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Diapsid Phylogeny and the Origin and Early Evolution of Squamates by Tiago Rodrigues Simões 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 © Tiago Rodrigues Simões, 2018 ABSTRACT Squamate reptiles comprise over 10,000 living species and hundreds of fossil species of lizards, snakes and amphisbaenians, with their origins dating back at least as far back as the Middle Jurassic. Despite this enormous diversity and a long evolutionary history, numerous fundamental questions remain to be answered regarding the early evolution and origin of this major clade of tetrapods. Such long-standing issues include identifying the oldest fossil squamate, when exactly did squamates originate, and why morphological and molecular analyses of squamate evolution have strong disagreements on fundamental aspects of the squamate tree of life. Additionally, despite much debate, there is no existing consensus over the composition of the Lepidosauromorpha (the clade that includes squamates and their sister taxon, the Rhynchocephalia), making the squamate origin problem part of a broader and more complex reptile phylogeny issue. In this thesis, I provide a series of taxonomic, phylogenetic, biogeographic and morpho-functional contributions to shed light on these problems. I describe a new taxon that overwhelms previous hypothesis of iguanian biogeography and evolution in Gondwana (Gueragama sulamericana). I re-describe and assess the functional morphology of some of the oldest known articulated lizards in the world (Eichstaettisaurus schroederi and Ardeosaurus digitatellus), providing clues to the ancestry of geckoes, and the early evolution of their scansorial behaviour. I also provide a re-description and considerations on ontogeny and sexual dimorphism in the most complete Cretaceous lizard from North America (Polyglyphanodon sternbergi), followed by a biomechanical study on the function of the lower temporal bar in squamates, and a case of non-adaptive reacquisition of this structure in borioteiioids. As the groundwork for my phylogenetic dataset, I provide a thorough discussion on morphological dataset construction for phylogenetic analysis, including a set of basic criteria ii to be followed in order to avoid logical and biological biases in morphological characters. This is followed by a detailed revision of nearly 1,000 characters previously proposed for squamate phylogenies. In my final chapter, I introduce data personally collected by me over the course of 400 days of collection visits on all major lineages of diapsid reptiles and squamates. I analyse these morphological data along with molecular data obtained from online repositories and provide a new diapsid reptile phylogeny tested under distinct optimality criteria, also being the first with a deep sampling of squamates lineages. I find the first ever agreement between morphological and molecular data regarding the early evolution of squamates, and evidence that the Middle Triassic reptile Megachirella wachtleri represents the oldest known fossil squamate in the world. I implement the latest developments in divergence time estimation under relaxed clock Bayesian inference upon this dataset, and I find that the origin of the major diapsid clades, including lepidosaurs, lies prior to the Permian-Triassic extinction event. This revises previous ideas that the origin of lepidosaurs, archosaurs, and other important diapsid lineages happened in the Triassic, and indicates that, rather than triggering their origin, the Permian-Triassic Mass extinction triggered the diversification of already existing diapsid lineages. iii PREFACE The contents of this thesis include only works that have been led by myself, with contributions from my supervisor (Dr. Michael Caldwell), our main collaborator (Dr. Randall Nydam), additional collaborators from the University of Alberta and from notable other locations around the world. However, I have performed the majority of the work in all of the components of this thesis, including published chapters, to justify their inclusion herein. Chapters 1 and 7 were entirely written by myself, but includes short pieces of text that I have previously published in review studies: Simões, T. R., Apesteguía, S., Hsiou, A. S. & Daza, J. D. 2017. Lepidosaurs from Gondwana: An Introduction. Journal of Herpetology, 51(3), 297-299; and Simões, T. R., Caldwell, M. W., Weinschütz, L. C., Wilner, E. & Kellner, A. W. A. 2017. Mesozoic Lizards from Brazil and Their Role in Early Squamate Evolution in South America. Journal of Herpetology, 51(3), 307-315. Chapter 2 has been published as Simões, T. R., E. Wilner, M. W. Caldwell, L. C. Weinschütz and A. W. A. Kellner. 2015. A stem acrodontan lizard in the cretaceous of brazil revises early lizard evolution in gondwana. Nature Communications 6: 9149. I contributed with the description of the new taxon, the phylogenetic analysis, biogeographic considerations, and most of the manuscript writing. Dr. Kellner, Dr. Wilner and Dr. Weinschütz contributed with the fieldwork, Dr. Caldwell contributed with the discussions and editing of the manuscript. Chapter 3 has been published as in Simões, T. R., M. W. Caldwell, R. L. Nydam and P. Jiménez-Huidobro. 2017. Osteology, phylogeny, and functional morphology of two Jurassic lizard species and the early evolution of scansoriality in geckoes. Zoological Journal of the Linnean Society 180: 216-241. I contributed with the redescription of the specimens studying in this work, the phylogenetic analysis, morpho-functional considerations, and most of the iv manuscript writing. Dr. Jiménez-Huidobro contributed with image editing, and all my co-authors contributed with discussions and text editing. Chapter 4 has been published as Simões, T. R., G. F. Funston, B. Vafaeian, R. L. Nydam, M. R. Doschak and M. W. Caldwell. 2016. Reacquisition of the lower temporal bar in sexually dimorphic fossil lizards provides a rare case of convergent evolution. Scientific Reports 6: 24087. In this study, I was responsible for the specimens` redescription, phylogenetic analysis, ontogenetic and sexual dimorphism discussions, providing anatomical dissections and muscle load values for biomechanical analysis, and manuscript writing. G.F. Funston and B. Vafaeian conducted the finite element analysis, Dr. Doschak helped with the CT scans, and Dr. Caldwell and Dr. Nydam helped with discussions and manuscript editing. Chapter 5 has been published as Simões, T. R., M. W. Caldwell, A. Palci and R. L. Nydam. 2017. Giant taxon-character matrices: Quality of character constructions remains critical regardless of size. Cladistics 33: 198-219. I contributed with the development of the theoretical background, the phylogenetic character revisions, the phylogenetic analysis and the manuscript writing. My co-authors equally contributed to the discussions, expanding the theoretical concepts and manuscript editing. Chapter 6 is currently accepted for publication as Simões, Caldwell, Tałanda, Bernardi, Palci, Vernygora, Bernardini, Mancini & Nydam. The Origin of Squamates Revealed by a Middle Triassic Lizard from the Italian Alps. Nature. I contributed with the data collection, dataset construction, specimen redescription and phylogenetic analysis, and also wrote most of the manuscript. Dr. Bernardi, Mancini and Bernardini perform the synchrotron CT scan of the specimen, Dr. Palci helped with the CT scan segmentation of the skull of the specimen, O. v Vernygora helped with molecular alignments and figure editing, and Dr. Caldwell and Dr. Nydam supervised the project, helped with anatomical interpretations and discussions. 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 DEDICATION To my wife, Fernanda. My greatest source of intellectual inspiration. vii ACKNOWLEDGEMENTS I am greatly thankful for the support provided to me since the very first stages of this project by my supervisor, Dr. Michael Caldwell and our collaborator Dr. Randall Nydam. Dr. Caldwell conceptualized this project several years ago, and I was given the great honour and satisfaction of executing it. I am also grateful for the numerous inspiring discussions on homology and the evolution of lizards and snakes with both Dr. Caldwell and Dr. Nydam. I also thank the financial support provided to me by the two PhD scholarships I received during the last five years: the Vanier Canada Graduate Scholarship and the Izaak Walton Killam Memorial Scholarship. I like to thank the numerous discussions I have had with several people during the course of my PhD, including Alexander Kellner, Sebastián Apesteguía, Julia Desojo, Marisol Montellano- Balesteros, Jacques Gauthier, Gabriela Sobral, Aaron LeBlanc, Oksana Vernygora, Rodrigo Figueiredo, Taissa Rodrigues, Mateusz Talanda, Ilaria Papparella, Paulina Jimenez-Huidobro, Alessandro
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