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Ontogenetic Evidence for the Paleozoic Ancestry of Salamanders

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Ontogenetic Evidence for the Paleozoic Ancestry of Salamanders EVOLUTION & DEVELOPMENT 5:3, 314–324 (2003) Ontogenetic evidence for the Paleozoic ancestry of salamanders Rainer R. Schocha and Robert L. Carrollb aStaatlilches Museum für Naturkunde, Rosenstein 1, D-70191 Stuttgart, Germany bRedpath Museum, McGill University, Montréal, Québec, Canada, H3A 2K6 Authors for correspondence (e-mail: [email protected], [email protected]) SUMMARY The phylogenetic positions of frogs, sala- tire developmental sequence from hatching to metamor- manders, and caecilians have been difficult to establish. phosis is revealed in an assemblage of over 600 Data matrices based primarily on Paleozoic taxa support a specimens from a single locality, all belonging to the genus monophyletic origin of all Lissamphibia but have resulted in Apateon. Apateon forms the most speciose genus of the widely divergent hypotheses of the nature of their common neotenic temnospondyl family Branchiosauridae. The se- ancestor. Analysis that concentrates on the character quence of ossification of individual bones and the changing states of the stem taxa of the extant orders, in contrast, configuration of the skull closely parallel those observed in suggests a polyphyletic origin from divergent Paleozoic the development of primitive living salamanders. These clades. Comparison of patterns of larval development in fossils provide a model of how derived features of the sala- Paleozoic and modern amphibians provides a means to mander skull may have evolved in the context of feeding test previous phylogenies based primarily on adult charac- specializations that appeared in early larval stages of mem- teristics. This proves to be highly informative in the case of bers of the Branchiosauridae. Larvae of Apateon share the origin of salamanders. Putative ancestors of sala- many unique derived characters with salamanders of the manders are recognized from the Permo-Carboniferous families Hynobiidae, Salamandridae, and Ambystoma- boundary of Germany on the basis of ontogenetic changes tidae, which have not been recognized in any other group observed in fossil remains of larval growth series. The en- of Paleozoic amphibians. INTRODUCTION PHYLOGENETIC PROBLEMS AND APPROACHES The origin and interrelationships of frogs, salamanders, and An underlying reason for the uncertainty regarding the rela- caecilians (collectively termed the Lissamphibia) remain tionships of extant amphibians is the insufficient knowledge among the major unresolved problems in the phylogeny of of the fossil record during two important periods in the his- vertebrates. As recently summarized by Laurin (2002) and tory of tetrapods. Specific to the modern taxa are gaps lasting Schoch and Milner (in press), three divergent hypotheses from 80 to 100 million years that separate the oldest known are currently being debated. First, many authors believe representatives of the extant orders from any plausible an- that extant amphibians form a monophyletic clade that di- cestors in the late Paleozoic (Carroll 2001a). The oldest verged from a single group of Paleozoic amphibians, the known fossils of stemgroups frogs (Salientia), caecilians temnospondyls (Gauthier et al. 1988; Bolt 1991; Trueb and (Gymnophiona), and salamanders (Caudata), dating from Cloutier 1991; Milner 1993; Ahlberg and Milner 1994; the Lower to Upper Jurassic, are essentially similar to their Schoch 1995). Second, in sharp contrast, Laurin and Reisz living descendants, and no fossils are known from the Pale- (1997) and Laurin (1998) present data supporting a com- ozoic that are obvious ancestors (Jenkins and Walsh 1993; mon ancestry from a very distinct lineage, the lysorophid Jenkins and Shubin 1998; Gao and Shubin 2001). lepospondyls. Finally, others have argued that the modern Equally troublesome in establishing an informative phy- amphibians are diphyletic, with the caecilians allied with logeny of amphibians is an approximately 30 million year lepospondyls, the frogs with temnospondyls, and the sala- gap at the base of the Carboniferous, during which time the manders suggested as having affinities with either the lep- initial radiation of the later Paleozoic and Mesozoic tetra- ospondyls (Carroll and Holmes 1980; Carroll et al. 1999) or pods is presumed to have occurred (Coates and Clack 1995; with temnospondyls (Anderson 2001; Carroll et al. in Clack 2002). As a result of this hiatus, very few data are press). available to document the specific interrelationships of the © BLACKWELL PUBLISHING, INC. 314 Schoch and Carroll Ontogeny of Paleozoic salamander ancestors 315 major lineages of land vertebrates (Carroll 2002). Recent two possible positions, dependent on whether the crown phylogenetic analyses by Clack (2002) and Clack and Ahl- group is located at one or another node. berg (in press), based on newly recognized species from the The radical differences in the hypothesized sister-taxa of Lower Carboniferous, show very poor resolution of sister- the modern amphibian orders among Paleozoic tetrapods group relationships among Paleozoic tetrapods. Tetrapods suggest limits to the effective use of particular approaches to from the Upper Devonian, Lower Carboniferous, and Upper phylogenetic analysis. This is not to suggest that phyloge- Carboniferous appear as a succession of radiations, each of netic analysis as elaborated by Hennig (1966) is inherently which are characterized by unresolved polytomies (Clack flawed (in fact, it is an extremely effective means of estab- and Ahlberg in press). lishing relationships in most instances), but that there may be Most of the taxa studied by Clack belong to an assem- limits to the amount of missing data that can be accommo- blage long referred to as “labyrinthodonts,” which are as- dated (especially when there are extensive periods during sumed to include the stem taxa of all other tetrapods. These which major morphological changes must have occurred but animals are generally large, up to a meter or more in length, for which there are no data from the fossil record). with proportionately large skulls and a skeletal anatomy gen- In addition, this particular problem has been approached erally similar to that of the sarcopterygian sister-group of tet- in a manner that may have made it especially difficult to rapods, the tristichopterids (characterized by Eusthenopteron) solve using routine methods of phylogenetic analysis. All the and panderichthyids (Ahlberg and Johanson 1998). Unfortu- recent attempts to establish the ancestry of lissamphibians nately, the scarcity of fossils from the Lower Carboniferous have concentrated primarily on Paleozoic taxa, with very lit- makes it difficult to determine the specific interrelationships tle data incorported from the modern orders. This is espe- among the several orders included within the labyrinth- cially evident in the analysis by Laurin and Reisz (1997), in odonts or between any of these and more derived tetrapods. which so few characters of frogs, salamanders, and caecil- Here, the term labyrinthodonts is used in reference to the ians were included that not even the sequence of their diver- eight tetrapod taxa known from the Upper Devonian, of which gence from one another could be established. Most charac- the best known are Acanthostega and Ichthyostega; an assem- ters in their data matrix pertain to Paleozoic taxa but are of blage of archaic Carboniferous families, the Whatcheeriidae, little or no help in solving the problems of lissamphibian an- Crassigyrinidae, and Baphetidae (Clack 2002); and two major cestry. The number of steps that define the resulting cla- clades that dominated the Upper Carboniferous and Lower dogram are dominated by dichotomies involving Paleozoic Permian and continue into the lower Mesozoic, the temno- taxa, only a small percentage of which are significant to the spondyls (Holmes 2000) and anthracosaurs (Smithson 2000) relationships of the lissamphibians. Because only a few (which may have a sister-group relationship with the Sey- nodes determine the position of the lissamphibians, they are mouriamorpha [Laurin 2000]). Among the labyrinthodonts, very sensitive to changes in other parts of the tree. only the temnospondyls are currently considered as plausible On the other hand, a much more direct approach to this ancestors of some or all of the Lissamphibia. problem would be to concentrate on derived characters that The other major assemblage of Paleozoic amphibians are distinguish each of the three extant orders and attempt to the lepospondyls, which can be differentiated from laby- identify some of them in Paleozoic taxa. Instead of trying to rinthodonts by a host of skeletal characters, many of which solve a myriad of phylogenetic problems involving the en- can be associated with their much smaller body size. Lepo- tirety of tetrapod radiation in the Paleozoic, we can begin spondyl skulls are generally less than 4 cm in length and with the well-established monophyly of each of the extant show a diversity of specializations (Carroll 2000a). All lep- amphibian orders. This leaves only three key nodes to estab- ospondyls have spool-shaped vertebral centra in contrast lish: the sister-group relationships of frogs, salamanders, and with the multipartite vertebrae of the labyrinthodonts. Six caecilians with one another and with one Paleozoic lineage lineages of lepospondyls are recognized, ranging in time of (if the Lissamphibia is a truly monophyletic assemblage) or first appearance from Lower to Upper Carboniferous, none with two or three groups of archaic amphibians
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