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Skeletal Growth and Life History Evolution in Wild and Domesticated Mammals

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Skeletal Growth and Life History Evolution in Wild and Domesticated Mammals Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2015 Skeletal growth and life history evolution in wild and domesticated mammals Geiger, Madeleine Other titles: Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr.sc.nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Madeleine Geiger von Ermatingen TG Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-121297 Dissertation Published Version Originally published at: Geiger, Madeleine. Skeletal growth and life history evolution in wild and domesticated mammals. 2015, University of Zurich, Faculty of Science. Skeletal Growth and Life History Evolution in Wild and Domesticated Mammals Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Madeleine Geiger von Ermatingen TG Promotionskomitee Prof. Dr. Marcelo R. Sánchez-Villagra (Leiter der Dissertation und Vorsitz) Dr. Robert Asher Prof. Dr. Marcus Clauss Prof. Dr. Richard Schneider Prof. Dr. Christoph Zollikofer Zürich, 2015 To my family Skeletal Growth and Life History Evolution in Wild and Domesticated Mammals Madeleine Geiger Universität Zürich, 2015 Title page image: Extreme size variation within one species, exemplified by a St. Bernard dog and a Chihuahua. The markers of dental and skeletal growth which I was investigating throughout my PhD thesis are illustrated: closure of the cranial sutures and synchondroses, eruption of the permanent dentition into occlusion, and closure of the postcranial growth plates. Artwork by Madeleine Geiger, 2015, inspired by the Natural History Museum Bern. Contents Acknowledgements 1 Summary 2 Zusammenfassung 4 Introduction 7 CHAPTER 1 Heterochrony and post-natal growth in mammals – an examination of growth plates in limbs 23 CHAPTER 2 No change in the sequence of dental, skeletal, and sexual maturity in dogs due to domestication 57 CHAPTER 3 Cranial suture closure in domestic dog breeds and relations to skull anatomy – a comparison with human patterns 73 CHAPTER 4 Comparison of growth trajectories among ancient and modern breeds rejects a paedomorphic pattern of change associated with dog domestication 89 Conclusions and perspectives 109 Appendix 113 Curriculum Vitae 140 Acknowledgements (Anthropologisches Institut und Museum der Universität Zürich), Frieder Mayer and Nora I am greatly indebted to Prof. Dr. Marcelo R. Lange (Museum für Naturkunde, Berlin), Sánchez Villagra. His enthusiasm and genuine Loïc Costeur (Naturhistorisches Museum interest in my work, as well as his continual Basel), Marc Nussbaumer and Paul Schmid support, encouragement and patience made (Naturhistorisches Museum Bern), Daniela my time as a PhD student rewarding and en- Kalthoff (Naturhistoriska Riksmuseet, joyable. As a mentor, he not only taught me an Stockholm), Heinz Furrer (Paläontologisches incredible amount and the ability to think crit- Institut und Museum der Universität Zürich), ically and broadly, but also provided me with Renate Lücht (Populationsgenetik, Christian- the freedom to develop and pursue my own Albrechts-Universität zu Kiel), Marianne ideas. Prof. Dr. Hugo Bucher is thanked for Haffner and Barbara Oberholzer (Zoologisches being a supportive director. Further, I would Museum der Universität Zürich), Erich Weber like to thank the SNF and the Forschungskredit (Zoologische Schausammlung der Universität of the Universität Zürich for financial support Tübingen), and Caroline Lang (Zoologische and my committee Robert Asher, Marcus Staatssammlung München). Clauss, Richard Schneider, and Christoph As important as professional support, how- Zollikofer for their advice. ever, is also the personal facet of the work- Sincere thanks go to my co-authors and ing environment. In this respect I would like colleagues who gave me great methodolog- to thank especially Anna Sanson Barrera and ical as well as conceptual support and took Alexandra Wegmann for being fantastic of- them time for stimulating discussions: Loïc - Costeur, Analia M. Forasiepi, Manuela Fuchs, fice-mates and good friends who have al ways supported me. I would further like to Karine Gendron, Sinah Haussman, Patrick thank all the past and present members of the R. Kircher, Daisuke Koyabu, Johann Lang, Palaeontological Institute and Museum, who I Madlen Stange, Ingmar Werneburg, Florian had the opportunity to meet and who have not Willmitzer, Laura A.B. Wilson. Further, this only been supporting colleagues but also be- thesis would not have been possible without came good friends with whom I could spend the administrative help of Heike Götzmann enjoyable hours. and IT-support of Heini Walter. Many thanks Last but most importantly, heartfelt thanks also to them. to my family, my boyfriend, and all my friends My gratitude further goes to the curators and outside the PIM for being incredibly support- institutions that kindly and generously granted ive, patient and loving. me access to their collections: Marco Milella 1 Summary epiphyses separated throughout life, which probably represent the derived state. The second chapter concerns patterns of Not much is known about the generation of growth plate closure and tooth eruption in do- morphological disparity by means of differ- mestic dogs. It has been argued that the do- ential patterns of growth during postnatal on- mestication process has altered the sequence togeny in mammals. This PhD thesis aims at of dental maturity, skeletal maturity, and sex- elucidating aspects of growth, generation of ual maturity due to altered environmental con- variability and disparity, and their association ditions. The aim of this study was to test this to life history traits by investigating specific hypothesis by investigating a comprehensive markers of growth (tooth eruption, growth sample of domestic dog skeletons and teeth. plate closure, and suture closure) in mammals The analyses show that there is no change in in general and domestic dogs in particular. the sequence of dental, skeletal, and sexual Domestic dogs are tremendously variable, al- maturity in dogs due to domestication and that, though one single species, and relatively well despite their great variability, domestic dogs investigated. They thus comprise an ideal are wolf-like in terms of the here investigated study subject for addressing these questions. processes of somatic and sexual maturation. The study of skeletal and dental growth and In the third chapter, it was investigated alterations of skeletal morphology through- whether bulldog-like domestic dog breeds, out the domestication of dogs, in conjunction which are characterised by a relatively short with knowledge about variation in life history and broad skull with a dorsally rotated ros- traits, can not only improve our understanding trum, exhibit similar patterns of suture and of the ontogeny and domestication of dogs, synchondrosis closure than exhibited in some but also shed light on the mechanisms of do- human syndromes associated with a ‘bull- mestication in general and the evolution of dog-like’ small face and additionally prema- other species that live and evolve under a spe- ture fusion of certain craniofacial sutures and cial selective pressure leading to rapid evolu- cranial base synchondroses, e.g., achondropla- tion, e.g. on islands. sia, Apert syndrome, and Crouzon syndrome. The first chapter deals with heterochron- Comparisons of the relative amount of closing ic patterns (shifts in timing) of growth plate and closed sutures and synchondroses in adult closure in mammals which display a broad individuals showed that bulldog-type domes- spectrum of limb specialisations, coupled tic dog breeds have significantly higher clo- with different locomotor strategies and habi- sure scores than non-bulldog-type breeds and tat occupation. A common general pattern of that domestic dogs have significantly higher growth plate closure sequence was found, but closure scores than the wolf. These results in- one that is universal neither among species dicate that similar mechanisms might act on nor in higher-order taxa. Observed patterns the generation of the bulldog-type skull con- indicate that growth plate closure sequence is formations in humans and domestic dogs, but more strongly influenced through phylogenet- at the same time emphasise the importance of ic inertia than through locomotor adaptations. biomechanical influences on patterns of su- It was also found that heterochronic shifts in ture closure in domestic dogs. the growth plate closure sequence of marsupi- The fourth chapter examines the con- als occur with a higher rate than in placentals, troversial hypothesis of an association of which is in contrast with the more limited var- retardation of growth (heterochrony: paedo- iation in timing and morphospace occupation morphosis) with the generation of the typical typical for marsupial development. Moreover, skull shape in domestic dogs, with the latter unlike placentals, marsupials maintain many being ‘paedomorphic wolves’. We conducted 2 the first geometric morphometric analysis domestic dogs overlap, these trajectories are of ontogenetic series of dogs from different similar to each other, indicating similar pat- historical periods of domestication (modern, terns of growth. Therefore, we did not find premodern, prehistoric), serving to provide evidence for heterochrony
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