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Palacký University Olomouc Palacký University Olomouc Faculty of Science Department of Zoology and Laboratory of Ornithology Developmental modularity of cerebral tissues in the evolution of avian locomotion using high resolution imaging and geometric morphometric Ph.D. Thesis Vincent Beyrand Supervisors: Prof. Stanislav Bureš Dr. Paul Tafforeau Olomouc 2018 Promoter Prof. Stanislav Bureš Palacký University in Olomouc Faculty of Science Department of Zoology and Laboratory and Laboratory of Ornithology 17. listopadu 50 Olomouc 771 46 Czech Republic Dr. Paul Tafforeau European Synchrotron Radiation Facility Beamline ID19 38 avenue des Martyrs 38000 Grenoble Opponents Dr. Stig Walsh Department of Natural Sciences National Museums of Scotland Chambers Street Edinburgh EH1 1JF Prof. Eric Buffetaut Centre National de la Recherche Scientifique UMR 8538 Ecole Normale Supérieure de Paris 24 rue Lhomond 75231 Paris CEDEX 5 « Life always find a way » Michael Crichton I declare that this thesis is my original work and has not been submitted for the purpose of obtaining the same or any other academic degree earlier or at another institution. My contribution to each to each of the chapters comprising this work is expressed through the autorship order of the included chapters and author’s contribution statements complementing the chapters. Chapter 4 and 6 are/is reproduced with kind permission from the publishers Olomouc, 31st January 2018 ………………………………. Vincent Beyrand Bibliographic identification Name and surname of the author: Vincent Beyrand Title: Developmental modularity of cerebral tissues in the evolution of avian locomotion using high resolution imaging and geometric morphometric Type of thesis: PhD thesis Department: Department of Zoology and Laboratory of Ornithology, Palacký University Supervisors: Prof. Stanislav Bureš Dr. Paul Tafforeau Study program: P1527 Biology Study field: Zoology Year: 2017 Abstract Archosaurs is one of the vertebrate group with the longest history and the oldest origin. Through their long evolutionary history, they developed a large variability of size, morphological features and locomotion behaviours. Flight is a particular behaviour that has been developed twice independently by archosaurs during their evolution. As a complex locomotory behaviour, flight requires advanced cognitive capabilities in order to deal with all the information necessary for a proper locomotion. As the center of processing of information and selection of appropriate response, brain is an important structure to study in order to understand how cerebral capacities in archosaurs evolved in parallel of flight evolution. Because of its position at the root of birds, Archaeopteryx from the Jurassic of Germany, is a very important taxon as it is considered as the oldest form having developed active flight capabilities in the avian lineage. The study of the features showed the different Archaeopteryx specimens add information on how flight capabilities evolved in birds. Another important point of this evolutionary process is the mechanism leading to the appearance cerebral of features related to flight. In this respect, Haslzkaraptor escuillei, a small dromaeosaur from the Cretaceous of Mongolia, is a key specimen, showing brain characters very similar to Archaeopteryx, despite the fact that it was clearly not a flying animal and probably not having flying ancestors. 1 This thesis focuses on the study on the general shape of the endocast and the evolution of its coiling along the development of flight within archosaurs. A new Mongolian dromaeosaur, with particular features revealing a new ecomorphology and particular cerebral characteristics have also been studied during this thesis, with a particular focus on the neurovascular sytem into the snout, dentition organisation and brain anatomy. Because of the rareness and delicacy of fossil specimens bringing information about the origin of flight, their studies does not allow the use of destructive methods. As those fossils cannot be fully extracted from their rock slab, we need special methods in order to access as much as possible information on their anatomical characters for understanding their living behaviour. For that, we used X-ray imaging methods available at the European Synchrotron Radiation Facility, which are considered nowadays as the golden standard for non-destructive 3D investigation of fossils. Along archosaurs evolution toward flying forms, endocasts show an increase of coiling as well as of infilling level by the brain itself. Basal archosaurs such as crocodiles show an elongated and low- filled endocast, reflecting the primitive condition observed in lepidosaurian. Non-maniraptoriform dinosaurs and then Maniraptoriforms show two successive events of coiling increase, but only small maniraptoriforms suggest an increase of infilling. In crocodiles and non-maniraptoriforms dinosaurs, coiling and low infilling are independent from body size, contrary to maniraptoriforms for which small specimens do present a higher filling level than large sized specimen, for similar coiling values. Finally, birds show a total decoupling of those two characters and size. This general pattern is observed during crocodilian embryonic development, for which coiling and infilling decrease along ontogeny. This suggest a serie of progenetic events, associated with a general size reduction, along archosaurs lineages toward flying forms which was leading to cerebral shape unlocking the cerebral capabilities for flight. Further studies would require more research on shape modification of the different brain structure, by defining which character of brain anatomy influence flight specialisation, fossil reconstruction of crushed fossil in order to have a more accurate view of the process originating flight. Keywords : archosaur, endocast, coiling, infilling, developmental heterochrony, paedomorphosis, flight origin 2 Number of pages : 235 Language : English © Vincent Beyrand 2018 3 4 Content Abstract (in English)…………………………………………………………………………………….1 Chapter I General introduction……………………………………………………………………….7 I-Evolution of archosaurs……………………………………………………………………….9 I-A-Evolutionary history of archosaurs and origin of birds……………………….……9 I-B-Development of flight within Archosauria……………………………………….13 I-C-Influence of developmental heterochrony within Dinosauria…………………….14 II-Paleoneuroanatomy…………………………………………………………………………16 II-A-Brain organisation……………………………………………………………….16 II-B-History of paleoneuroanatomy…………………………………………………..24 II-C-Review of brain anatomy in bird-line through the evolution of flight……………27 Chapter II Bi-energy imaging for neuroanatomical features………………………………………31 I-Generalities and history of imaging methods………………………………………………...33 II-Use of contrast agent and bi-energy scans…………………………………………………..34 III-Propagation phase contrast………………………………………………………………...39 IV-Combined use of K-edge/bi-energy and propagation phase contrast imaging techniques….39 V-Application to neuroanatomy……………………………………………………………….42 Chapter III Fossils…………………………………………………………………………………….49 I-Compsognathus longipes…………………………………………………………………….51 II-Halszkaraptor escuillei……………………………………………………………………..56 III-Archaeopteryx……………………………………………………………………………...64 Chapter IV Synchrotron scanning reveals amphibious ecomorphology in a new clade of bird-like dinosaurs…………………………………………….....73 Chapter V Geometric morphometrics analysis and cerebral information reflecting evolutionary history of archosaurs and the development of flight………………………91 I-Geometric morphometrics and application in paleontology………………………...93 II-Three-dimensional geometric morphometric analysis……………………………..93 III-Qualitative accuracy of endocranial representativity of brain anatomy…………113 Chapter VI Developmental evolution of the brain enabled archosaurian flight………………………………………………………………….119 5 Chapter VII Progenetic scenario within Archosauria……………………………………………..195 Co-author affiliation…………………………………………………………………………………..201 Bibliography………………………………………………………………………………………….203 Acknowledgments……………………………………………………………………………………236 Abbreviations: ESRF: European radiation Synchrotron Facility; ESRF collection: Specimen preserved at the European Synchrotron Radiation Facility; LFAC: La Ferme aux Crocodiles, Pierrelattes, France; TL: Thierry Loeb, Echirolles, France; ENS: Ecole Normale Supérieure, Lyon, France; MHN Grenoble: Museum d’Histoire Naturelle, Grenoble, France; MNHN: Museum National d’Histoire Naturelle, Paris, France; CCEC: Centre de Conservation et d’Etude des Collections, Lyon, France; Peaugres: Safari de Peaugres, Peaugres, France. 6 Chapter I General introduction 7 8 I-Evolution of archosaurs I-A-Evolutionary history of archosaurs and origin of birds Archosaurs find their origin during the early Triassic, after the split with Lepidosauria, their sister taxa within Diapsida (Romer 1966, Reig 1970, Benton and Clark 1988). Along their evolutionary history, they developed particular posture from sprawling to erect and semi-erect (Edwards 1977, Parish 1987, Reilly and Elias 1998). This variation of limb position influenced the large amount of locomotory behaviour that have been developed within this lineage (quadrupedal/bipedal, terrestrial/aquatic/flying,…) leading to a large range of body shape (Hutchinson and Gatesy 2000, Hutchinson 2006, Bates and Schachner 2012, Allen et al. 2013). Archosaurs are only represented by living crocodilians and birds nowadays, but they were also represented by dinosaurs, pterosaurs and fossil forms of crocodylomorphs (Figure I-1). Crocodilians are the most primitive
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