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The Palaeozoic Ancestry of Salamanders, Frogs and Caecilians

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The Palaeozoic Ancestry of Salamanders, Frogs and Caecilians Blackwell Publishing LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2007? 2007 150s2 1140 Original Articles LISSAMPHIBIAN ANCESTRYR. L. CARROLL Zoological Journal of the Linnean Society, 2007, 150 (Suppl. 1), 1–140. With 78 figures The Palaeozoic Ancestry of Salamanders, Frogs and Caecilians ROBERT L. CARROLL FLS1 1Redpath Museum, McGill University, 859 Sherbrooke St W., Montreal, P.Q. Canada, H3A 2K6 The relationships of frogs, salamanders, and caecilians (Gymnophiona) with one another and with the vast assem- blage of Palaeozoic amphibians remain highly contentious phylogenetic problems. Cladistic analyses support a com- mon ancestry of the three modern orders, but fail to achieve a consensus regarding their affinities with Palaeozoic amphibians. The most exhaustive phylogenetic analyses that have been applied to the ancestry of lissamphibians have recognized few, if any, biologically significant characters differentiating the living orders. These results can be attributed to limiting the database primarily to characters common to Palaeozoic amphibians and including few fea- tures that distinguish the modern orders. Making use of the numerous derived characters that are expressed in either the larvae or adults of extant salamanders, frogs, and caecilians provides the basis for recognizing a nested sequence of synapomorphies that support a common ancestry of salamanders and anurans with temnospondyl lab- yrinthodonts to the exclusion of caecilians. The larvae of Carboniferous and Permian temnospondyl labyrinthodonts provide strong evidence for their being members of the stem group of urodeles. This is based primarily on the great similarity in the sequence of ossification of the bones of the skull and appendicular skeleton, but is also supported by detailed similarities of the hyoid apparatus. Recognition of a sister-group relationship between Permo- Carboniferous branchiosaurids and crown-group salamanders makes it possible to determine the sequence of changes in the anatomy and ways of life that occurred during the origin of urodeles, and to determine their time of divergence relative to that of frogs and caecilians. The Lower Triassic salientian Triadobatrachus exhibits early stages in the evolution of the anuran skull that enable close comparison with Palaeozoic dissorophoid amphibians and point to the early evolution of anuran hearing and vocalization. The Lower Jurassic caecilian Eocaecilia shows few if any unique derived characters in common with salientians or caudates, but the anatomy of the skull and the elongate body form point to affinities with the Permian microsaur Rhynchonkos. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150 (Suppl. 1), 1–140. ADDITIONAL KEYWORDS: Anura – Apateon – branchiosaurs – caecilians – Caudata – Hennig – neoteny – phylogenetic analysis – sequential ossification – urodeles. INTRODUCTION larvae and adults in order to understand their pat- terns of evolution and relationships. Living amphibians differ fundamentally from other The amphibious way of life of frogs, salamanders, terrestrial vertebrates – the reptiles, birds, and mam- and caecilians has long been thought to result from a mals (collectively the Amniota) – in that primitive retention of characteristics of animals transitional members of all three orders have a biphasic life his- between fish and amniotes. With the discovery of tory. Typically, these species have obligatorily aquatic Palaeozoic tetrapods with lateral-line canal grooves larval stages possessing lateral-line sensory organs, and gilled larval stages, they were grouped with the but facultatively terrestrial adult stages. Amphibian modern orders in the Class Amphibia. However, it was larvae and adults are commonly highly distinct from soon recognized that the Palaeozoic amphibians were one another, with different body forms, modes of loco- very different from the modern orders in nearly all motion, and ways of feeding. Most show a clearly rec- aspects of their skeletal anatomy, and provided very ognizable metamorphosis between larvae and adults. little evidence of specific relationships. The free-living larvae are subject to different selective Many different hypotheses of relationships between regimes from the adults, and have distinct evolution- various groups of Palaeozoic amphibians and the three ary trajectories. Functional complexes such as feeding modern orders were proposed in the mid-20th century, and locomotion must be described separately for the but the fossil evidence was not sufficient to support a © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150 (Suppl. 1), 1–140 1 2 R. L. CARROLL consensus (e.g. Gregory, Peabody & Price, 1956; Eaton, such as Eusthenopteron. Although the monophyletic 1959; Szarski, 1962; Reig, 1964). The basic problem origin of tetrapods from among the osteolepiforms, was the almost total absence of fossils from beds of more specifically the tristichopterids and panderich- intermediate age that provided anatomical links thyids, is now broadly accepted (Gaffney, 1979; between any of the many lineages of archaic amphib- Panchen & Smithson, 1988; Ahlberg & Johanson, ians and the highly derived frogs and salamanders 1998; Heatwole & Carroll, 2000; Clack, 2000, 2002a), known from the Mesozoic. There was also, until there remain very serious problems in recognizing an recently, a complete absence of fossil caecilians. immediate common ancestry for frogs, salamanders, A central question has been whether frogs, sala- and caecilians. manders, and caecilians are monophyletic in terms of In addition to providing evidence for the monophyl- having an immediate common ancestor that can be etic origin of frogs, salamanders, and caecilians, Par- distinguished from all other known groups of Palaeo- sons & Williams (1963) attempted to visualize a model zoic amphibians. This question remains difficult to of the anatomy of a plausible common ancestor, but answer because of the fundamental differences be- they were unsuccessful in identifying any Palaeozoic tween frogs, salamanders, and caecilians at their first tetrapod with an appropriate combination of charac- appearance in the fossil record, as well as the dis- ters. At the time, an outline of the relationships of tinction of all three from any known Palaeozoic Palaeozoic tetrapods was fairly well established, as groups. Molecular evidence is also lacking, due to the reviewed by Romer (1945, 1947). Two major groups of absence of surviving sister taxa of any basal Palaeo- Palaeozoic amphibians had been recognized, the laby- zoic lineages. rinthodonts and the lepospondyls. Parsons & Williams (1962, 1963) initiated the mod- The labyrinthodonts were generally of large size, ern analysis of extant amphibian relationships with from 20 cm to a metre or more in length, and united their search for specialized anatomical characters that primarily by primitive characters, recognizably simi- were present in two or three of the modern orders, but lar to those of choanate fish, such as Eusthenopteron, were not known in Palaeozoic amphibians or in generally considered to be the sister taxa of land amniotes [see Appendix 1 for synapomorphies listed vertebrates. by Parsons & Williams (1963)]. Although they did not These include multipartite vertebrae and retention cite Hennig’s prior publications (Hennig, 1950, 1953, of most of the primitive complement of bones of the 1956) emphasizing the importance of using unique, skull and lower jaw. Three broad groups of labyrinth- shared, derived characters (synapomorphies) rather odonts can be recognized: (1) a stem assemblage than primitive features for establishing relationships, present in the Upper Devonian and Lower Carbonif- this was clearly the approach taken by Parsons and erous, mostly without obvious relationships to any Williams. Their concept of the monophyly of the three later tetrapods; (2) the anthracosauroids, which may extant orders (collectively termed the Lissamphibia) include the ancestors of amniotes; and (3) the temno- continues to serve as the most generally accepted spondyls (Fig. 1A), which are most often cited as being hypothesis of their relationships. related to the lissamphibians (Carroll & Holmes, One of the reasons for the investigation of Parsons 2007). and William into the monophyly of the modern The lepospondyls include an assortment of lineages, amphibian orders [also emphasized by Szarski (1962)] distinguished from labyrinthodonts by a number of was to counter the hypotheses of Holmgren (1933, derived features, including their generally smaller 1949) and Jarvik (1942, 1954, 1960), who argued for a size, less than 20 cm in body length, the presence of diphyletic origin of all tetrapods that was reflected in spool-shaped vertebral centra frequently fused to the divergence of the lineages leading to frogs and sala- neural arch, variable loss of skull bones, and reduction manders at the level of their fish ancestors. On the or loss of limbs (Carroll et al., 1998; Carroll, 1999). basis of conspicuous differences in the mode of limb Five highly distinct orders are recognized: microsaurs, development, Holmgren argued that salamanders nectrideans, lysorophids, adelelospondyls, and aïsto- were unique among tetrapods in having evolved from pods. Microsaurs are a relatively conservative assem- lungfish, whereas frogs and all other terrestrial verte- blage; all of them retain fully developed limbs and brates shared a common ancestry
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