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On the Origin and Evolution of the Ophidia by Alessandro Palci

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On the Origin and Evolution of the Ophidia by Alessandro Palci On the Origin and Evolution of the Ophidia by Alessandro Palci A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in SYSTEMATICS AND EVOLUTION Department of BIOLOGICAL SCIENCES University of Alberta © Alessandro Palci, 2014 ABSTRACT With well over 3,400 described species, snakes undoubtedly represent one of the most successful groups of reptiles. Much has been written about their ecology, behavior, anatomy, relationships and evolution. However, despite the debate about the origin of this taxonomic group dating back to the second half of the XIX century, no consensus has been reached, yet. Scenarios that portray the first snakes as evolving from aquatic lacertilian ancestors are countered with others that see the first snakes as the result of long-term adaptations to a burrowing, cryptic lifestyle. The supporters of the first type of scenario found their evidence mostly in osteological comparisons of non-burrowing snakes with extinct aquatic lizards (e.g., mosasaurs, dolichosaurs and adriosaurs), while the supporters of the second type of scenario base their conclusions mostly on anatomical comparisons between modern legless squamates and burrowing snakes. The debate is further complicated by the scarcity of well-preserved fossil remains that may help elucidate the origin of the group, and by the contradictory interpretations that different authors have provided after examination of the same fossil specimens. Therefore, the goal of this work was that of analyzing all the evidence that has been put forward so far in support of the two main origin scenarios, critically evaluate the contradictory evidence provided by different researchers, examine first-hand all the pivotal extant and fossil taxa that have been used in the formulation and support of each scenario, and provide a phylogenetic analysis of snakes within squamate reptiles that is based both on molecular and morphological data. The examination of over 400 ii specimens of squamates, including both extant and fossil species, lead to the following results: (1) the redescription of several important fossil taxa (Pachyrhachis, Eupodophis, Haasiophis, Najash, and Dinilysia), and the identification, in some of them, of anatomical features never reported before (e.g., chevron bones in Haasiophis, mental foramina and a sacral vertebra in Pachyrhachis); (2) the discovery of new material (a pelvic girdle) attributable to the fossil species Wonambi naracoortensis, a snake whose pelvic anatomy was previously unknown; (3) the retrieval of evidence that supports a reinterpretation of the circumorbital bones of snakes, with particular regard to the “postorbital” and the “supraorbital”, here reinterpreted as primary homologues of the jugal and postfrontal, respectively; (4) a detailed assessment of what constitutes the “crista circumfenestralis” of snakes and how this anatomical feature varies within the Ophidia; (5) new hypotheses regarding the ingroup relationships of snakes, which imply a possible convergent evolution of the macrostomatan skull condition, and the possibility that scolecophidians may represent an aberrant lineage of alethinophidian snakes. iii PREFACE Some of the research conducted for this thesis forms part of an international research collaboration, led by Professor Michael W. Caldwell at the University of Alberta. The literary reviews in chapters one and two, as well as the phylogenetic analyses in chapter eight, are entirely the product of my original work, with some minor edits from my supervisor (M. W. Caldwell). Chapter three of this dissertation has been published as Palci, A., M. W. Caldwell, and R. L. Nydam (2013), Reevaluation of the anatomy of the Cenomanian (Upper Cretaceous) hind-limbed marine fossil snakes Pachyrhachis, Haasiophis, and Eupodophis, Journal of Vertebrate Paleontology, vol. 33, issue 6, 1328–1342. I was responsible for the collection of the data and part of its interpretation, manuscript composition, figures, and phylogenetic analyses. M. W. Caldwell and R. L. Nydam contributed to manuscript edits and some of the interpretations. R. L. Nydam also contributed to enhancing the contrast and sharpness of some of the figures. Chapter four of this dissertation has been published as Palci, A., M. W. Caldwell, and A. M. Albino (2013), Emended diagnosis and phylogenetic relationships of the Upper Cretaceous fossil snake Najash rionegrina Apesteguía and Zaher, 2006, Journal of Vertebrate Paleontology, vol. 33, issue 1, 131–140. I was responsible for the collection and interpretation of the data, manuscript composition, figures, table, and phylogenetic analyses. M. W. Caldwell and A. M. Albino contributed to manuscript edits. Chapter five of this dissertation has been published as Palci, A., M. W. iv Caldwell, and J. D. Scanlon (2014), First report of a pelvic girdle in the fossil snake Wonambi naracoortensis Smith, 1976, and a revised diagnosis for the genus, Journal of Vertebrate Paleontology, vol. 34, issue 4, 965–969. I was responsible for the collection and interpretation of the data, manuscript composition, and figure. M. W. Caldwell and J. D. Scanlon contributed to manuscript edits. Chapter six of this dissertation has been published as Palci, A., and M. W. Caldwell (2013), Primary homologies of the circumorbital bones of snakes. Journal of Morphology, vol. 274, issue 9, 973–986. I was responsible for the collection and interpretation of the data, manuscript composition, figures, and tables. M. W. Caldwell was involved with concept formation and contributed to manuscript edits. Chapter seven of this dissertation has been published as Palci, A., and M. W. Caldwell (2014), The Upper Cretaceous snake Dinilysia patagonica Smith-Woodward, 1901, and the crista circumfenestralis of snakes, Journal of Morphology, vol. 275, issue 10, 1187–1200. I was responsible for the collection and interpretation of the data, manuscript composition, figures, and tables. M. W. Caldwell was involved with concept formation and contributed to manuscript edits. Chapter nine of this dissertation provides the general conclusions to the whole dissertation, and as such, it represents the product of my original work, with the only exception of portions of text that were adapted from the abstracts of the above-mentioned published chapters, which may include minor edits from v my co-authors. Permission is hereby granted to the University of Alberta Libraries to reproduce single copies of this thesis and to lend or sell such copies for private, scholarly or scientific research purposes only. Where the thesis is converted to, or otherwise made available in digital form, the University of Alberta will advise potential users of the thesis of these terms. The author reserves all other publication and other rights in association with the copyright in the thesis and, except as herein before provided, neither the thesis nor any substantial portion thereof may be printed or otherwise reproduced in any material form whatsoever without the author's prior written permission. vi ACKNOWLEDGMENTS The completion of this dissertation would not have been possible without the support of my supervisor M. W. Caldwell. Discussions with him about topics that span from snake anatomy to character construction in phylogenetic analyses have been invaluable in molding my intellectual skills and critical thinking. Other people who have been a source of intellectual stimulation and whom I wish to thank for my personal growth are, in no particular order: R. L. Nydam, A. Murray, R. Holmes, M. S. Y. Lee, T. Konishi, A. LeBlanc, B. Barr, and E. Maxwell. For providing access to data that was used for the completion of this dissertation, I wish to thank O. Rieppel and M. Kearney, who provided the CT- scan data of several squamate taxa (data originally acquired under the Deep Scaly Project); J-C. Rage, Muséum National d’Histoire Naturelle in Paris; D. Kizirian, R. J. Pascocello, and M. G. Arnold, American Museum of Natural History in New York (USA); K. Kelly and A. Resetar, Field Museum of Natural History in Chicago (USA); R. Rabinovich, Museum of the Hebrew University in Jerusalem (Israel); A. G. Kramarz, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Buenos Aires (Argentina); J. B. Losos, J. Rosado, J. Martinez and T. Takahashi, Museum of Comparative Anatomy at Harvard University, Cambridge (USA); M. Fernandez, Z. Gasparini, and E. Tonni, Museo de La Plata, La Plata (Argentina); G. Teruzzi and C. Dal Sasso, Museo Civico di Storia Naturale in Milano (Italy); P. Campbell, Natural History Museum in London (England); K. Smith, Senckenberg Museum in Frankfurt; W. Boehme, P. Wagner, U. Bott, and C. Koch, Zoologisches Forschungsmuseum Alexander vii Koenig in Bonn (Germany); and J. Scanlon and K. Hughes, Riversleigh Fossil Centre, Mount Isa (Australia). Special thanks also go to T. Konishi, P. Huidobro and H. Street for providing several pictures of mosasauroid reptiles. I am very grateful to the members of my defense committee for their valuable comments and suggestions on how to improve this dissertation: J. Acorn, M. W. Caldwell, D. Evans, A. Murray, and R. L. Nydam. I also wish to thank all of the graduate students that shared the joys and pains of being in a graduate program, people who have been part of my life for several years and provided ways to vent the stress and make this experience as enjoyable as possible. These people are, in no particular order: A. LeBlanc, S. Blais, J. Croghan, H. Street, P. Jimenez Huidobro, M. Campbell, T. Simões, J. Liu, B. Kruk, O. Vernygora, T. Argyriou, G. Bradley, K. Grieve, J. Divay, M. Burns, V. Arbour, W. S. Persons, A. Wendruff, and B. Scott. I am also grateful for the friendship of the people I have met outside of the university during my stay in Edmonton, people who made my life in Canada so much more enjoyable: A. Sorochan, M. E. Gurney, K. and M. Werbitski, and L. and C. Strynadka. I wish to thank my parents, Gianfranco and Iolanda, who have always been very supportive of my interest in nature and of my curiosity about evolution and animal diversity. Last but not least, I am grateful to the Department of Biological Sciences of the University of Alberta, my supervisor M.
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