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(Temnospondyli), and the Evolution of Modern THE LOWER PERMIAN DISSOROPHOID DOLESERPETON (TEMNOSPONDYLI), AND THE EVOLUTION OF MODERN AMPHIBIANS Trond Sigurdsen Department of Biology McGill University, Montreal November 2009 A thesis submitted to McGill University in partial fulfillment of the requirements of the degree of Doctor of Philosophy © Trond Sigurdsen 2009 1 ACKNOWLEDGMENTS I am deeply grateful to my supervisors Robert L. Carroll and David M. Green for their support, and for revising and correcting the drafts of the individual chapters. Without their guidance, encouragement, and enthusiasm this project would not have been possible. Hans Larsson has also provided invaluable help, comments, and suggestions. Special thanks go to John R. Bolt, who provided specimens and contributed to Chapters 1 and 3. I thank Farish Jenkins, Jason Anderson, and Eric Lombard for making additional specimens available. Robert Holmes, Jean-Claude Rage, and Zbyněk Roček have all provided helpful comments and observations. Finally, I would like to thank present and past members of the Paleolab at the Redpath Museum, Montreal, for helping out in various ways. Specifically, Thomas Alexander Dececchi, Nadia Fröbisch, Luke Harrison, Audrey Heppleston and Erin Maxwell have contributed helpful comments and technical insight. Funding was provided by NSERC, the Max Stern Recruitment Fellowship (McGill), the Delise Allison and Alma Mater student travel grants (McGill), and the Society of Vertebrate Paleontology Student Travel Grant. 2 CONTRIBUTIONS OF AUTHORS Chapters 1 and 3 were written in collaboration with Dr. John R. Bolt from the Field Museum of Chicago. The present author decided the general direction of these chapters, studied specimens, conducted the analyses, and wrote the final drafts. Dr. John Bolt made many of the relevant specimens available, provided additional observations, data, and photographs, and corrected drafts. 3 TABLE OF CONTENTS Acknowledgments 2 Contributions of Authors 3 General abstract / Résumé 7 General introduction 9 CHAPTER 1. The Lower Permian Amphibamid Doleserpeton (Temnospondyli: Dissorophoidea), the interrelationships of amphibamids, and the origin of modern amphibians Abstract 15 Introduction 16 Systematic paleontology 19 Materials and methods 21 Description 22 Phylogenetic analyses 48 Discussion 52 Bridging text 1 64 CHAPTER 2. The otic region of Doleserpeton (Temnospondyli) and its implications for the evolutionary origin of frogs Abstract 65 Introduction 66 Materials and methods 68 Description 69 Discussion 88 4 Bridging text 2 98 CHAPTER 3. The lissamphibian humerus and elbow joint, and the origins of modern amphibians Abstract 99 Introduction 100 Materials and methods 102 Results 104 Discussion 115 Bridging text 3 123 CHAPTER 4. The anuran humerus and the evolution of jumping in early salientians Abstract 125 Introduction 126 Materials and methods 128 Results 130 Discussion 142 Bridging text 4 145 CHAPTER 5. The origin of modern amphibians: a reevaluation Abstract 147 Introduction 148 Materials and methods 151 Results 154 Discussion 169 5 CONCLUSIONS 175 BIBLIOGRAPHY 179 APPENDIX 1 199 APPENDIX 2 201 APPENDIX 3 211 APPENDIX 4 216 APPENDIX 5 217 APPENDIX 6 224 APPENDIX 7 229 APPENDIX 8 230 APPENDIX 9 241 APPENDIX 10 246 6 ABSTRACT The origin and evolution of modern amphibians is still a subject of controversy. The amphibamid temnospondyl Doleserpeton has often been suggested as a close relative of modern amphibians, but the skeletal morphology of this important taxon has never been fully described. In this thesis, a study of the skeletal anatomy of Doleserpeton is presented, and the interrelationships of dissorophoids are discussed. The relationships of modern amphibians and Paleozoic tetrapods are studied using phylogenetic analyses based on both Bayesian inference and parsimony. The skull of Doleserpeton is preserved in such detail that it allows the first description of the inner ear of an amphibamid temnospondyl. It is found to house a posteriorly positioned perilymphatic duct, a feature which is today restricted to amphibians. Evidence for the presence of a frog-like tympanic annulus is also described. During the studies of the limb skeleton of Doleserpeton, it was realized that important features of the forelimb of modern salamanders were misinterpreted in previous anatomical descriptions. Comparisons of the forelimbs of salientians (frogs), caudates (salamanders) and the Lower Jurassic caecilian Eocaecilia reveal important shared derived traits that are also found in Doleserpeton. Humeral evidence also indicates that saltation was an important part of the locomotion of the Lower Triassic salientian Triadobatrachus. Previous phylogenetic analyses are reexamined and numerous problems in previous character coding are revealed. An analysis of the new data collected suggests that modern amphibians may be a monophyletic group closely related to dissorophoid temnospondyls. 7 RÉSUMÉ L’origine des amphibiens modernes reste un sujet de controverse. Doleserpeton a longtemps été suggéré comme un proche parent des lissamphibiens, mais l’anatomie de ce spécimen important n’avait toujours pas été complètement décrite. La présente thèse porte sur ce spécimen énigmatique en comparant sa morphologie aux amphibiens modernes et fossiles. Ceci nous nous informe sur les liens phylogénétiques entre les amphibiens modernes et ceux datant du Paléozoique en utilisant des analyses basées sur la parcimonie ainsi que sur l’inférence bayésienne. Les conditions de préservation du crâne de Doleserpeton sont telles qu’elles permettent la première description de l’oreille interne d’un membre de ce groupe. Ceci a permis de trouver la présence de conduits périlymphatiques, un trait généralement réservé aux lissamphibiens. Les structures tympaniques rappellent aussi celles des anoures. Ces nouvelles études comparatives ont permis de corriger certaines informations au sujet de l’anatomie des membres supérieurs des salamandres. Les comparaisons anatomiques entre les anoures, les salamandres et le fossile Eocecilia datant du Jurassique présentent de nombreux caractères communs qui permettent de mieux situer les caractéristiques de Doleserpeton. Les données provenant de l’observation de l’humérus ont permis d’établir que la saltation était présente chez Triadobatrachus. De nouvelles analyses phylogénétiques ont été effectuées afin de rectifier les stades des caractères utilisés. Ces nouvelles analyses suggèrent une descendance commune des amphibiens modernes à partir d’un groupe relié aux temnospondyles dissorophoides. 8 INTRODUCTION The Permian amphibamid Doleserpeton annectens (Temnospondyli: Dissorophoidea) is generally regarded as one of the most important fossil taxa for our understanding of the origins of modern amphibians (Bolt, 1968, 1969; Holmes, 2000; Ruta and Coates, 2007). It was found in the Lower Permian (Leonardian) fissure fills of the Dolese Brothers limestone quarry near Fort Sill in Oklahoma. Although this small Permian temnospondyl is a subject worthy of discussion in its own right, the possibility of a close relationship between Dolseserpeton and modern amphibians provides a unique opportunity to study the evolutionary origins of a major group of tetrapods living today. Modern amphibians (often united in the taxon Lissamphibia) consist of three orders within Tetrapoda. These orders are Salientia, Caudata and Apoda (Milner, 1988; Cannatella and Hillis, 2004). Salientia comprise crown-group Anura (frogs and toads) and fossil stem salientians (proanurans). Caudata includes Urodeles (salamanders and newts) and stem taxa. Finally, Apoda consists of Gymnophiona (caecilians) and their fossil relatives. The problem of modern amphibian origins is not only due to the lack of plausible fossils sister-groups, but also the fact that the three modern orders are morphologically disparate, making the search for potential “proto-lissamphibians” difficult (Carroll, 2000). Consequently, there are several opposing hypotheses seeking to explain the evolutionary origins of extant amphibians (Vallin and Laurin, 2004; Carroll, 2007; Ruta and Coates, 2007; Anderson et al., 2008b). 9 A relatively diverse fossil record of modern amphibians first occurs in the Lower Jurassic (Carroll, 2007). The earliest forms include the virtually modern- looking salientians Prosalirus (Shubin and Jenkins, 1995) from the Kayenta formation in Arizona, and Vieraella (Baez and Basso, 1996) from the Lower Jurassic of Argentina. Among the earliest unequivocal caudates we find Karaurus (Ivachnenko, 1978), and Kokartus (reviewed in Milner, 2000) from Kazakhstan and Kirghizstan respectively. The earliest undisputed caecilian is Eocaecilia (Jenkins et al., 2007), which is the only limbed apodan known to science. Like Prosalirus, it was found in the Kayenta formation. In addition to these Jurassic forms, undisputed basal salientian fossils are known from the Lower Triassic. However, only one specimen is represented by an articulated skeleton; that of Triadobatrachus massinoti from Madagascar (Rage and Roček, 1989; Roček and Rage, 2000). Whereas the Lower Jurassic salientian Prosalirus is though to have been a capable jumper (Shubin and Jenkins, 1995; Jenkins and Shubin, 1998), the mode of locomotion in Triadobatrachus is uncertain (Rage and Roček, 1989; Roček and Rage, 2000). Almost nothing is known of the evolution of the modern amphibian groups prior to the Triassic (Carroll, 2007). Although a great variety of tetrapods are known from the Carboniferous and Permian, very few show any features that can demonstrably
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