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Understanding Primate Mandibular Symphyseal Fusion: Function, Integration, and Ontogeny

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Understanding Primate Mandibular Symphyseal Fusion: Function, Integration, and Ontogeny UNDERSTANDING PRIMATE MANDIBULAR SYMPHYSEAL FUSION: FUNCTION, INTEGRATION, AND ONTOGENY A DISSERTATION SUBMITTED TO THE FACULTY OF THE UNIVERSITY OF MINNESOTA BY RYAN P. KNIGGE IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY DR. KIERAN P. MCNULTY December 2017 @ Ryan P. Knigge 2017 Acknowledgements First, I am deeply indebted to my advisor and mentor, Kieran McNulty, for many years of patience and support. He opened my eyes to exciting and innovative areas of scientific research and has challenged me to become a better student of anthropology, biology, and statistical practices. I am also particularly grateful for my committee members, Martha Tappen, Michael Wilson, and Alan Love, for so many interesting discussions and insights over the years. I thank the Department of Anthropology and my many friends and colleagues within for years of emotional and academic support. Many data collection and field work trips were funded through department block grants. Surely without these contributions, I would not have been able to succeed as a graduate student. I would like thank the previous and current managers of the Evolutionary Anthropology Labs at the University of Minnesota, John Soderberg and Matt Edling, for access to the collections and technical support. Without their help and generosity, data collection and analysis would not have been possible. I thank the University of Minnesota for supporting my research in many ways during my graduate school career. Portions of my data collection were funded through the University of Minnesota Graduate School Thesis Research Travel Grant. Dissertation writing support was provided through the Doctoral Dissertation Fellowship. I thank the curators and staff of the many institutions that let me visit and research in their collections: Field Museum of Natural History, Chicago, Illinois; Smithsonian i National Museum of Natural History, Washington, D.C.; American Museum of Natural History, New York City, New York; Duke Lemur Center, Durham, North Carolina; National Museums of Kenya, Nairobi, Kenya; and Institut Catala de Paleontologia Miguel Crusafont, Sabadell, Spain. I would also like to thank Drs. Christopher J. Vinyard and Lauren Halenar and also Jason Massey for sharing their 3D models of primate skulls. I would also like to thank Dr. Christopher J. Vinyard for sharing EMG data that were collected with support from NSF. I thank the Smithsonian's Division of Mammals (Dr. Kristofer Helgen) and Human Origins Program (Dr. Matt Tocheri) for the scans of USNM specimens used in this research (http://humanorigins.si.edu/evidence/3d- collection/primate). I am profoundly indebted to my friends and family, particularly my parents and partner, Allison. I could not have completed this journey without their unconditional personal support and patience over the years. ii Abstract Understanding the function-shape relationships of the primate masticatory apparatus has been a focus of anthropological research for many decades. One particular feature of the masticatory apparatus, mandibular symphyseal fusion, is investigated in this work because symphyseal fusion has the potential to provide important information on masticatory function and mandibular fragments are often preserved in the fossil record. Regardless of the attention this anatomical feature has received, a complete understanding of the underlying mechanisms driving the evolution of symphyseal fusion remains elusive. The research presented in this dissertation tackles this dilemma by investigating the functional, integrative, and ontogenetic elements of symphyseal fusion. Function and morphology are linked through innovative approaches using the burgeoning geometric morphometric toolkit to challenge previously held notions about mandibular symphyseal fusion and generate new hypotheses. Ultimately, this work acknowledges similar underlying mechanisms for symphyseal fusion in different primate lineages which were previously thought to be different, questions the utility of symphyseal fusion for reconstructing evolutionary relationships of primates, and finds potential evidence for the independent evolution of symphyseal fusion within the crown anthropoid clade. iii Table of Contents Acknowledgements ............................................................................................................ i Abstract ............................................................................................................................. iii List of Tables ................................................................................................................... vii List of Figures ................................................................................................................... ix 1 Introduction .....................................................................................................................1 1.1 Overview of the masticatory apparatus ..................................................................... 2 1.1.1 Structure of the masticatory apparatus ............................................................... 2 1.1.2 Jaw kinematics and chewing cycle ..................................................................... 5 1.2 Methods overview: Geometric morphometrics ......................................................... 9 1.2.1 Procrustes superimposition ............................................................................... 10 1.2.2 Application of geometric morphometrics in this study .................................... 13 1.3 Importance of research on mandibular symphyseal fusion ..................................... 17 2 Function and fusion of the mandibular symphysis in living and extinct primates ......................................................................................................................19 2.1 Introduction ............................................................................................................. 19 2.1.1 Masticatory activity and loading regimes ......................................................... 22 2.1.2 The function of mandibular symphyseal fusion ............................................... 26 2.1.3 Symphyseal fusion in fossil lineages ................................................................ 29 2.1.4 Study goals ....................................................................................................... 33 2.2 Materials and methods ............................................................................................ 35 2.3 Results ..................................................................................................................... 50 2.3.1 Masticatory muscle activity and mandibular shape .......................................... 50 2.3.2 Testing hypotheses of strength and stiffness for symphyseal fusion................ 58 2.3.3 Inferring masticatory function in fossil primates ............................................. 64 2.4 Discussion ............................................................................................................... 72 2.4.1 EMG patterns and mandibular shape ................................................................ 72 2.4.2 Strength vs. stiffness models for symphyseal fusion ........................................ 78 2.4.3 Partial vs complete symphyseal fusion ............................................................. 81 iv 2.4.4 Masticatory function and symphyseal fusion in fossil primates....................... 82 2.5 Conclusions ............................................................................................................. 88 3 Mandibular symphyseal fusion and the wishboning motor pattern ........................90 4 Morphological integration of the skull and the evolution of symphyseal fusion ...........................................................................................................................93 4.1 Introduction ............................................................................................................. 93 4.1.1 Mandibular symphyseal fusion in primates ...................................................... 93 4.1.2 The relationship between the wishboning motor pattern and loading regime .. 96 4.1.3 Evolution of the wishboning motor pattern ...................................................... 97 4.1.4 Mandibular fusion and the WMP as an Evolutionary Stable Configuration .. 103 4.1.5 Evolutionary impact of mandibular symphyseal fusion ................................. 105 4.1.6 Study goals ..................................................................................................... 107 4.2 Materials and methods .......................................................................................... 110 4.3 Results ................................................................................................................... 119 4.3.1 Analysis of the WMP and skull shape ............................................................ 119 4.3.2 Comparisons of skull shape between primates with and without the WMP .. 124 4.3.3 Patterns of craniomandibular integration associated with the WMP ............. 129 4.4 Discussion ............................................................................................................. 138 4.4.1 Wishboning motor pattern and skull morphology .......................................... 138 4.4.2 Morphological integration of skull components as an ESC ........................... 143 4.4.3 Interpreting
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