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An Anatomical and Genetic Analysis of the Ceboid Lumbosacral Transition and Its Relevance to Upright Gait

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An Anatomical and Genetic Analysis of the Ceboid Lumbosacral Transition and Its Relevance to Upright Gait AN ANATOMICAL AND GENETIC ANALYSIS OF THE CEBOID LUMBOSACRAL TRANSITION AND ITS RELEVANCE TO UPRIGHT GAIT A thesis submitted to the Kent State University Honors College in partial fulfillment of the requirements for University Honors by Allison L. Machnicki May, 2012 Thesis written by Allison L. Machnicki Approved by ________________________________________________________________, Advisor __________________________________________, Chair, Department of Anthropology Accepted by _____________________________________________________, Dean, Honors College ii TABLE OF CONTENTS LIST OF FIGURES v LIST OF TABLES vi ACKNOWLEDGEMENTS vii CHAPTER I. INTRODUCTION 1 A Brief Review of the Lumbosacral Spine 1 II. BACKGROUND OF ANATOMY AND DEVELOPMENT 4 Ligamentous Anatomy of the Lumbosacral Spine 4 The Development of the Lumbosacral Spine 5 Hox genes 6 III. OSTEOLOGY AND ANATOMY 10 Purpose 10 Methods 11 Osteology and Metric Data 11 Dissection 14 Results 15 Osteometrics of the Museum Sample 19 Conclusions 21 IV. GENETICS 23 Purpose 23 Methods 23 Genomic DNA 23 Polymerase Chain Reaction (PCR), Cloning, and Sequencing 24 Results 28 Discussion 32 V. SUMMARY AND FINAL CONCLUSIONS 33 WORKS CITED 34 iii APPENDIX 1. APPENDIX A: Full Alignment 39 iv LIST OF FIGURES Figure 1. Regions of Hox gene expression in the vertebral column 8 Figure 2. Measurements 13 Figure 3. Ligamentous Drawings 18 Figure 4. Relative Sacral Height 19 Figure 5. Plot of Alar Width Compared to Centrum Width 21 Figure 6. HoxD11 Enhancer Sequence 24 Figure 7. A Phylogenetic Comparison of Transcription Factor Binding Sites in Sequenced Specimens 30 v LIST OF TABLES Table 1. Osteological Measurement Definitions 12 Table 2. The Observed Conservation of Each Species 28 Table 3. Transcription Factor Binding Site Definitions 31 vi ACKNOWLEDGEMENTS I would like to thank my advisor Dr. C. Owen Lovejoy for directing this study and for being the ultimate inspiration for a young anthropologist. Without his incredible knowledge and time this project would not have been possible and I would never have discovered my love for the study of anatomy. I would also like to thank him for always supporting me, encouraging me, and remembering that I played oboe. I would like to thank Dr. Linda Spurlock for assisting with dissections, helping with research, and providing drawings. I am also thankful to her for reading drafts, for her unbelievable and unending support throughout this project, and for making this project exceedingly enjoyable to undertake. I would like to thank Dr. Chi-hua Chiu for guiding the genetics portion of this study, for the use of her lab, and for serving on my defense committee. I would like to thank Dr. Elizabeth Howard and Dr. Douglas Kline for serving on my defense committee. I would like to thank Daniel Sprockett for training me in the genetics lab, running procedures for me, and helping me troubleshoot; without him the genetics portion of this project would not have been possible. I would like to thank Yohannes Haile-Selassie for selecting me as his Adopt-A- Student intern at the Cleveland Museum of Natural History where I began this project. I would like to thank Lyman Jellema for access to the Hamann Todd Osteology collection, vii photography, x-rays, and help finding cadavers. I would like to thank Chris Vineyard and Mary-Ann Raghanti for dissection specimens. I would like Chris Flask, John Jesberger, and Matt Griswold for MRIs. I would like to thank Steve Ward for his support and funding in this project. I would like to thank Kelly Droney and Caitlin Sheesley for their help with this project. I would like to thank Gerri Machnicki and Peter Koby for their unending encouragement and reading drafts. I would also like to thank Peter Koby for helping with figures. I would like to thank the following institutions: The Kirtlandia Society, The Cleveland Museum of Natural History, and Kent State University. viii CHAPTER I INTRODUCTION A Brief Review of the Lumbosacral Spine: The human trunk is characterized by three distinct curvatures: a cervical lordosis, a thoracic kyphosis, and a lumbar lordosis. In humans, the cervical portion has an erect atlas and axis, the lumbar column is long, and the sacrum is broad and short (Ishida, 2006). In contrast, the chimpanzee has only two curvatures: a cervical lordosis and a thoracic-lumbar kyphosis (Ishida, 2006). Furthermore, in chimpanzees the atlas (C1) is tilted on the axis (C2), the lumbar column is short, and the sacrum is narrow and long (Ishida, 2006). During human bipedalism the weight of the body is supported solely by the hindlimb and vertebral column, rather than the forelimbs (as in quadrupedalism). Of critical importance is the ability to lordose the lower lumbar spine—that is, to reverse the direction of spinal curvature in such a way as to allow the body's center of mass to be placed forward over the hip and knee joints. Only with lordosis could our ancestors have adopted a striding gait that did not involve the bent hip and bent knee joints seen in most primates that walk bipedally (McCollum et al., 2009). Such a gait pattern is exhibited by African apes which have almost completely eliminated lower spinal mobility by shortening their spine and “submerging” their most caudal lumbar(s) between the dorsally elongated ilia of their pelvis. 1 2 Human erect walking is a unique specialization among primates and even among mammals. While many other mammals are upright during locomotion, they retain this posture because they are saltatory (hopping) or suspensory. The human gait pattern is not shared with any other primate and requires many unique features in the pelvis to have evolved in our ancestors. The hominid pelvis was undergoing changes for adaptations to bipedality 3 to 4 million years ago, when hominid brains were only slightly larger than those of chimpanzees (Lovejoy, 2009). The earliest hominid fossil with definitive anatomical adaptations for bipedality is Ardipithecus ramidus, dating to 4.4mya (Lovejoy, 2009). On average, Old World monkeys possess seven lumbar vertebrae while New World monkeys possess from four to seven lumbar vertebrae with atelines having four or five. Great apes have three to four lumbars, and the lesser apes have five lumbar vertebrae (Schultz and Strauss, 1945). Modern Humans have five lumbar vertebrae with occasional variations of four or six lumbars (Schultz and Strauss, 1945). The Most Recent Common Ancestor (circa 7-10 mya) of African apes and hominids is argued to have retained a long lower spine (most likely 6 lumbars) (McCollum et al., 2009). Such mobility would have permitted more effective bipedality than is seen in extant apes. On the other hand, a long lumbar column, with more lumbar vertebrae, might have been mechanically less capable than a short one for bridging behaviors or climbing in the manner of extant apes (Sanders, 1997). In humans (hominids), the most caudal lumbar vertebra is free from constriction by contact with the dorsal ilia, suggesting that reduction in iliac height and an increase in 3 the breadth of the sacrum are early adaptations to a bipedal locomotion. Freeing of the most caudal lumbar vertebra by iliac height reduction and sacral broadening therefore could have been the earliest adaptations to upright walking in hominids (McCollum et al., 2009). By contrast, in Old World monkeys and apes the most caudal lumbar is partially trapped by dorsally extended ilia, restricting lordosis and preventing bipedality without a bent-hip-bent-knee (BHBK) gait (Lovejoy & McCollum, 2010). Interestingly, while no New World monkeys are terrestrial or bipedal, one prominent group, the atelines (Ateles, Brachyteles, Lagothrix, Alouatta; family Atelidae; Wildman et al. 2009) have flexible and highly enervated prehensile tails, with which they suspend themselves while frequently also using their forelimbs (Personal communication – K. Strier). This posture places their lower spines in lordosis, a lumbar posture similar to that exhibited in hominids. Some physical characteristics of the lumbar column in atelines and hominids, then, are convergent. In this thesis, I explore this hypothesis of convergent evolution and subsequent impacts on locomotion in hominids by using morphometrics and genetic analysis in a range of primates with focus on members of the Atelidae. CHAPTER II BACKGROUND OF ANATOMY AND DEVELOPMENT Ligamentous Anatomy of the Lumbosacral Spine: In humans, multiple ligaments stabilize the articulation of the vertebral column with the pelvis. The lumbosacral ligament connects the lower portion of the most caudal lumbar vertebra to the lateral surface of the sacrum, blending with the sacroiliac ligament (Gray, 1977). It is short, thick, and triangular. The sacroiliac ligament is made up of anterior and posterior parts (Gray, 1977). The anterior portion is made of thin bands that connect the anterior surface of the sacrum to the ilium (Gray, 1977). The posterior portion is composed of strong interosseous fibers and is positioned in the posterior depression between the sacrum and ilium (Gray, 1977). The human iliolumbar (IL) ligament helps stabilize the lumbosacral spine on the pelvis (Luk, 1986). It passes horizontally from the transverse process of the most caudal lumbar vertebra to the crest of the ilium in front of the articulation of the sacroiliac joint (Gray, 1977). The iliolumbar ligament is formed by collagenation of the fibers of the quadratus lumborum muscle (Pun, 1987). Studies have emphasized the importance of the IL in restraining extension and lateral bending of L5 and in maintaining stability of the lumbosacral junction (Pool, 2001). The IL has been shown to be present in humans and rhesus 4 5 macaques but absent in other quadrupeds (i.e. rats, rabbits, and dogs) with a horizontal spine (Pun, 1987). The IL is also present in New and Old World primates including Ateles, Brachyteles, Alouatta, langurs, and gibbons (personal observation: this study). In the rhesus macaque, the IL connects the last, and occasionally the second-to-last, lumbar transverse process to the adjacent iliac wing (Pun, 1987).
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