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BURGESS-DISSERTATION-2018.Pdf ONTOGENETIC CHANGES IN LIMB BONE STRUCTURAL PROPERTIES AND LOCOMOTOR BEHAVIOR IN PAN by Mary Loring Burgess A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland June, 2018 ABSTRACT As our closest living relatives, chimpanzees have often served as models to help reconstruct early hominin behavior. However, despite documented behavioral variation at the species and subspecies level, we still know little about how skeletal variation relates to behavior among living chimpanzees. This is especially important in light of increasing evidence that early hominins engaged in a variety of locomotor modes involving mixtures of arboreal and terrestrial behaviors: previous studies have often focused on broad taxonomic and behavioral groups, but closely-related modern taxa with subtle behavioral differences may provide better models. Studies of ontogenetic trajectories within groups can also serve as "natural experiments" for testing the relationship of morphology to known behavioral changes with age while controlling for genetic heritage. This study compares skeletal morphology with field observational behavioral data among bonobos and the individual subspecies of common chimpanzee. Aspects of skeletal morphology previously hypothesized to reflect locomotor behavior, including bone lengths, articular proportions, phalangeal curvature and dorsal metacarpal and metatarsal ridge (DMR) morphology, and cross-sectional structural properties (e.g. inter- limb strength proportions, diaphyseal shape ratios), were compared both across adult P. paniscus and P. troglodytes subspecies and during ontogeny. These results were then contextualized in existing data on locomotor behavior frequencies in these same taxa. Bone lengths and articular proportions were hypothesized to primarily reflect genetic differences and thus mainly vary along phylogenetic lines, while internal cross-sectional geometry, phalangeal curvature, and the DMR were predicted to show greater concordance with behavior regardless of phylogenetic relationships. ii Results suggest that, even at these narrow taxonomic levels, length and articular proportions primarily vary along taxonomic lines, distinguishing P. paniscus from other Pan, while cross-sectional geometry and phalangeal curvature show more differences between P. troglodytes subspecies and are more consistent with differences in frequencies of locomotor behavior. Dorsal metacarpal ridge morphology seemed to be related both to body size and to behavior. This increased understanding of the relative importance of genetic inheritance and developmental plasticity in the production of adult skeletal features in Pan informs both our understanding of the functional anatomy of living hominoids and our interpretations of morphological variation in fossil hominins. Advisor: Christopher Ruff, Johns Hopkins University School of Medicine Dissertation Committee: Adam Sylvester, Johns Hopkins University School of Medicine Shannon McFarlin, The George Washington University Sandra Inouye, Midwestern University iii ACKNOWLEDGEMENTS This work would not have been possible without the guidance and support of many very generous people. First and foremost, a huge amount of credit is due to my advisor, Chris Ruff. Chris has guided me through every step of this process, from the initial pilot data collection (as part of a whirlwind tour of Europe with our collaborator, Juho-Antti Junno) through data analysis and writing up, and his advice and assistance have been invaluable. His patience and understanding as I dealt with some fairly challenging life circumstances have also made all the difference over the past few years. Chris has many, many responsibilities, yet somehow always manages to give his students the time and attention we need. I couldn’t have asked for a better, more supportive advisor, and am extremely grateful. Practically speaking, this project would not have been possible without a number of collections, curators, and other helpful folks. Thanks to the staff at the Royal Museum for Central Africa in Tervuren and the Powell-Cotton Museum in Birchington, and to Christophe Boesch, Department of Primatology, and Jean-Jaques Hublin, Department of Human Evolution, Max Planck Institute in Leipzig, for access to specimens in their care. Special thanks also to Zewdi Tsegai and David Plotzki at the Max Planck Institute for helping me with CT scans and generally showing me the ropes. I’d also like to thank my committee members Shannon McFarlin, Adam Sylvester, and Sandra Inouye, who gave up several weeks of their time during the busiest part of the year to read through this dissertation. Their comments and suggestions have materially improved the quality of this work, and I am grateful for the insight they have provided. In addition to being a part of my committee, Shannon was an invaluable iv sounding board and source of information about dental development and age estimation during the early stages of this project. Thanks to the FAE faculty and students, past and present, for their support and friendship. Special shout-out to my first year lab-mates Nicky Squyres and Heather Ahrens, for seeing me through some tough times and for answering my increasingly panicky text messages over the past few months with grace and calm. I could always count on Megan Holmes, my FAE big sister, for a much-needed dose of sanity (and a really silly nickname). Thanks to Francois Gould and Evan Garofalo, who made sure I felt welcome from the moment I stepped in the door. I also have to extend a special thanks to Arlene Daniel, our Administrative Manager, without whom I’m convinced nothing would ever get done. I also have to thank my family for everything they’ve done for me through what must have seemed to them like an endless project. My parents and sister have been there for me in every possible way over the past few years. I can confidently say that this dissertation would never have been finished without the unwavering support of my mom, who went above and beyond the call of duty to help me when I needed it the most. My dad was always there to listen when I needed a sympathetic ear, and we spent many hours commiserating about the writing process. Carl and Cindy, my uncle and aunt, also stepped in to help me through a particularly rough period, for which I’ll always be grateful, and my sister Clara has been a constant source of delight. Lastly, thanks to my wonderful partner Claudia, who continues to make me extremely happy every single day. v TABLE OF CONTENTS Abstract ............................................................................................................................... ii Acknowledgements ............................................................................................................ iv Table of Contents ............................................................................................................... vi List of Tables ..................................................................................................................... ix List of Figures ................................................................................................................... xii 1 Introduction and research design .............................................................................1 1.1 Rationale ........................................................................................................... 1 1.2 Organization of dissertation .............................................................................. 3 1.3 Conceptual framework ...................................................................................... 4 1.3.1 Genetic and ecological variation in Pan ............................................ 4 1.3.2 Morphological variation in Pan ......................................................... 8 1.3.3 Behavioral variation in Pan ............................................................. 16 1.4 Bone morphology and plasticity ..................................................................... 26 1.4.1 Differential plasticity of skeletal structural properties ..................... 26 1.4.2 Ontogeny as a “natural experiment” ................................................ 34 1.5 Research design and Hypotheses .................................................................... 41 2 Materials and methods ...........................................................................................47 2.1 Sample............................................................................................................ 47 2.2 Morphological data ......................................................................................... 49 2.2.1 External linear measurements .......................................................... 49 2.2.2 Cross-sectional geometry ................................................................. 52 2.2.3 Metacarpal, metatarsal, and phalangeal curvature ........................... 58 2.2.4 DMR height and angle ..................................................................... 62 2.2.5 Body mass ........................................................................................ 63 2.3 Dental aging .................................................................................................... 68 2.3.1 Radiographs and scoring .................................................................. 68 2.3.2 Taxonomic and habitat effects on age estimation ...........................
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