Phylogenetic Systematics and the 2 Origins of Amphibians and Reptiles he extant amphibians and reptiles are a diverse col- lection 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- 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. 20 Chapter 2 Phylogenetic Systematics and the Origins of Amphibians and Reptiles 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 com- mon 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) 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. 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.