely or partially homologous to the ancestral am- teeth. At metamorphosis these teeth are replaced by niote penis (Gredler et al. 2014; Leal and Cohn 2015). Despite bicuspid, pedicellate teeth. In dissorophoids, but not its secondary loss in lepidosaurs and birds, the male penis is lissamphibians, these bicuspid, pedicellate teeth are considered a shared derived character of Amniota. Within gradually replaced by adult teeth that are monocus- the amniotes, reptilian monophyly is supported by characters pid and have the characteristic labyrinthodont struc- of the skull and limbs (deBraga and Rieppel 1997) and by ture. Thus, the adult lissamphibian tooth condition countless phylogenetic analyses of DNA data. (pedicellate, bicuspid, and lacking labyrinthodont The earliest extinct relatives of Amniota are the Late structure) is that shown by juvenile dissorophoids. In Carboniferous reptilomorphs (e.g., Diadectes; Figure 2.14A). other words, adult lissamphibians retain the juvenile All of the extant amniote groups can be traced to the Perm- condition shown by ancestral temnospondyls. ian or Early Triassic. Thus, amniotes appear in the fossil Many peculiar aspects of morphology are comprehensible record at approximately the same time as early stem-group when lissamphibians are viewed as paedomorphic relative lissamphibians. The earliest identified fossil amniote is to Paleozoic stem tetrapods. Understanding paedomorpho- Casineria, a small (~85 mm) lizardlike animal from the sis sheds light on a fundamental evolutionary process gov- Late Carboniferous (~340 mya), and numerous taxa (e.g., erning morphological evolution in many tetrapods. Paleothyris; Figure 2.14B) have been discovered in slightly younger fossil deposits (~310–300 mya). Paton et al. (1999) speculated that the amniote lineage is even older, possibly 2.5  Characteristics and Origin dating back to approximately 360–350 mya, dates also sup- of the Amniotes ported by molecular clock studies (Hedges 2009). There- fore, Lissamphibia and Amniota probably diverged within We have traced the phylogeny of tetrapods from their ori- 30 million years after the origin of the earliest tetrapods. gins to the basic split among the extant groups Lissamphibia Early Carboniferous limestone deposits in Scotland contain and Amniota and considered the evolutionary relationships fossil amniotes, temnospondyls, lepospondyls, and several of taxa associated with the amphibian clade. Now we turn specimens that have a mixture of amniote and temnospon- to Amniota, the reptiles (including birds) and mammals. dyl characters, and constitute one of the oldest terrestrial vertebrate assemblages known (Milner and Sequeira 1994; The origins of Amniota Clack 1998; Paton et al. 1999). Amniotes are named for their highly specialized amniotic egg (see Chapter 9). The evolution of the amniote egg al- The major amniote lineages: Synapsida lowed vertebrates to move into new ecological niches, most and Diapsida notably land, as it freed reproduction from dependence on The phylogeny of the amniotes has been extensively studied external water. The amniote egg consists of an outer flexible using morphological and molecular data sets and, with the or hard shell and contains the embryo and four extraem- exception of the turtles, there is broad agreement on the re- bryonic membranes: the yolk sac, which stores energy; the lationships among the major groups (see Figure 2.7). During fluid-filled amnion, which surrounds and cushions the em- the Early Carboniferous, amniotes split into two lineages, bryo; and the chorion and allantois, which perform multiple Synapsida and Reptilia. Synapsida gave rise to the mam- functions, including gas exchange and, in the case of the mals and the extinct therapsids that were the dominant ter- allantois, storage of nitrogenous waste. In viviparous am- restrial megafauna of the Permian. The Reptilia diversified niotes (many squamates and most mammals), the chorion into numerous Carboniferous and Permian lineages, all of and sometimes the allantois are modified into the embry- which became extinct except the Diapsida—the group that onic portion of the placenta. includes extant reptiles (including birds) as well as the ex- In addition to the shell and extraembryonic membranes, tinct pterosaurs and dinosaurs. characters supporting the monophyly of Amniota include Synapsida and Diapsida are named for the number of derived characters of the skull, pectoral girdle, and appen- holes, called fenestrae (Latin fenestra “window”), in the dicular skeleton (Laurin and Reisz 1995), as well as molecular temporal region of the skull. Turtles and some extinct am- data. Some aspects of soft anatomy that may be derived char- niotes lack these openings, a condition called anapsid, from acters have probably been secondarily lost over evolutionary the Greek an, “without” + apsid, “arch” (Figure 2.15A).

Orbit Figure 2.14 Diversity of (A) Diadectes (~0.3 m) Late Paleozoic amniotes. (A) Diadectes is an early extinct relative of Amniota. (B) Paleothyris, one of the oldest known amniotes. (C) Scutosaurus, a “parareptile” with an anapsid skull condition lacking temporal (B) Paleothyris (~0.3 m) Orbit fenestrae. (D) Petrolacosau- rus, an early diapsid. (E) The synapsid Dimetrodon. (A after Romer 1944, Carroll 1969; B after Carroll 1969, Carroll and Baird 1972; C after Kuhn 1969; D after Reisz 1981; E after Romer and Price 1940.) (C) Scutosaurus (~3 m) Orbit

Fenestrae

(D) Petrolacosaurus (~0.5 m) Orbit

Fenestra Orbit

(E) Dimetrodon (~3 m)

Synapsids (from the Greek syn, “together”) have a single the sail-finned Dimetrodon (see Figure 2.14E) and multiple temporal fenestra (Figure 2.15B). In humans, this fenestra lineages of large, predatory therapsids. However, these ex- can be seen as the opening between the cheekbone (the zy- tinct lineages are more closely related to mammals than gomatic arch) and the temporal and sphenoid bones of the to reptiles, and are thus more properly referred to as non- cranium. The evolution of synapsids is beyond the scope of mammalian syapsids. this book, other than to briefly mention the stem synapsids Diapsids have two temporal fenestrae (Figure 2.15C), but that dominated the Permian prior to the rise of dinosaurs. the lower temporal fenestra has been secondarily lost in These early synapsids, sometimes called “mammal-like lizards (Figure 2.15D) and in the extinct rhynchocephalian reptiles” because of their superficial resemblance to ex- lineages, and both fenestrae have been lost in the highly tant and extinct mammals, includePough iconic 4e animals such as modified snake skull. In both diapsids and synapsids, the Sinauer Associates Morales Studio Pough4e_02.14.ai 03-12-15 uncorrected page proofs © 2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 2.6  Diapsida: Lepidosauria and Archosauria 37

(A) Anapsid (B) Synapsid (C) Diapsid Orbit Fenestra Fenestrae

Figure 2.15 Three general patterns of temporal (D) Lizard fenestration in amniote skulls. (A) Among extant Fenestra amniotes, only the turtles have the anapsid skull condition. Parietal (B) Modern mammals and several extinct non-mammalian Postorbital lineages have the synapsid condition. (C) Extant reptiles Squamosal have the diapsid condition. However, the pattern of fenes- Jugal tration in the squamate skull (D) is secondarily modified from the diapsid condition by loss of the lower temporal bar, resulting in a single fenestra. distinction between the two is that Sauria contains only extant diapsids, whereas Diapsida includes Sauria and extinct stem lineages. We will use the name Diapsida for the temporal fenestrae permit space for bulging jaw muscles remainder of this chapter. and are important adaptations that allow a strong bite force. Diapsida includes many familiar fossil groups, includ- Indeed, you can locate your own fenestra by clenching your ing those highly modified for a marine existence such as teeth and feeling the bulge of the temporalis muscle that ichthyosaurs and plesiosaurs, but two other lineages, Lepi- passes through the fenestra behind the cheekbone. dosauria and Archosauria, are most relevant to this discus- Thus, extant reptiles have either an anapsid skull condi- sion. Lepidosauria includes Squamata (lizards and snakes), tion (turtles only) or a diapsid skull (lizards, snakes, tua- Rhynchocephalia (tuatara), and several fossil groups. Ar- tara, crocodylians, and birds). It is generally agreed that the chosauria includes Crurotarsi (crocodiles and extinct rela- anapsid skull is the ancestral condition for amniotes, and tives) and Avemetatarsalia, which contains Pterosauria (ex- therein lies one of the most disputed aspects of amniote tinct flying reptiles), Dinosauria (dinosaurs and birds), and phylogeny: Where do turtles fit into the reptile phylogeny? the highly aquatic Ichthyosauria and Plesiosauria. To make Because the anapsid condition is ancestral for amniotes, the matters more confusing, Crurotarsi is sometimes called fact that turtles have an anapsid skull gives no clue to their Pseudosuchia and Avemetatarsalia is called Ornithodira relationships. We will return to this question after first out- in the literature (see Nesbitt 2011). Molecular dating indi- lining the radiation of diapsids. cates that Lepidosauria and Archosauria split in the Early to Middle Permian (~285–260 mya) (Jones et al. 2013). 2.6  Diapsida: Lepidosauria Lepidosauria and Archosauria Lepidosauria includes Squamata (lizards and snakes) and Rhynchocephalia (tuatara). Characters of both the skull and The clade Diapsida includes most, and perhaps all, extant appendages support the monophyly of Lepidosauria (e.g., reptiles (depending on whether turtles are diapsids; see Gauthier et al. 1988; Evans 2003; Hill 2005), as do all recent Section 2.7). Diapsids are an extraordinary radiation that phylogenetic analyses of molecular data (e.g., Crawford et produced major components of terrestrial and marine eco- al. 2012; Mulcahy et al. 2012). The soft anatomical char- systems from the Late Carboniferous (e.g., Petrolacosaurus; acters of Lepidosauria are the major characters by which see Figure 2.14D) to the present. Of the extraordinary radia- we recognize squamates and tuatara. Lepidosaurs have a Pough 4e Sinauertion of Associates diapsids in the Mesozoic, only a few major groups transverse cloacal slit (versus an anteroposterior orientation Moralesof Lepidosauria Studio and Archosauria are still extant, although in other tetrapods), loss of a single penis and subsequent Pough4e_02.15.aibirds and squamates 05-05-15 account for more species than all other evolution of paired penes (hemipenes) or their homologs extant amniotes combined. The number of extant diapsid residing in the tail base, and regular cycles of shedding (ec- species—more than 19,000—far surpasses that of their dysis) of the outer layer of the epidermis (see Chapter 4). sister group Mammalia (Synapsida), which numbers about Most early ancestors of Lepidosauria (the Lepidosauro- 5,400 species. morpha) were small and did not fossilize well. The oldest The taxonomic nomenclature of diapsids can be confus- lepidosaur fossils are a jaw fragment, skull, and anterior ing not only because of the many clade names, but also skeleton of Megachirella wachtleri (Renesto and Bernardi because the name Sauria (rather than Diapsida) is often 2013), both from the Middle Triassic (~240 mya) (Jones et used to refer to extant reptiles. Both names are correct in al. 2013). Although both rhynchocephalians and squamates that they refer to clades that contain extant reptiles. The were both present through the rest of the Mesozoic, the

Late Triassic and Early Jurassic rhynchocephalian fauna is in the Mesozoic. More than 1,400 species of extinct dino- far better represented in the fossil record (Evans and Jones saurs have been discovered, and extant dinosaurs are rep- 2010; see Chapter 4). Although some Jurassic squamate fos- resented today by the more than 10,000 species of birds. sils exist, modern, morphologically diverse families are not widely represented until the Middle Cretaceous. Thus, the fossil record suggests that the early history of Lepidosauria 2.7  The Debated Origins of Turtles was dominated by rhynchocephalians that were later replaced by squamates. However, given the poor fossil record Notably absent from our discussion of reptile phylogeny is of early squamates, this generalization should be viewed the origin of turtles, a long-debated topic that has produced with skepticism until more data are collected. numerous papers supporting different phylogenetic resolu- tions (see Carroll 2013 and Scheyer et al. 2013 for reviews). Archosauria The highly modified body plan of turtles makes assessing Archosauria include Crurotarsi (crocodylians) and Avemeta- homology of morphological characters difficult. tarsalia (pterosaurs, dinosaurs, and birds). Characters of All studies agree that turtles, archosaurs, and lepidosaurs both the skull and appendages support the monophyly of form a clade (Reptilia), but they disagree on the sister lin- Archosauria (e.g., Benton 1985; Brusatte et al. 2010; Nesbitt eage to turtles. Turtles lack temporal fenestrae (the anapsid 2011), as do all recent phylogenetic analyses of molecular condition; Figure 2.16A) and therefore may be related to a data (e.g., Chiari et al. 2012; Crawford et al. 2012; Fong et group of reptiles that share this anapsid condition and that al. 2012; Field et al. 2014). diverged before the origin of diapsids—the “parareptilia” Early archosaurs were typically large and robust and left (see Scutosaurus, Figure 2.14C). Indeed, numerous recent a more complete fossil record than did the contempora- studies based on extensive morphological data sets that in- neous lepidosaurs (Nesbitt 2011). The earliest member of clude both extinct and extant taxa support this relationship Archosauria is the Early Triassic (~249 mya) Xilousuchus, a (e.g., Gauthier 1988; Werneburg and Sánchez-Villagra 2009; pseudosuchian with a sail-like dorsal structure similar to Lyson et al. 2010, 2013). However, no modern phylogeny that of the synapsid Dimetrodon (see Figure 2.14E) (Nestbitt based on molecular data supports this relationship. Rather, et al. 2010). Both major lineages of archosaurs, Crurotarsi essentially all molecular studies support a sister relation- and Avemetatarsalia, experienced their greatest diversity ship between archosaurs and turtles (Figure 2.16B). Finally, in the Late Triassic (~228–209 mya) and then suffered a some morphological studies (e.g., deBraga and Rieppel 1997; marked loss of diversity during the Triassic–Jurassic ex- Rieppel 2000; Hill 2005) support a third possible position tinction, although avemetatarsalians, represented mostly of turtles as sister to lepidosaurs (Figure 2.16C). If either of by pterosaurs and dinosaurs, remained diverse throughout the latter two hypotheses is correct, the anapsid condition the Jurassic and Cretaceous, the last two-thirds of the age of the turtle skull must be secondarily derived from an an- of dinosaurs (Brusatte et al. 2011). cestral diapsid condition and therefore convergent with the The radiation of Archosauria was marked by two no- anapsid skull condition seen in “parareptiles.” table morphological trends. First, early members of the There are many possible explanations for the differing clade show derived cranial modifications associated with results among the phylogenetic studies based on morpho- increased predatory efficiency, including elaborated cranial logical data, but which taxa are included in the analysis is musculature and sharp, thecodont dentition (i.e., teeth set probably the most important. Given their aquatic nature in sockets in the jaw bones). These and other modifica- and heavily ossified body plan, turtles have an extensive tions reached their culmination in some dinosaurs, which fossil record, thereby allowing morphological analysis of added features such as raptorial forelimbs suitable for grab- both extinct and extant species. However, the homologies of bing prey. Many features of birds that are associated with some morphological characters are debated, and phyloge- flight—long forelimbs and birdlike wrists, fused clavicles netic analysis of these data is sensitive to which taxa are in- (furcula), a fused bony sternum, hollow bones, and long cluded. It is more difficult to explain the differing results of forelimbs—evolved earlier in the archosaur radiation in the molecular and morphological analyses. The molecular association with predatory habits (Gauthier and Padian analyses may be the best representation of turtle phyloge- 1985). Even feathers evolved in pre-avian dinosaurs (e.g., netic relationships because they include far more characters Padian and Chiappe 1998; Xu et al. 2003; Godefroit et al. (thousands) than those based on morphological data (hun- 2014). Second, modifications in the postcranial skeleton of dreds), and are arguably less biased to the interpretation of archosaurs permitted an erect stance, a narrow-track gait, homology by the investigator. However, because molecular and the ability to breathe while running (Parrish 1986). The data cannot be collected from fossil taxa, studies based on evolution of locomotor specializations, a hallmark of the morphological data can better capture stem lineages that archosaur radiation, indicates evolutionary trends toward are phylogenetically informative. Although it is highly un- more active lifestyles than observed in the lepidosaur ra- likely that phylogenies estimated from turtle morphology diation. Dinosaurs were an extraordinarily diverse group and DNA will reach a consensus, the archosaur origin of comprising major components of terrestrial vertebrate life turtles is increasingly accepted.

(A) Anapsid hypothesis (B) Archosaur hypothesis Archosauria Archosauria Aves Aves Archosauromorpha Diapsida Crocodylia Crocodylia Diapsida Squamata Testudines

Lepidosauria Rhynchocephalia Squamata Reptilia Testudines Rhynchocephalia Lepidosauria Synapsida “Parareptiles”

Archosauria Aves Synapsida Crocodylia Figure 2.16 Three hypotheses of turtle origins. (A) The anapsid Diapsida Lepidosauria hypothesis proposes that turtles are most closely related to early-diverging Squamata “parareptile” lineages that had no temporal fenestration. Although morpho- Rhynchocephalia logical data support this hypothesis, no analysis of molecular data upholds it. (B) The hypothesis supported by almost all phylogenetic analyses of DNA Testudines data is that turtles are diapsids and the sister lineage to extant archosaurs Lepidosauromorpha (crocodiles and birds). (C) The hypothesis that turtles are diapsids and the sis- Synapsida ter lineage to lepidosaurs (lizards, snakes, and tuatara) is supported by some morphological data but is not widely accepted.

Summary  Phylogenies are a critical tool in understanding A stem-based taxonomic name (e.g., Tetrapodomorpha) the evolutionary history of life. includes a group more closely related to one taxon than Phylogenetic systematics, also known as cladistics, to another. emphasizes the importance of derived characters (char-  Discovering and describing new species is a acters that have changed from the ancestral condition) fundamental goal of phylogenetic systematics. shared among taxa in recognizing monophyletic groups The morphology, and often DNA, of a putative new (clades). species is compared to that of existing described species Phylogenies can be reconstructed using many different to identify potential differences. kinds of data. Skeletal features and DNA data are most Multiple criteria are used to decide whether or not an commonly used. organism is a new species. These usually consist of DNA has become the predominant type of data to infer morphological features such as coloration or scale pat- phylogenies of extant organisms because of the larger terns (in reptiles), or of advertisement calls (in frogs), data sets that can be constructed compared with mor- but new species can also be identified by phylogenetic phological data. However, only morphological (mostly analysis of DNA. skeletal) data can be collected for fossil taxa. New species are described in a scientific paper that The use of DNA data allows researchers to study the defines a holotype (the individual specimen that pos- evolutionary history of organisms that may not display sesses all the characters of that species) and that pro- substantial morphological differences and allows esti- vides a unique binomial species name, a morphological mationPough of4e when lineages diverged. description of the new species, and an explanation of Sinauer Associates how this new species differs from other species.  Rank-freeMorales Studio taxonomy dispenses with the use of LinneanPough4e_02.16.ai ranks above 05-05-15 the genus level.  Tetrapods are evolutionarily derived from Late Equal Linnean ranks do not necessarily represent Devonian sarcopterygian fish. groups that are equal in diversity or age. The transition from water to land was a gradual pro- A node-based taxonomic name (e.g., Tetrapoda) in- cess over the span of approximately 20 million years. cludes the most recent common ancestor of at least two Increasing adaptations to terrestriality are preserved taxa and all of its descendants. in the fossil record in multiple aquatic taxa, including

Eusthenopteron, Pandericthys, Tiktaalik, Acanthostega, and Many of the morphological features of Lissamphibia Ichthyostega. can be explained by paedomorphosis. The greater effect of gravity on land compared with  Reptiles and mammals form the clade Amniota. water required the evolution of skeletal adaptations to bear the mass of the animal. These adaptations includ- Amniotes are defined primarily by their possession of ed extensively interlocking vertebrae and robust limbs the amniotic egg—a specialized structure composed and pelvic and pectoral girdles. of a protective eggshell and four extraembryonic membranes. The loss of gills and the evolution of oil- and wax- producing glands are adaptations to living in a dry ter- The earliest fossil amniote is from the Late Carbonifer- restrial environment. ous and was contemporaneous with lissamphibians. Terrestrial living also required changes to sensory sys- With the possible exception of turtles, all extant amni- tems, especially hearing. otes are classified in two clades, Synapsida and Diap- sida.  Extant amphibians, which include salamanders, • Synapsida includes mammals and extinct non- frogs, and caecilians, form a clade called mammalian species identifiable by the possession of Lissamphibia. a single temporal fenestra in the skull. Numerous characters, including features of the teeth, • Diapsida includes two major clades: sensory systems, musculature, and skeleton, support Archosauria (crocodylians, dinosaurs, and the monophyly of Lissamphibia. birds) and Lepidosauria (lizards, snakes, and The evolutionary origins of Lissamphibia are debated. rhynchocephalians). Diapsids are identifiable by the The temnospondyl hypothesis is the most widely ac- possession of two temporal fenestrae in the skull, cepted and states that lissamphibians are derived from although this condition has been secondarily lost in the temnospondyls—amphibians with vertebrae com- all squamates and some extinct rhyncocephalians. posed of two distinct centra.  There are three major hypotheses of turtle origins. The lepospondyl hypothesis states that lissamphibians Most phylogenetic analyses of morphological data sup- are derived from the lepospondyls—amphibians with a port the sister relationship of turtles and Diapsida. single circular centrum. Essentially all phylogenetic analyses of molecular data The diphyly hypothesis states that Lissamphibia is support the sister relationship between turtles and not monophyletic and that caecilians are derived from Archosauria. lepospondyls, and frogs and salamanders from temnospondyls. This hypothesis is not widely accepted. Some morphological studies support the sister relationship of turtles and Lepidosauria, although this hypoth- Most phylogenetic studies support a clade composed esis is not widely accepted. of frogs and salamanders (Batrachia) that is the sister lineage to caecilians.

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