3D analysis of hip joint mobility and the evolution of locomotor abilities in Miocene hominoids

286 Pages·2013·8.45 MB·English

by  Ashley S. Hammond

3D ANALYSIS OF HIP JOINT MOBILITY AND THE EVOLUTION OF
LOCOMOTOR ABILITIES IN MIOCENE HOMINOIDS

A Dissertation
Presented to
The Faculty of the Graduate School
at the University of Missouri

In Partial Fulfillment
Of the Requirements for the Degree
Doctor of Philosophy

By
ASHLEY S. HAMMOND
Dr. Carol V. Ward, Dissertation Supervisor

December 2013
© Copyright by Ashley S. Hammond 2013
All Rights Reserved
The undersigned, appointed by the dean of the Graduate School,
have examined the Dissertation entitled
3D ANALYSIS OF HIP JOINT MOBILITY AND THE EVOLUTION OF
LOCOMOTOR ABILITIES IN MIOCENE HOMINOIDS
Presented by Ashley S. Hammond
A candidate for the degree of
Doctor of Philosophy
And hereby certify that, in their opinion, it is worthy of acceptance.

Carol V. Ward

J. Michael Plavcan

Gregory Blomquist

Scott Maddux

Casey Holliday
This work is dedicated to Kristina Aldridge and Cheryl Hill, for their support.
ACKNOWLEDGMENTS

I have had the great fortune to work with amazing people these last few years.
First and foremost, Carol Ward, who has been a loyal and enthusiastic advisor. Carol’s
research has guided my own work and I thank her for helping me achieve virtually every
goal I had upon entering graduate school. My committee-- Mike Plavcan, Greg
Blomquist, Scott Maddux, and Casey Holliday-- deserve special recognition for helping
me develop my ideas and articulate them clearly. My committee has been a great
strength to me and I can’t thank them enough for their support, encouragement, and
difficult questions.

All faculty in the Integrative Anatomy group have been instrumental to my
success, including Kris Aldridge, Cheryl Hill, Matt Ravosa, Rachel Dunn, and Kevin
Middleton. In particular, I am deeply appreciative of Kevin’s extreme patience for my
never-ending questions related to R and phylogenetic quantitative methods.
I have countless insightful and generous colleagues which have made this
experience more rewarding, and here I name just a few. I consider my field work with
Meave Leakey to be one of the most memorable and rewarding times of my life and I
cannot fully express how grateful I am for the experience. David Begun and Laszlo
Kordos have shown extreme generosity in sharing the Rudapithecus fossils, and I am
fortunate to have been given access and permission to study the fossils from
Rudabánya. Laura MacLatchy’s work has been inspirational and the foundation for
much of my own work, and I have greatly valued Laura’s advice and feedback at multiple
stages during my dissertation. I must thank everyone at the Institut Català de
Paleontologia for allowing me to join their field crew for a season and study the original
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fossils under their care. In particular, I thank Salvador Moyà-Solà, David Alba, Isaac
Casanovas-Vilar, and Sergio Almécija. I will not soon forget the late nights in Barcelona
philosophizing about Miocene ape evolution over beers with David and Sergio.
In addition, all graduate and undergraduate students in the University of Missouri
Integrative Anatomy program have enriched my life and my work! I cannot thank our
undergraduate research assistants enough for processing what must have seemed like
endless amounts of scan data. I sincerely hope that Sarah Swartz, Zach Winkler, and
Nik Koscielniak did not find themselves in need of glasses and with chronic ulnar nerve
pain from too many hours using PolyWorks. Rachel Menegaz, Kim Congdon, Ian
George, Henry Tsai and Elizabeth Moffett have made outstanding grad student
colleagues and I look forward to being colleagues with them for years to come. Henry, I
thank you for the frequent light-hearted banter and your love of mammals.
In the last year, I have found a place in Anatomical Sciences at Stony Brook
University. Even as a graduate student, I have been welcomed as a colleague into one
of the most successful, evolutionary-focused anatomy departments in the country. I
have valued my interactions with each of the faculty and postdocs, and must particularly
thank Bill Jungers, Susan Larson, Brigitte Demes, and John Fleagle for discussions
relevant to my dissertation.
I am indebted to the museum curators and collection managers who allowed me
to study the collections under their care. I thank Eileen Westwig, Judy Chupasko,
Lyman Jellema, Loic Costeur, Lorenzo Rook, Darrin Lunde, Bill Stanley, Dave Hunt,
Michael Hiermeier, Steven van der Mije, Emma Mbua, and Kyalo Manthi for facilitating
my collection visits. I am also greatly appreciative for the advice and PolyWorks
software support offered by Angelia Payne, Jack Cothren, and the Center for Advanced
Spatial Technologies (CAST) at the University of Arkansas.
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I have been very fortunate to work with many wonderful veterinarians. Doug
Armstrong and Julie Napier allowed me collect pilot data at the Omaha Henry Doorly
Zoo. I attribute this early data collection on hominoids as being instrumental to receiving
grants later. Everyone at the Omaha Zoo, including Doug and Julie, were incredibly
gracious and facilitated my work in every way possible. I must also thank Kathy Brasky,
Robert Baker, Chris Hanley, Beth Hammond, Nancy Schultz-Darken, Fawn Stroud,
Elizabeth Strobert, and all veterinary staff at the zoos and National Primate Research
Centers I have worked with. All of you exposed me to an entirely different perspective
than I would ordinarily encounter in my research.
Debbie Allen and Mark Hannink in the MU Life Sciences Fellowship program
always expressed enthusiasm for my research and made annual reporting a genuinely
fun experience. I thank the administrators and staff at my granting agencies, including
Leslie Aiello (Wenner-Gren Foundation), Paddy Moore (LSB Leakey Foundation), and
Carolyn Ehardt (National Science Foundation, Award BCS 1232393).
To my friends and family—I couldn’t have done it without you and apologize for
not being available often these last few years. I have missed birthdays, weddings,
holidays, and plenty of good times to work on my dissertation, and I thank you for being
so understanding. My parents and my sister Aimee have been incredible parents to
Beast (an extremely challenging dog!) while I collected data and, I’m ashamed to admit,
for quite some time after data collection was finished. Sergio—thank you for
understanding that dissertations are not supposed to be fun and trying your best to make
me have fun anyways. A number of friends hosted me while collecting data, and I must
thank Sam Sargeant, Darice Westphal, Erin Dougherty, Susan Dougherty, Dave Leslie,
and Alex Townsend in particular for their generosity. Darice Westphal offered me more
emotional support than I am probably capable of giving anyone myself, and for that I
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cannot thank her enough. I hope I can repay all of you for your deeds these last few
years.

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TABLE OF CONTENTS

ACKNOWLEDGMENTS .................................................................................................. ii
TABLE OF FIGURES .................................................................................................... xii
ABSTRACT ................................................................................................................... xv
CHAPTER 1: INTRODUCTION ...................................................................................... 1
CHAPTER 2: BACKGROUND ........................................................................................ 7
Range of motion and adaptation ........................................................................... 7
Extant anthropoid locomotor behaviors ................................................................. 9
Gibbons (Hylobates) and siamangs (Symphalangus) ........................................... 10
Orangutans (Pongo pygmaeus, Pongo abelii) ....................................................... 10
Western lowland gorillas (Gorilla gorilla gorilla) and mountain gorillas (G.
beringei beringei) ..................................................................................................... 11
Chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) ........................... 12
Colobines (Subfamily Colobinae) ............................................................................. 12
Cercopithecines (Subfamily Cercopithecinae) ....................................................... 13
Spider monkeys (Ateles) ............................................................................................ 14
Howler monkeys (Alouatta) ....................................................................................... 15
Capuchin monkeys (Cebus sp.) ............................................................................... 16
Locomotor adaptation................................................................................................. 16
Extant anthropoid hip joint range of motion ..........................................................18
Influence of soft tissue morphology on hip mobility ...............................................20
Hip joint capsule and capsular ligaments ................................................................ 21
Ligamentum teres femoris ......................................................................................... 22
Labrum .......................................................................................................................... 24
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Muscles ........................................................................................................................ 25
Osteological correlates of suspension ..................................................................28
Features of the femur and pelvis attributed to high hip mobility .......................... 28
Features of the femur and pelvis that increase span at the foot ......................... 33
Hominoid evolution ...............................................................................................34
Fossil evidence of locomotor evolution in Miocene apes ..................................... 34
Problems in understanding evolution of fossil apes .............................................. 49
Modeling joint function ..........................................................................................50
Model validation .......................................................................................................... 52
Table 2.1 Comparison of percentages of adult locomotion in extant anthropoids
.....................................................................................................................54
Table 2.2 Broad locomotor categorization of extant anthropoids considered in
this study ......................................................................................................55
Table 2.3 Comparison of published values for anthropoid hip joint mobility.. ...56
CHAPTER 3: IN VIVO RANGE OF MOTION .................................................................67
Objective ..............................................................................................................67
Sample .................................................................................................................68
Methods ...............................................................................................................69
Measurements ............................................................................................................. 69
Quantitative Analyses................................................................................................. 72
Phylogenetic regression and ordinary least squares regression ......................... 73
Results .................................................................................................................75
ANOVA results ............................................................................................................ 75
Tukey’s HSD pairwise comparisons ........................................................................ 75
Spearman correlations and regressions.................................................................. 76
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