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Patterns of Morphological Evolution in the Skull of Turtles: Contributions from Digital Paleontology, Neuroanatomy and Biomechanics

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Patterns of morphological evolution in the skull of turtles: contributions from digital paleontology, neuroanatomy and biomechanics Dissertation der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen zur Erlangung des Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) vorgelegt von M.Sc. Gabriel S. Ferreira aus Santa Bárbara d’Oeste/ Brasilien Tübingen 2019 Gedruckt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Eberhard Karls Universität Tübingen. Tag der mündlichen Qualifikation: 27.05.2019 Dekan: Prof. Dr. Wolfgang Rosenstiel 1. Berichterstatter: Prof. Dr. Madelaine Böhme 2. Berichterstatter: Prof. Dr. Max C. Langer In nature we never see anything isolated, but everything in connection with something else which is before it, beside it, under it and over it Johann Wolfgang von Goethe Doubt is not a pleasant condition, but certainty is absurd François Voltaire i Ferreira – Patterns of morphological evolution in the skull of turtles Acknowledgements I am very grateful to my supervisor Max Langer, who offered me a space in his lab for the past ten years and immensily contributed to shape my career path until now. Max not only helped me think through paleo-problems, but also about career options and personal matters, always being present and giving support when I needed. I also thank my PhD co- supervisor in Tübingen, Prof. Dr. Madelaine Böhme, who accepted and welcomed me at the Senckenberg Institute and Universität Tübingen for a whole year, offering me not only a space to work, but also interesting discussions on various subjects. I am very grateful to my “unofficial” co-supervisor, PD Dr. Ingmar Werneburg, who has supported me from the beginning of my PhD, helping already when I was writing my doctoral research project and now, during this agitated last year. He granted me an invaluable amount of time during my stay in Tübingen, and also after I returned to Brazil, through several Skype calls and email exchange. All the conversations and discussions with them were very productive and insightful and, no doubt, they shaped not only the way I think about paleontology, evolutionary biology and science, but also about my life. I would also like to thank Juliana Sterli, who was my co-supervisor during my Master dissertation and with whom I spent six months working in Trelew. I learned a lot with you and you also had an importat role in defining my career. To you, my sincere thanks! I gratefully acknowledge FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) for granting me the funding for my PhD project and my stay at the Universität Tübingen (grant numbers 2014/2539-5 and 2016/03934-2) and support by the Center for Biodiversity Documentation (Centro para Documentação da Biodiversidade), Department of Biology, FFCLRP, University of São Paulo, Brazil. This thesis constitutes part of the project 'Core-facility for the conservation of scientific documentation: biological collections and high technology research in comparative morphology' (CT-INFRA 01/2013), financed by the Funding Authority for Studies and Projects (FINEP), Ministry of Science, Technology, Innovations and Communication, Brazilian Federal Government. ii Ferreira – Patterns of morphological evolution in the skull of turtles I acknowledge the contribution of the following colleagues for discussion, collaboration, reviewing, collection or facility access, etc.: A. C. Arruda-Campos (Monte Alto, Brazil), A. Tröscher (Tübingen, Germany), A. Kupfer (Stuttgart, Germany), A. Rincón (Caracas, Venezuela), A. Solórzano (Caracas, Venezuela), B. Simpson (Chicago, USA), C. A. Francisco (Monte Alto, Brazil), C. Mehling (New York, USA), C. Pfaff (Viena, Austria), D. J. Button (London, UK), D. Silva, (Monte Alto, Brazil), D. Brinkman (New Haven, USA), D. Schwarz (Berlin, Germany), D. Kizirian (New York, USA), E. Cadena (Bogotá, Colombia), E. Almeida (Ribeirão Preto, Brazil), F. A. Carbonaro (Bauru, Brazil), F. V. Iori (Monte Alto, Brazil), G. S. Bever (New York, USA), I. G. Danilov (St. Petersburg, Russia), I. Ruf (Frankfurt, Germany), J. Prochel (Tübingen, Germany), J. Ziermann (Washington DC, USA), J. Cundiff (Boston, USA), J. Carrillo (Zürich, Switzerland), J. Hinz (Tübingen, Germany), J. Kriwet (Viena, Austria), K. Tighe (Washington DC, USA), K. Mahlow (Berlin, Germany), L. E. Sabino (Araraquara, Brazil), L. Vonnahme (New York, USA), M. S. Magalhães (Manaus, Brazil), M. de la Fuente (San Rafael, Argentina), M. Sánchez-Villagra (Zürich, Switzerland), P. S. R. Romano (Viçosa, Brazil), R. Garbin (Fribourg, Switzerland), R. P. Ghilardi (Bauru, Brazil), R. Schoch (Stuttgart, Germany), R. Diaz Jr. (Riverside, USA), R. Hirayama (Tokyo, Japan), R. Butler (Birmingham, UK), R. Benson (Oxford, UK), R. Diogo (Washington DC, USA), S. Bandyopadhyay (Kolkata, India), S. Evers (Fribourg, Switzerland), S. Chapman (London, UK), S. Lautenschlager (Birmingham, UK), S. S. Nihei (São Paulo, Brazil), S. Walsh (Edinburgh, UK), T. Kohlsdorf (Ribeirão Preto, Brazil), T. Scheyer (Zürich, Switzerland), V. Volpato (Frankfurt, Germany), W. G. Joyce (Fribourg, Switzerland), W. Maier (Tübingen, Germany). To all the PaleoLab past and present members for the uncountable hours of coffee breaks, Cantina do Seu Zé, bandejões, PaleoNatais and the endless and coolest (and sometimes also useless) discussions on an increadible diversity of topics. In particular, to my friends Tomate, Wafa, Julio, Simone, Mariela, Squirtle, Bruninho, Schumy, Fezão, Marquinho, Roque, Annie, who were part of my life during (very) different stages, and to the more recent coming, Bruna, Gustavo, Fellipe, Silvio, João, Chico, Gabriel, you became very rapidly an important part of my life. To all my Tübingen colleagues and friends, in particular Márton, Eme, Alex, Antonio, Anna, Priscila, Zeina, Melina, you helped me to have a great time during my German year. I am very thankful to all of you! iii Ferreira – Patterns of morphological evolution in the skull of turtles To all my friends in Americana, Nacim, Diógenes, Giu, Danilo, Gui, and in Ribeirão Preto, from Tiana’s lab, in particular Melissa, Gäelle, Nathalia, Aline, Gaga. To Gabriela, for your partnership and love during all these years, you have a special place in my heart, no matter what. To all 45ers, in particular Frango, Mestre, Ursa, Ket, Luigi, Zuado, Canjica, Garfo, MX, Paulinha, all of you. To Letícia, who notwithstanding I’ve found (or you found me?) in this troubled period, readly offered me happiness, companionship and love, pure love. Finally, to all my family, in particular my parents Ana and Gil, my grandparents, Vó Cida, Vó Peê and Vô Nésio, and my tia Cristina, who always supported and believe in me, since I was a little kid, with a lot of hair on my head. Thank you all, very much, for your companionship, friendship, and love, lots of love, through all those years! O amor da gente é como um grão, morre e nasce trigo, vive e morre pão iv Ferreira – Patterns of morphological evolution in the skull of turtles English Abstract In the current framework of Evolutionary Biology, Paleontology has an important role to play. The fossil record represents a fundamental aspect in studies on the evolution of morphology, since from its study it is possible to retrieve reliable data on many pertinent aspects, e.g., rates of evolution, the role of mass extinctions on species diversity, the polarity of character changes, and a glimpse into morphotypes that don’t exist nowadays. At the same time, new tools and methods, such as computed tomography, digital reconstructions, and Finite-Element Analysis, known collectively as digital or virtual paleontology, have brought novel possibilities on how to formulate and answer paleontological questions. In this Thesis, I employ digital paleontological techniques to analyze the patterns of morphological evolution of the skull of turtles and, based on these data, I provided novel interpretations of the neuroanatomical and functional relations of specific cranial traits to the whole skull architecture. Organized in four chapters, an overview of the osteological, muscular, developmental, and functional evolution of the craniocervical system of turtles is provided. By applying computed tomography and other 3-D digital methods, I performed reconstructions of the jaw adductor musculature and the neuroanatomical structures of one of the earliest turtles, Proganochelys quenstedti, to investigate the early evolution of the adductor chamber and the sensorial anatomy in this taxon. A new extinct side-necked turtle species, Yuraramirim montealtensis, is described, and its brain, inner ear, and neurovascular system were reconstructed in order to provide an account of the paleoneuroanatomy in one of the major turtle groups, the pleurodires. For the last chapter, I performed Finite-Element Analyses based on 3-D digital models of a series of extinct and extant taxa, together with hypothetical simulated morphotypes, to analyze the relation between muscle stress distribution patterns and skull architecture in the group. A scenario of progressive correlation between neck and skull morphological modifications is presented, which may be related to the great diversification of turtles during the Jurassic. Keywords: computed tomography; digital endocast; Finite-Element Analysis; Testudinata; skull v Ferreira – Patterns of morphological evolution in the skull of turtles Resumo em Português No estado atual da Biologia Evolutiva, a Paleontologia possui um importante papel. O registro fossilífero
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    www.nature.com/scientificreports OPEN An early bothremydid from the Arlington Archosaur Site of Texas Brent Adrian1*, Heather F. Smith1, Christopher R. Noto2 & Aryeh Grossman1 Four turtle taxa are previously documented from the Cenomanian Arlington Archosaur Site (AAS) of the Lewisville Formation (Woodbine Group) in Texas. Herein, we describe a new side-necked turtle (Pleurodira), Pleurochayah appalachius gen. et sp. nov., which is a basal member of the Bothremydidae. Pleurochayah appalachius gen. et sp. nov. shares synapomorphic characters with other bothremydids, including shared traits with Kurmademydini and Cearachelyini, but has a unique combination of skull and shell traits. The new taxon is signifcant because it is the oldest crown pleurodiran turtle from North America and Laurasia, predating bothremynines Algorachelus peregrinus and Paiutemys tibert from Europe and North America respectively. This discovery also documents the oldest evidence of dispersal of crown Pleurodira from Gondwana to Laurasia. Pleurochayah appalachius gen. et sp. nov. is compared to previously described fossil pleurodires, placed in a modifed phylogenetic analysis of pelomedusoid turtles, and discussed in the context of pleurodiran distribution in the mid-Cretaceous. Its unique combination of characters demonstrates marine adaptation and dispersal capability among basal bothremydids. Pleurodira, colloquially known as “side-necked” turtles, form one of two major clades of turtles known from the Early Cretaceous to present 1,2. Pleurodires are Gondwanan in origin, with the oldest unambiguous crown pleurodire dated to the Barremian in the Early Cretaceous2. Pleurodiran fossils typically come from relatively warm regions, and have a more limited distribution than Cryptodira (hidden-neck turtles)3–6. Living pleurodires are restricted to tropical regions once belonging to Gondwana 7,8.