Expression of Fluctuating Asymmetry in Primate Teeth: Analyzing the Role of Growth Duration

Expression of fluctuating asymmetry in primate teeth: Analyzing the role of growth duration.

Dissertation

Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of the Ohio State University

Sarah Abigail Martin, M.A.

Graduate Program in Anthropology

The Ohio State University

2013

Dissertation Committee:

Dr. Guatelli-Steinberg, Advisor

Dr. Scott McGraw

Dr. Paul Sciulli

Dr. Dawn Kitchen

Sarah Abigail Martin

2013

Abstract

This dissertation furthers our understanding of the association between growth duration and developmental noise (DN) by examining fluctuating asymmetry (FA) in a non-sexually selected and a sexually selected structure. FA occurs as small, random deviations from bilateral symmetry without any directionality between sides. Extended periods of growth may provide a ‘window of opportunity’ for growing body structures to accumulate perturbations resulting in elevated DN, manifested as FA. In comparison to other mammalian species, primates exhibit prolonged growth. Within the primate order, growth periods lengthen from prosimians to apes and humans. Although prolonged growth periods can be advantageous, lengthening of the growth period may provide the opportunity to accumulate deviations from symmetry. An association between growth duration and DN has yet to be studied across the primate order. This dissertation tested if and to what extent growth duration was associated with dental FA in primates.

This potential association between growth duration and FA was first examined in the non-sexually selected first molar. First molar FA was compared between species based on crown formation times (CFTs) and life history (LH) schedules to test the hypothesis that species with prolonged CFTs or LH schedules would express greater first molar FA relative to species with shorter CFTs or LH schedules. The results generally lend support to the hypothesis; however, not all comparisons are statistically significant. ii

An additional aim was to elucidate the mechanism(s) which underlie the

association between FA and sexually selected structures. Sexually selected structures are

prone to exhibiting elevated FA because they may be destabilized by directional

selection. The primate canine has been given as one example of a sexually selected

structure prone to expressing elevated FA. It is possible that the mechanisms believed to

explain elevated canine FA in primates may not be associated with the destabilization of

developmental processes but rather with the fact that males of sexually dimorphic species

grow their canines for a longer period of time relative to their female counterparts. Two

approaches were used in testing for an association between FA and sexual selection.

First, canine FA was compared between males and females of a species. Generally, males of sexually dimorphic species expressed greater canine FA but not all comparisons were statistically significant. To further test this association, male canine FA was evaluated through linear regressions and controlled comparisons among males of different species.

Linear regression results indicated that canine growth duration more closely predicted canine FA than variables representing sexual selection. Controlled comparisons that included great apes support the hypothesis that prolongation of growth is associated with elevated FA. An association between growth duration and FA is further supported in some but not all comparisons between males of different monkey species.

Because anthropologists, and other scholars, use FA as an indicator of developmental stress, understanding what factors are associated with FA is essential to accurately intrepreting FA data. The results of this dissertation lend support to the hypothesis that growth duration contributes to dental FA in both a non-sexually selected and a sexually selected structure. iii

DEDICATION

I dedicate this dissertation to my mother, Christine, my father, Andrew, and my brother, Daniel. Without your love, support, and encouragement I would not have made it this far.

ACKNOWLEDGEMENTS

I wish to thank my advisor, Dr. Debbie Guatelli-Steinberg, for her intellectual support, encouragement, and enthusiasm. I am also grateful to my other dissertation committee members, Dr. Paul W. Sciulli, Dr. W. Scott McGraw, and Dr. Dawn Kitchen, for their guidance and support, as well as Dr. Gary Schwartz for providing unpublished data on dental growth of great apes. I would also like to extend my gratitude to my fellow graduate students who served as a source of support through our shared experiences.

I thank everyone who provided access to the primate collections used in this dissertation: Judith Chupasko (Museum of Comparative Zoology, Harvard University),

Lyman Jellema (Cleveland Museum of Natural History), Darrin Lunde (National

Museum of Natural History), Bill Stanley (Field Museum), Martha Tappen (Tappen

Collection, University of Minneapolis), and Eileen Westwig (American Museum of

Natural History). This dissertation would not have been possible without the support from the Wenner-Gren Foundation (Grant #Gr8395), National Sigma Xi, and The Ohio

State University’s Sigma Si Chapter, Critical Difference for Women Program, Graduate

School, and Department of Anthropology.

Finally, I am indebted to my family and friends for their love and support. I especially thank Daniel Martin, Bradley Vile, Denise Fickes, Christina Leach, Krystle

Gnatz, Whitney and Matthew Senn, Jennifer Spence, Jennifer Everhart, and Jesse

Fuhrman for sharing in the joys and growing pains of life. Lastly, I thank my parents,

Andrew and Christine, for always being a source of love, guidance, and support.

VITA

June 2000 ...... Lower Cape May Regional High School

2004...... B.S. Biological Sciences, Rowan University

2006...... M.A. Anthropology, The Ohio State University

2007-2011 ...... Graduate Teaching Associate, Department of Anthropology, The Ohio State University

2011-present ...... Lecturer, Department of Anthropology, The Ohio State University

Publications

Martin SA, Guatelli-Steinberg D Sciulli PW. (2011). Relationships among crown formation time, fluctuating asymmetry, and linear enamel hypoplasia in gibbons and gorillas. Presented at the 80th Annual Meeting of the American Association of Physical Anthropologists, Minneapolis, Minnesota. American Journal of Physical Anthropology 144 (S52): 207.

Martin SA, Guatelli-Steinberg, D, Sciulli PW, Walker, PL. (2008). Brief Communication: Comparison of Methods for Estimating Chronological Age at Linear Enamel Formation on Anterior Dentition. American Journal of Physical Anthropology 135(3): 362-365.

Fields of Study

Major Field: Anthropology

vii

TABLE OF CONTENTS

Abstract ...... ii

Dedication ...... iv

Acknowledgements ...... v

Vita ...... vii

List of Tables ...... xiv

List of Figures ...... xvii

Chapter 1: Introduction ...... 1

Objectives ...... 5

Hypotheses ...... 7

Hypothesis #1...... 7

Hypothesis #2...... 8

Hypothesis #3...... 10

Significance...... 11

Chapter 2: Literature Review – Theoretical Context ...... 14

Description and Causes of Fluctuating Asymmetry ...... 18

Elevated Fluctuating Asymmetry: A Measure of Increased Developmental Noise

...... 20

Directional Selection, Fluctuating Asymmetry, and Sexually-Selected Structures ...26

Growth Processes and Fluctuating Asymmetry ...... 31 viii

Growth Duration and Fluctuating Asymmetry ...... 35

Filling in the Gaps ...... 38

Chapter 3: Literature Review – Estimating Fluctuating Asymmetry ...... 41

Validating the Data Prior to Calculating Fluctuating Asymmetry...... 43

Measurement Error ...... 44

Forms of Asymmetry ...... 46

Type and Number of Structures ...... 49

Wear and Damage ...... 52

Structure Size ...... 53

Indices and Analysis: Fluctuating Asymmetry ...... 56

Fluctuating Asymmetry Indices ...... 56

Recommendations Given in the Literature for Statistical Analysis of Fluctuating

Asymmetry ...... 63

Chapter 4: Material and Methods ...... 69

Materials ...... 69

Sample Selection of Non-human Primate Species ...... 69

Taxonomy Considerations ...... 70

Sample Size ...... 71

Methods...... 74

Variables ...... 74

Data Collection ...... 83

Analytical Phase ...... 87

Summary ...... 93 ix

Chapter 5: Fluctuating Asymmetry of Primate First Molars: Association with Growth

Duration ...... 94

Introduction ...... 94

Stage One Description ...... 95

Stage One Description ...... 96

Results ...... 99

Stage 1 ...... 99

Discussion ...... 109

Stage 1 ...... 109

Results II ...... 115

Stage 2 ...... 115

Discussion ...... 121

Stage 2 ...... 121

Summary ...... 122

Chapter 6: Extending the Test of the Association Between Growth Duration and Dental

Fluctuating Asymmetry ...... 124

Introduction ...... 124

Predictions of Hypothesis 1b ...... 127

First Set of Comparisons ...... 127

Second Set of Comparisons ...... 130

Results ...... 131

Maxillary First Molars ...... 132

Mandibular First Molars ...... 140 x

Discussion ...... 144

Great Apes: Life In the Slow Lane ...... 147

Folivorus and Frugivorous: Old World Monkeys ...... 149

Linear Enamel Hypoplasia, Fluctuating Asymmetry, and the WOV Hypothesis

...... 150

Conclusions ...... 152

Chapter 7: Canine Fluctuating Asymmetry: A Comparisons Between Males and Females

...... 154

Introduction ...... 154

Objectives and Hypothesis ...... 156

Canine Dimorphism Index ...... 157

Testing Hypothesis 2...... 159

Stage 1 ...... 159

Stage 2 ...... 163

Results ...... 163

Stage 1 ...... 164

Stage 2 ...... 169

Discussion ...... 181

Conclusion ...... 185

Chapter 8: Fluctuating Asymmetry of the Male Primate Canine ...... 187

Hypothesis 3...... 189

Linear Enamel Formation Times (EFTs) ...... 189

Competition Levels ...... 192 xi

Regression Analysis ...... 193

Linear Regression: Results and Discussion ...... 195

Controlled Comparisons ...... 206

Controlled Comparison Results ...... 209

First Series of Controlled Comparisons: Mean Lateral EFTs of 80% Crown

Height ...... 211

Second Series of Controlled Comparisons: Mean Lateral EFTS of 80% Crown

Height ...... 217

First Series of Controlled Comparisons: Mean Lateral EFTs of 90% Crown

Height ...... 221

Second Series of Controlled Comparisons: Mean Lateral EFTs of 90% Crown

Height ...... 227

Discussion ...... 231

Reprised: Vulnerability to Asymmetry ...... 233

Cebus apella: The Odd Species Out? ...... 236

Size Matters ...... 240

Conclusion ...... 242

Chapter 9: Discussion and Conclusions ...... 245

Summary of Objectives ...... 245

Summary of Hypotheses ...... 247

‘Window of Vulnerability’ ...... 253

So Little Time, Such Great Symmetry ...... 253

Sex Differences in Mandibular Canine FA ...... 255 xii

Growth Processes ...... 262

Dental Indicators of Stress ...... 264

General Overview of Patterns Observed Across Primate Species ...... 264

A Second Look: Dental FA in Great Apes ...... 268

Nutritional Stress ...... 268

Parasites and FA ...... 271

Limitations of Comparisons ...... 273

Conclusions ...... 274

Contribution of this Dissertation to Understanding Dental FA Patterns ...... 276

References ...... 279

Appendix A: Specimen Listings ...... 311

Appendix B: Hypothesis 1a: ANOVA Tables ...... 317

Appendix C: Hypothesis 1b: ANOVA Tables ...... 325

Appendix D: Hypothesis 2: ANOVA Tables...... 329

xiii

LIST OF TABLES

Table 1: Factors Influencing the Presence of Developmental Stability and Developmental

Instability within a Developmental System ...... 16

Table 2: Indices for Fluctuating Asymmetry ...... 58

Table 3: Indices for Measurement Error ...... 66

Table 4: Taxonomic Classification – Changes from 1990s to Present ...... 71

Table 5: Primates Included in the Dissertation Sample ...... 72

Table 6: References and First Molar Crown Formation Times for Testing H1a ...... 75

Table 7: Weaning Ages of Primate Species for Testing H1b ...... 77

Table 8: Mean Lateral Enamel Formation Times for 80% and 90% Crown Height ...... 79

Table 9: Competition Levels of Primate Species Used to Test H3 ...... 82

Table 10: Sample Size and CFTs of Primate Species Used to Test H1a ...... 97

Table 11: Maxillary and Mandibular First Molar FA Results ...... 99

Table 12: F-tests Stage 1, H1a ...... 100

1 Table 13: F-test for M and M1 FA Comparisons...... 113

Table 14: FA Estimates, H1a Stage 2 ...... 115

Table 15: F-test Stage 2, H1a ...... 116

Table 16: Sample Sizes of Primate Species Used to Test H1b ...... 128

Table 17: Weaning Ages of Primate Species Used to Test H1b ...... 131

Table 18: FA Estimates of Maxillary and Mandibular First Molar Crown Area ...... 132 xiv

Table 19: Maxillary and Mandibular F-tests ...... 133

Table 20: ANOVA Tables for Linear Regression Analysis (N=12)...... 143

Table 21: Sample Sizes for Stage 1 of Testing H2 ...... 158

Table 22: Sample Sizes for Stage 2 of Testing H2 ...... 158

Table 23: Maxillary and Mandibular Canine Dimorphism Indices ...... 160

Table 24: Canine FA Estimates – H2, Stage 1 ...... 165

Table 25: F-tests, Stage 1...... 166

Table 26: Results of Comparisons Between Males and Females of Sexually Dimorphic

Species – H2, Stage 1 ...... 169

Table 27: Canine FA Estimates, H2, Stage 2 ...... 170

Table 28: F-tests, Stage 2...... 172

Table 29: Results of Comparisons Between Males and Females of Sexually Dimorphic

Species – H2, Stage 2 ...... 179

Table 30: Mean Lateral EFTs for 80% and 90% Crown Height – New World Monkeys,

Old World Monkeys, and Lesser Apes ...... 190

Table 31: Mean Lateral EFTs for 80% and 90% Crown Height for Great Apes ...... 192

Table 32: Data Used for Linear Regressions (LR) ...... 196

Table 33: Set 1, Linear Regression Results ...... 200

Table 34: Set 2, Linear Regression Results ...... 201

Table 35: Set 3, Linear Regression Results ...... 201

Table 36: Species Used for Controlled Comparisons ...... 207

Table 37: First Series of Controlled Comparisons ...... 208

Table 38: Second Series of Controlled Comparisons ...... 208 xv

Table 39: F-tests for Controlled Comparisons Using Mean Lateral EFTs at 80% Crown

Height ...... 212

Table 40: F-tests for Controlled Comparisons Using Mean Lateral EFTs at 90% Crown

Height ...... 222

Table 41: Results of Comparisons: Same CLs, Different C1 Lateral EFTs ...... 232

Table 42: Results of Comparisons: Different CLs, Similar C1 Lateral EFTs ...... 233

Table 43: Mean Lateral EFTs for 80% Crown Height ...... 257

Table 44: Mean Lateral EFTs for 90% Crown Height ...... 258

Table 45: F-tests for Cebus C1 FA ...... 267

Table 46: First Molar Crown Formation Times, Sample Sizes, and FA Estimates ...... 269

Table 47: F-tests for First Molar FA of Great Apes ...... 270

xvi

LIST OF FIGURES

Figure 1: Relationship Among Developmental Processes ...... 17

Figure 2: Tooth Section Depicting the Relationship of Striae of Retizus to Perikymata

...... 78

Figure 3: Predicted Fluctuating Asymmetry Magnitudes Among Platyrrhines and

Catarrhines ...... 98

Figure 4: Mandibular First Molar FA Estimates of Apes, H1a Stage 1 ...... 103

Figure 5: Maxillary First Molar FA Estimates, H1a Stage 1 ...... 105

Figure 6: Mandibular First Molar FA Estimates, H1a Stage 1 ...... 106

Figure 7: Maxillary and Mandibular FA Estimates, H1a Stage 2 ...... 119

Figure 8: Maxillary First Molar Crown Area FA Results...... 141

Figure 9: Regression Graph for Maxillary Molars ...... 142

Figure 10: Mandibular First Molar Crown Area FA Results ...... 145

Figure 11: Regression Graph for Mandibular Molars ...... 146

Figure 12: Maxillary Canine Dimorphism Index ...... 161

Figure 13: Mandibular Canine Dimorphism Index ...... 162

Figure 14: C1 FA Results for Predictions 2.1 and 2.2, Stage 1 ...... 167

Figure 15: C1 FA Results for Predictions 2.1 and 2.2, Stage 1 ...... 168

Figure 16: C1 BL FA Results for Prediction 2.1, Stage 2 ...... 175

Figure 17: C1MD FA Results for Prediction 2.1, Stage 2 ...... 176 xvii

Figure 18: C1 BL FA Results for Prediction 2.1, Stage 2 ...... 177

Figure 19: C1 MD FA Results for Prediction 2.1, Stage 2 ...... 178

1 Figure 20: C1 and C FA Results for Prediction 2.2, Stage 2 ...... 180

Figure 21: Graph of C1 BL FA (asy) and Lateral EFTs (LEFTS) ...... 198

Figure 22: Graph of C1 MD FA (asy) and Lateral EFTs (LEFTS) ...... 199

Figure 23: Graphs for C1 FA (asy) and Competition Level (cl), Set 1 ...... 202

Figure 24: Graphs for C1 FA (asy) and Canine Dimorphism (cd), Set 1 ...... 203

Figure 25: Graphs for C1 FA (asy) and Competition Level (cl), Set 2 ...... 204

Figure 26: Graphs for C1 FA (asy) and Canine Dimorphism (cd), Set 2 ...... 205

Figure 27: First Series of Controlled Comparisons for 80% Crown Height ...... 209

Figure 28: First Series of Controlled Comparisons H3a, 90% Crown Height...... 210

Figure 29: Second Series of Controlled Comparisons 80% Crown Height ...... 210

Figure 30: Second Series of Controlled Comparisons for 90% Crown Height ...... 211

Figure 31: Results for the First Series of Controlled Comparisons – Mean Lateral EFTs at

80% Crown Height – C1 BL ...... 214

Figure 32: Results for the First Series of Controlled Comparisons – Mean Lateral EFTs at

80% Crown Height – C1 MD ...... 215

Figure 33: Results for the Second Series of Controlled Comparisons – Mean Lateral

EFTs at 80% Crown Height – C1 BL ...... 219

Figure 34: Results for the Second Series of Controlled Comparisons – Mean Lateral

EFTs at 80% Crown Height – C1 MD ...... 220

Figure 35: Results for the First Series of Controlled Comparisons – Mean Lateral EFTs at

90% Crown Height – C1 BL ...... 224 xviii

Figure 36: Results for the First Series of Controlled Comparisons – Mean Lateral EFTs at

90% Crown Height – C1 MD ...... 225

Figure 37: Results for the Second Series of Controlled Comparisons – Mean Lateral

EFTs at 90% Crown Height – C1 BL ...... 229

Figure 38: Results for the Second Series of Controlled Comparisons – Mean Lateral

EFTs at 90% Crown Height – C1 MD ...... 230

xix

CHAPTER 1: INTRODUCTION

Across the primate order, periods of growth lengthen from strepsirrhines, which

erupt their teeth and achieve adult body proportions over short periods of time (Smith

1989; Godfrey et al. 2001), to apes and humans, which require several years of growth to

achieve adult form (Leigh and Shea 1995; Schwartz and Dean 2001). While prolonged

growth periods may be advantageous in some respects (e.g., affording time for learning), they may represent an opportunity for growing body structures to experience

developmental stress and sustain injury to developing systems. Various researchers

(Vrijenhoek 1985; Hallgrimsson 1993, 1995) have hypothesized that longer periods of growth provide the opportunity for growing body structures to accumulate developmental perturbations resulting in deviations from perfect bilateral symmetry. Van Valen (1962)

coined the term ‘fluctuating asymmetry’ (FA) to describe small deviations from bilateral

symmetry that are random with respect to the side that is larger. Despite efforts to test the

association between growth duration and FA in primates (e.g. Nass 1982; Hallgrimsson

1999), this potential association has yet to be tested systematically across the primate

order. This dissertation aims to do so, providing a foundation for interpreting what FA

means in terms of stress, as it is used as an indicator of stress experienced during

development (e.g. Mal et al. 2002; Trotta et al. 2005; Dongen et al. 2009).

Sexually selected structures are suggested to be more prone to expressing elevated

FA relative to non-sexually selected structures because directional selection relaxes the

control mechanisms of development in sexually selected structures so that an increase in

trait expression can occur (Moller 1990; Moller and Pomiankowski, 1993; Watson and

Thornhill 1994). FA in sexually selected structures has therefore been proposed as a signal of quality which can be used by in conflict assessment by competing males and in mate selection by choosy females (Moller, 1993; Moller and Pomiankowski, 1993). The primate canine has been given as one example: males of species with sexually dimorphic

canines tend to exhibit greater FA than males of species with sexually monomorphic

canines (Manning and Chamberlain, 1993).

However, not all studies have found that sexually selected structures exhibit greater

FA than non-sexually selected structures (e.g. Tomkins and Simmons, 1995; Bjorksten et al., 2000; Lens et al., 2002). Furthermore, since the proposal of the FA-sexual selection hypothesis in the 1990s (e.g. Moller, 1990; Moller and Hoglund, 1991; Moller, 1992) there has been a dramatic decrease in the amount of support for the hypothesis (Tomkins and Simmons, 2003). The inconsistent results raise the question as to why some but not all studies find a relationship between sexually selected structures and elevated FA. As such, an additional aim of this study is to determine whether growth duration can explain the association between FA and sexually selected primate canine. The explanation for the association between sexually selected structures and FA may not be limited to the destabilization of developmental processes associated with sexual selection (Moller 1990;

Moller and Pomiankowski, 1993; Watson and Thornhill 1994). Rather, prolonged growth

duration may contribute to the observation that sexually selected structures exhibit elevated FA.

Vrijenhoek (1985) describes the opportunity to accumulate deviations during development as a “window of vulnerability” (WOV). Relative to body structures that take

a short time to form, those structures that take longer to form have a greater WOV to

experience stress and accumulate developmental perturbations, which reduce bilateral

symmetry. If sexually selected structures have prolonged growth periods relative to non- sexually selected structures, then they may also have a greater WOV to accumulate perturbations and express developmental noise, as measured through FA. Therefore, the mechanism that explains the association between sexually selected structures and FA might not be the destabilization of the developmental process associated with sexual selection, but rather a “window of vulnerability” caused by growth prolongation.

In sexually dimorphic primate species, male canines take longer to form than those of females (Swindler et al., 1982; Sirianni and Swindler, 1985; Swindler, 1985;

Schwartz et al. 1999, 2001; Schwartz and Dean 2001; Guatelli-Steinberg et al. 2009). For example, on average Gorilla males grow their canines for almost three years longer than

Gorilla females (Schwartz and Dean, 2001). Thus, male canines may simply have a greater opportunity to accumulate deviations from symmetry resulting in elevated canine

FA relative to those of females. This dissertation aims to elucidate the mechanism(s) that underlie the association between sexually selected structures and FA. However, answering the question of if, and to what degree, duration of canine growth, as assessed

by canine crown formation times, explains the variation observed in canine FA

expression across the primate taxa is complicated.

Directional selection, or selection that tends to favor phenotypes at one extreme of

the phenotypic range, is believed to relax developmental control mechanisms resulting in

a reduction in efficiency and, ultimately, the stability of the developmental system

(Parsons 1992; Palmer 1994; Watson and Thornhill 1994). The relaxation of control mechanisms in structures under intense directional selection is hypothesized as the reason for why sexually selected structures are more prone to developmental perturbations and exhibit elevated FA than non-sexually selected structures (Moller 1990, 1992; Watson and Thornhill 1994; Moller and Swaddle 1997). Sexual selection has not only been

hypothesized to bring about ‘developmental destabilization’ leading to increased FA but

is also associated with prolonged canine crown formation times in sexually dimorphic

primate species (Schwartz et al. 1999, 2001; Schwartz and Dean 2001; Guatelli-Steinberg

et al. 2009). Because ‘developmental destabilization’ and prolonged canine crown

formation are both associated with sexual selection, it is difficult to separate them from

each other in order to adequately address which variable appears to better explain

variation in dental FA.

This dissertation was designed to determine if growth duration is associated with

dental FA in a non-sexually selected structure and to disentangle the potential effects of

‘developmental destabilization’ and prolonged canine crown formation times in male FA,

both of which are associated with sexual selection. Before examining the sexually

selected primate canine, it must first be determined if growth duration is associated with

FA in teeth that are not sexually selected. If a non-sexually selected structure follows the

pattern of FA predicted by WOV (Vrijenhoek, 1985), then it is reasonable to hypothesize

that the same FA pattern would be observed in sexually selected structures.

Objectives

The purpose of this dissertation is to determine the extent to which growth duration is associated with developmental noise in primate teeth. There are important

reasons to investigate developmental instability and examine dental FA.

Developmental instability (DI) is “the inherent noisiness of a developmental

pathway,” (Waddington, 1957, p. 40). The developmental noise (DN) that Waddington

(1957) refers to is the result of all the random, independent events occurring over

developmental time, which have the potential to disrupt the normal trajectory of

development. When the developmental system’s trajectory is disrupted, DN develops,

causing bilateral structures to express non-directional subtle differences referred to as FA.

Branches of biology as well as other disciplines have commonly used departures

from symmetry to estimate the occurrence of processes that disrupt development (e.g.

Parsons, 1990; Livshits and Kobyliansky, 1991; Zakharov, 1994; Hallgrimmson, 1995;

Moller and Swaddle, 1997). A great deal of focus has been given to the association

between FA and fitness (e.g. Moller, 1990; Parsons, 1990; Zakharov, 1992; Palmer,

1996). The general assumption is that individuals who are more fit are better able to

successfully buffer developmental perturbations and achieve the target phenotype relative

to individuals who have reduced fitness (Maynard Smith et al. 1985; Gibson and Wagner,

2000). If an individual is unable to buffer the effects of perturbations, the developmental

trajectory is disrupted resulting in noise that is expressed as FA.

There are advantages to investigating FA in dentition over that of the skeleton

(Goodman and Armelagos, 1989; Goodman and Rose, 1991; Hillson, 1996; Wood, 1996;

Hillson and Bond, 1997). First, unless affected by wear, the size and shape of the tooth does not change after crown formation ceases. Relative to FA in the skeleton, teeth record perturbations experienced throughout the developmental period only rather than during the most recent stage of development or since the last time bone was remodeled.

Additionally, teeth are durable, leading them to be commonly found within paleontological and archaeological assemblages.

In this study, FA is evaluated in two tooth types of non-human primates: the permanent first molar and permanent canine. In the first step of this dissertation, the objective is to determine if growth duration is associated with variation in FA expression in the primate first molar. Since ‘developmental destabilization’ and growth duration are both associated with sexual selection, the sexually dimorphic primate canine cannot be used to initially determine if prolonged growth provides an opportunity for the accumulation of perturbations leading to greater FA. Because the first molar of non- human primates is a non-sexually selected tooth, it can be used to determine if FA expression is influenced by prolonged growth since it is not influenced by

‘developmental destabilization’. First molar FA will be compared across primate species

with varying crown formation times (CFTs) of first molars obtained from the literature

(e.g. Macho, 2001; Smith et al., 2007; Kelley and Schwartz, 2009). In this first step,

males and females of a species are combined because first molar CFTs do not differ between the sexes of a species (Macho, 2001). If growth duration is shown to be

associated with elevated first molar FA, it is hypothesized that growth duration may also

be associated with canine FA.

Canine FA is evaluated through two separate hypotheses. First, canine FA is

compared between males and females of a species in order to examine if males of

sexually dimorphic species express greater canine FA relative to females. However,

comparing male and female canine FA will not provide a clear indication of if canine FA

is associated with ‘developmental destabilization’ or growth duration, or both. To

evaluate ‘growth duration’ and ‘developmental destabilization’ independently, canine FA

is compared among males of different primate species.

Hypotheses

Hypothesis #1

The first hypothesis (H1) is that length of growth duration influences the

expression of FA such that longer periods of growth are associated with elevated FA in a

non-sexually selected structure. H1 is tested in two different phases: H1a and H1b. Both

phases test the hypothesis that primate species with longer growth periods will exhibit a

greater WOV resulting in elevated FA relative to primate species with shorter growth

periods. In the first phase, H1a, first molar CFTs represent the growth variation through

which FA of primate species are compared. The second phase, H1b, uses a continuum of

‘slow’ to ‘fast’ life history (LH) schedules of primates to evaluate if developmental timing is associated with elevated first molar FA.

Primate first molar FA has been examined only in Macaca (Hallgrimsson 1999).

This dissertation examines FA in the first molar of ten catarrhine and three platyrrhine species to explicitly test the hypothesis that variation in growth duration is associated with elevated FA. Using both first molar CFTs and a continuum of LH schedules allows for H1 to be tested through two different but related variables. Dental development has been shown to be closely associated with LH variables across primates (Smith, 1989,

1992, 1994; Macho, 2001; Dean, 2006). Moreover, Macho (2001) demonstrated that the timing of weaning is strongly related to first molar CFTs in anthropoid primates. H1a will be tested using CFTs of primate species. In order to increase the number of species included in the comparison, H1b will be tested using LH schedules and weaning age as proxies for developmental timing.

Hypothesis #2

Hypothesis 2 (H2) is that: 1) within sexually dimorphic anthropoid primate species, FA will be greater in male canines relative to female canines; and 2) within anthropoid primate species with minimal or no canine sexual dimorphism, male and female canines will exhibit similar FA. H2 represents the first step in evaluating dental

FA in a sexually selected structure.

The primate canine is a sexually selected structure whose opportunity to experience developmental perturbations may be influenced by ‘developmental

destabilization’ associated with sexual selection and/or sex differences in canine growth durations also associated with sexual selection. Therefore, H2 does not tease apart the potential effects of ‘developmental destabilization’ and/or the ‘window of vulnerability’

(WOV). Rather, the results of H2 will determine 1) if males of sexually dimorphic species exhibit canine FA that is statistically significantly greater than their female counterparts; and 2) if similar canine FA is expressed by males and females of primate species with minimal or no canine sexual dimorphism. If male canines of sexually dimorphic species do express FA that is statistically significantly greater than female canine FA, then the question becomes: Do canine FA estimates better support the

‘developmental destabilization’ or WOV hypothesis?

If some, but not all, males of sexually dimorphic primate species express statistically significantly greater FA than their female counterparts, an additional question arises: What factor(s) may influence one sexually dimorphic primate species to express canine FA estimates that differ significantly between the sexes, while another sexually dimorphic primate species does not?

An additional component of testing H2 is the use of canine dimensions not influenced by use-related wear. In a previous canine FA study (Manning and

Chamberlain, 1993), FA was determined from the dimension of canine height. Canine height is a dimension susceptible to use-related wear. Because use-related wear does not necessarily occur bilaterally, canine height wear could skew FA estimates. Moreover, significant methodological and statistical advances in the study of FA have occurred since the publication of Manning and Chamberlain’s (1993) paper. FA is greatly

influenced by measurement error (ME) because the distribution of signed FA and ME

display similar statistical properties and are often comparable in magnitude (Smith et al.,

1982; Greene, 1984; Palmer and Strobeck, 1986; Palmer, 1994; Swaddle et al., 1995).

This study will measure canine dimensions that are not affected by use-related wear and includes a step in the methodological protocol to examine wear prior to measurement. The most recent methodological and statistical approaches for FA studies are utilized in this study including performing a two-way mixed model ANOVA and factoring out other forms of asymmetry prior to calculating FA.

Hypothesis #3

Hypothesis 3 (H3) is that males of primate species with similar durations of

canine growth will exhibit similar FA, while males with different durations of canine growth will express different FA magnitudes. Specifically, males with longer durations of

canine growth, as determined by lateral enamel formation times (EFTs) of canines, will

exhibit greater FA relative to males of primate species with shorter periods of growth.

To test this hypothesis a series of controlled comparisons meant to disentangle the

variables of ‘developmental destabilization’ and growth duration are employed. The

strength of sexual selection is represented by competition levels (CL) among males taken

from the work of Plavcan and colleagues (Kay et al., 1988; Plavcan and van Schaik,

1992). Growth duration is represented by canine lateral enamel formation times

(Schwartz and Dean, 2001; Guatelli-Steinberg et al., 2009). The first series of controlled

comparisons is between primate species with different durations of canine growth, but

assigned to the same CL. Under the WOV hypothesis, species with a longer duration of

growth will exhibit greater canine FA; while under the ‘developmental destabilization’

hypothesis, species with the same CL will exhibit similar canine FA. The second set of

controlled comparisons will compare primate species with similar growth durations, but

different CLs. Under the WOV hypothesis, canine FA is expected to be similar when

growth duration is the similar; while under the alternative ‘developmental destabilization’

hypothesis, canine FA should be greater in species assigned to a higher ranked CL.

Controlled comparisons between males of different primate species will allow

‘developmental destabilization’ and WOV to be evaluated separately in the primate

canine. The results of H3 will elucidate if either or both “developmental destabilization”

and WOV play role in canine FA.

Significance

This dissertation contributes to anthropological theory and to the discipline by

attempting to resolve critical questions surrounding what underlies the expression of FA

in both a non-sexually selected and a sexually-selected structure. Because FA is

commonly used as an indicator of stress experienced during development, knowing what

influences or is associated with FA of a morphological structure is essential to accurately

interpreting FA data (e.g.Townsend and Brown, 1980; Manning and Chamberlain, 1994;

Leung and Forbes, 1996, 1997; Roy and Stanton, 1999).

Human anterior teeth are known to vary in CFTs across populations (Reid and

Dean, 2006) and differences in CFTs may exist between some modern humans and

Neanderthals (Guatelli-Steinberg et al., 2005, 2009; Guatelli-Steinberg and Reid, 2008;

Smith et al., 2007; Smith et al., 2010). If growth duration is associated with FA, elevated

FA in one human population relative to another human population may not be due to greater environmental and/or genetic stress as suggested in past studies (e.g. Suarez,

1974; Doyle and Johnston, 1977; Perzigian, 1977; Corruccini et al., 1982). Rather, a longer duration of growth might have permitted a greater window of time to experience developmental perturbations, deviate from bilateral symmetry and express FA.

Associations between FA and growth duration have not been adequately explored within mammalian species and, in particular, among primate species. Through this study, examining a non-sexually selected and sexually selected structure in separate hypotheses, a framework that elucidates what underlies FA expression will be established.

If the variation of FA observed in the non-sexually selected primate first molar is found to be associated with growth duration this result suggests that prolonged periods of growth entail costs to the developmental system, as proposed by Van Valen (1985; 2003).

Furthermore, through determining if there is an association between prolonged growth periods and elevated FA, researchers will be better equipped to interpret FA data when making comparsion within and between populations or species.

Examining FA of the sexually dimorphic primate canine will determine if males of sexually dimorphic species exhibit greater canine FA than their female counterparts.

This project goes a step further and attempts to disentangle the potential effects of

‘developmental destablization’ and prolonged canine growth, both associated with sexual

selection. If developmental timing is found to be associated with DI of the primate canine, then these results could help explain why some studies do not find evidence for the ‘developmental destabilization’ hypothesis (e.g. Bjorksten et al., 2000; Lens et al.,

2002). By offering an opportunity to experience a greater number of perturbations, prolonged periods of growth of some, but not all, sexually-selected structures could account for the inconsistent results in studies of the relationship between FA and sexual selection. This is because some sexually selected structures may result from sex differences in growth rates as opposed to sex differeneces in growth duration.

Finally, primate species represent a strong sample in which to test these hypotheses because of the variation of CFTs, lateral EFTs, and life history schedules observed across the primate order. The intense focus on canine dimorphism over the last few decades has generated a wealth of information on the achievement of canine sexual dimorphism and on the variation that exists across primate species (Leutenegger and

Kelly, 1977; Harvey et al., 1978; Kay et al., 1988; Plavcan and van Schaik, 1992;

Greenfield, 1992; Plavcan, 1993; Plavcan et al., 1995; Thoren et al., 2006; Guatelli-

Steinberg et al., 2009). Such information permits the use of controlled comparisons in order to disentangle ‘development destabilization’ and WOV when examining canine FA.

Overall, the testing of these hypotheses will not only provide a greater understanding of the effects of growth duration on developmental instability, but also produce a more detailed picture of dental FA variation in primate species.

CHAPTER 2: LITERATURE REVIEW – THEORETICAL CONTEXT

Symmetry has long been a topic of interest for biologists, since body plans of many organisms’ exhibit one form or another of symmetry. Structures of bilaterally symmetrical organisms have the possibility of exhibiting three different forms of asymmetry, or the absence of symmetry (Ludwig, 1932; Van Valen, 1962; Leary and

Allendorf, 1988). Directional asymmetry (DA) occurs when a particular character has

greater development on one side of the bilateral plane than on the other (Van Valen,

1962). Several examples of DA are found in bilateral organisms, such as the mammalian

heart. Antisymmetry (AS) occurs in a population of individuals where most are

asymmetric, but it is random as to which side of the organism shows greater development

(Van Valen, 1962). The randomness of which side exhibits greater development results in

a bimodal distribution of (R-L) variation (Van Dongen et al., 1999). The most frequently cited example of AS are the claws of male fiddler crabs (genus Uca). One claw of the fiddler crab is always much larger than the other, but which claw (right or left) varies from male to male. The third form of biological asymmetry is fluctuating asymmetry

(FA), which occurs as small deviations from perfect bilateral symmetry that are random with respect to direction (Van Valen, 1962). Unlike the other two forms of asymmetry,

FA can be detected in a population when a structure exhibits left-minus-right differences, which are centered around a mean of zero (Van Valen, 1962).

A relationship between stability and symmetry is not a novel idea, but it is a

relationship that was not given significant attention until the mid-1900s when terms to

describe developmental processes were proposed (citations). Waddington (1942, 1953,

1961) introduced the terms developmental stability (DS) and developmental noise (DN)

to describe various processes associated with development. DS was originally defined by

Waddington (1942) as referring to the lack of disruption within the developmental system. Later researchers (Zakharov 1989, 1992; Palmer, 1994; Clarke, 1998; Auffray et al., 1999; Van Dongen and Lens, 2000) expanded on DS, providing slightly different definitions, but all agreeing that a buffering process deflecting developmental perturbations in order to maintain development along an ideal trajectory is part of achieving DS. Thus, morphological structures continue to develop along the ideal

developmental trajectory since DS minimizes the effects of developmental perturbations

on the developmental system through a variety of avenues including feedback regulation,

gene interactions, and biochemical interactions (Rutherford, 2000; Hartman et al., 2001).

However, when developmental perturbations overload the system, an organism may be

unable to buffer developmental perturbations resulting in a deviation or several

deviations from the ideal form.

The counterpart to DS is developmental instability (DI), which describes

processes that disrupt development (Waddington, 1942; Polak and Trivers, 1994;

Markow, 1995; Nijhout and Davidowitz, 2003). The outcome of developmental

perturbations displacing developmental off of an ideal trajectory is known as development noise (DN) (Table 1; Figure 1).

Developmental Process Factors Result 1. Buffering processes (other than Ideal developmental feedback mechanisms) trajectory is maintained or 2. Feedback mechanisms ‐ 'correct' ‘restored’; greater presence Developmental Stability or 'restore' development of developmental stability 3. Genetics ‐ increased relative to developmental heterozygosity, epigenetics (normal instability interaction) 1. Sensitivity to stress ‐ directional selection Ideal developmental 2. Genetics ‐ decreased trajectory is disrupted; heterozygosity, epigenetics (non‐ greater presence of Developmental Instability normal interactions) developmental instability 3. Environmental ‐ temperature relative to developmental variation, chemical pollutants, stability parasite load

Table 1: Factors Influencing the Presence of Developmental Stability and Developmental Instability within a Developmental System

Bilateral asymmetry has emerged as the most convenient variable to evaluate the integrity of developmental systems. All three forms of asymmetry have been proposed as indicators of DS being disrupted during development (e.g. Graham et al., 1993; Moller and Sawddle, 1997; Graham et al., 1998). Directional asymmetry has been argued not to be an indicator of DS because this form of asymmetry has an unknown amount of genetic variance that does not provide information about whether, and to what extent, development has been disrupted (Palmer and Strobeck, 1986, 1992, 2003; Palmer, 1994;

Klingerberg, 2003). Scholars have debated whether or not AS represents an indicator of

Resulting Intensity of Developmental Noise: Assessed through measuring a structure’s fluctuating asymmetry

Developmental noise decreases Developmental noise increases

Development does not deviate Development deviates from or is from or is restored to the ideal not restored to the ideal trajectory trajectory

Developmental instability Developmental instability decreases increases Developmental stability increases Developmental stability decreases

Able to buffer disruptions or Unable to buffer disruptions or development has been have development

‘corrected’/‘restored’ through ‘corrected’/‘restored’ through feedback mechanisms feedback mechanisms

Experiences developmental perturbation(s)

Figure 1: Relationships Among Developmental Processes

the processes that work to maintain the ideal developmental trajectory. Some scholars argue that AS does provide information processes that work to buffer development 17

because it is sensitive to perturbations experienced during development (Leary and

Allendorf, 1989; Graham et al., 1993; Moller and Swaddle, 1997; Rowe et al., 1997);

while others claim that AS has a genetic origin that is not known to be sensitive to

developmental perturbations (Palmer and Strobeck, 1986, 1992, 2003; Palmer, 1994;

Klingerberg, 2003). Since both DA and AS contain a genetic component that is believed to prevent these forms of asymmetry from communicating information on the integrity of

developmental processes, the only form of asymmetry left to provide such information is

FA. FA is the most commonly used indicator of whether or not developmental

perturbations have affected developmental trajectories. Fluctuating asymmetry is argued

to be affected by both DS and DI. Buffering processes that resist or minimize the effect

of developmental perturbations maintain the integrity of the developmental process of

DS. If DS is maintained, only a low degree of DN is present in the developmental system

leading FA of a morphological structure to be low or absent (Figure 1). Factors that

disrupt development (Figure 1) lead to an increase in DI because the integrity of DS is be

maintained. An increase in DI results in an increase in intensity of DN within the

developmental system, which is measured as elevated FA. FA estimates are therefore

measuring the amount of underlying DN since DN represents the combination of the

processes of DS and DI.

Description and Causes of Fluctuating Asymmetry

Because FA can be examined in an individual as well as in a population, two

definitions have emerged. Fluctuating asymmetry is defined as either the average

deviation of multiple structures within a single individual (Van Valen, 1962) or the deviation of a single structure within a population (Palmer and Strobeck, 1986, 2003;

Parsons, 1992). Since FA is commonly used measure to evaluate DN, it is important to discuss how FA relates to the definitions of developmental stability, developmental instability, and DN (Figure 1). When there is an absence of DN (e.g. when DS is acting to

buffer developmental perturbations) in a morphological structure, FA will be low or

absent. When there is an increase in DN (e.g. when DS fails to buffer developmental

perturbations and processes associated with DI disrupt development), FA will increase in

a morphological structure.

Fluctuating asymmetry values are used to assess the accumulation of

developmental perturbations that acted upon the developmental system causing a

deviation from the ideal developmental trajectory. The core idea behind FA as a measure

of DN is that, because the left and right body sides of a bilateral symmetric organism are

replicates of the same structure, they share the same genome and react to external effects

in development in similar ways within a given environment. In a system which is

deterministic, ideally, left and right body sides should be mirror images of each other because they develop under the same conditions both genetically and environmentally.

However, developing organisms do not develop within a deterministic system. Rather, because developmental perturbations act locally, perturbations do not occur bilaterally.

Left and right sides of a body structure separately experience and accumulate developmental perturbations. The resulting bilateral asymmetry, assessed through FA, is the manifestation of DN.

Elevated Fluctuating Asymmetry: A Measure of Increased Developmental Noise

When processes work to buffer disruptions, development is predicted to continue along an ideal trajectory. Stress acting upon the developmental system can cause disruptions resulting in physiological consequences including decreased DS resulting in increased DN. A handful of environmental and genetic stressors have been suggested as forms of developmental perturbations which have the potential to cause a deviation from ideal developmental trajectories.

Environmental Stressors

Studies investigating the relationship between elevated FA and environmental stress have focused on a wide range of taxa including: amphibians (e.g. Fox et al., 1961), insect (e.g. Beardmore, 1960; Parsons, 1962; McKenzie and Yen, 1995), and fish (e.g.

Leary et al., 1992). A variety of environmental stressors have been claimed to cause developmental disruption of morphological structures, resulting in increased DN (e.g.

Palmer and Strobeck, 1986; Parsons, 1990, 1992; Markow, 1995; Moller and Swaddle,

1997). Studies on temperature extremes, parasitic loads, pollutants, and environmental change comprise the majority of the literature addressing the relationship between FA magnitude and environmental stress.

Bilateral structures exposed to temperatures that deviate from a species’ specific temperature range have been reported to exhibit increased FA (Doyle 1975; Sciulli et al.,

1979; Zakharov, 1987, 1989, 1993; Fox et al., 1961; Clarke and McKenzie, 1992; Leary et al., 1992; Imasheva et al., 1997). For example, sand lizards were found to exhibit low

FA within a specific temperature range, but as soon as temperatures shifted outside of the

range, FA increased (Zakharov, 1987, 1989). However, not all species exhibit greater FA

when temperature fluctuations occur (Brana and Ji, 2000: Chapman and Goulson, 2000).

Parasite loads are another environmental factor that has received attention in the FA

literature (e.g. Hamilton and Zuk, 1982; Parsons, 1990; Zakharov et al., 1991; Polak and

Trivers, 1994). Hamilton and Zuk (1982) found that individuals able to resist parasites not only produced the most extravagant sexually selected structures, but also exhibited low FA relative to individuals not able to resist the parasites. Chemical pollutants have

been linked to elevated FA in some, but not all, studies (e.g. Valentine and Soule, 1973;

Zakharov and Yablokou, 1990; Fox et al., 1961; Graham et al., 1993; Mpho et al., 2001).

Several researchers (Ames et al., 1979; Zakharov, 1981; Jagoe and Haines, 1985) have found that fish species located in bodies of water with high concentrations of mercury and/or low pH exhibit increased FA . Studies investigating the link between asymmetry

and chemical pollution were motivated by ecological considerations and FA has since

emerged as important research tool for conservation.

Habitat destruction and changes to the environmental context are considered to be stressors capable of increasing FA in morphological structures (e.g. Manning and

Chamberlain, 1994). Moreover, measuring DN through FA has emerged as an assessment

tool in conservation studies because such information can be used to detect stressors

before a population is seriously affected (Leary and Allendorf, 1989; Parsons, 1992;

Clarke, 1995; Lens et al., 1998; Lens et al., 2002). In particular, Lens and colleagues

(2002) suggest that FA of a single-trait may be an effective early warning system for

conservationists. Finally, habitat location including optimal versus suboptimal and/or

non-optimal sites has also been connected to FA in some Passeriformes (e.g. perching

birds) (e.g. Swaddle and Witter, 1994; Carbonell and Telleria, 1998; Gonzalez-Guzman

and Mehlman, 2000) as well plants (e.g. Siikamaki and Lammi, 1998) and lizards (e.g.

Zakharov, 1981).

When environmental stress acts on the developing system, the organism is

believed to be more susceptible to developmental perturbations because the

developmental system is under pressure and does not perform at optimal levels. A

decrease in the system’s efficiency of buffering developmental perturbations (e.g. a

decrease in DS) coupled with an increase in DI (e.g. processes that disrupt development),

generates high DN as assessed through FA.

Genetic Stressors

When studying Drosophila, Mather (1953) and Thoday (1958) proposed that the

general characteristics of the genotype influence FA. Waddington (1957) argued that DS, or the processes that act to buffer developmental disruptions and maintain developmental along an ideal trajectory, could be influenced by genetic factors. In later studies investigating the influence of genes on FA, overall genotype characteristics were linked to the levels of homozygosity and genetic co-adaptation (e.g. Zakharov, 1987, 1989;

Clarke, 1993; Zakharov and Yablokov, 1997). Genetic co-adaptation describes the

beneficial interaction among genes located on different loci (Ridley, 1996).

Processes that buffer developmental perturbations (e.g. DS) are argued to be

positively correlated with levels of genetic heterozygosity (Lerner, 1954; Palmer and

Strobeck, 1986; Clarke & McKenzie, 1987; Leary and Allendorf, 1989; Zakharov, 1989;

Moller, 1992; Moller and Pomiankowski, 1993; Hutchinson and Cheverud, 1995; Roldan et al., 1998; Waldmann, 2001; Radwan, 2003). When homozygosity is high or co- adaptation is disrupted, FA is expected to be elevated (Palmer and Strobeck, 1986). The heterozygote is believed to be more capable of buffering developmental perturbations and remaining on the ideal developmental trajectory because of allelic dominance results in the masking of recessive alleles that might be deleterious to the developmental system

(Soule, 1979; Vrijenhoek and Lerman, 1982; Leary et al., 1984 1992; Mitton, 1993).

Thus, the heterozygote buffers perturbations occurring during development, which

reduces DN as assessed through FA.

When different genotypes are exposed to similar forms of stress, varying levels of

FA are produced suggesting that certain genotypes might be better suited to buffering

developmental stress (Zakharov, 1989). Researchers have suggested that heterozygosity

represents one way in which an organism buffers developmental perturbations (Clarke et

al., 1986; Ben-David et al., 1992; Roldan et al., 1998). Hutchinson and Cheverud (1995),

for example, found that Saguinus populations exhibiting less heterozygosity in cranial

morphology traits expressed elevated FA in comparison with populations with greater

heterozygosity. The effects of inbreeding on FA have also been investigated as a way to

investigate if heterozygosity is associated with buffering developmental perturbations

(Clarke et al., 1986; Ben-David et al., 1992; Roldan et al., 1998). Inbreeding has been

suggested as leading to an increase in homozygosity which reveals the presence of

deleterious recessive alleles (Clarke et al., 1986). Increased homozygosity is proposed to decrease an organism’s ability to buffer developmental perturbations leading to increased

DN as assessed through FA (Clarke et al., 1986; Moller and Swaddle, 1997).

An analysis conducted by Vollestad and colleagues (1999) demonstrated a weak association between heterozygosity and FA. This analysis, coupled with the fact that the relationship between DS and heterozygosity is supported mainly through correlational evidence, called into question whether or not heterozygosity contributes to the

maintenance of processes which buffer developmental perturbations (Clarke et al., 1992;

Clarke, 1993; Markow, 1995; Kruuk et al., 2003; Woolf and Markow, 2003). Because of conflicting evidence, the relationship between heterozygosity and DS continues to be investigated in the FA literature.

The field of epigenetics studies heritable changes in gene expression that do not involve a change to underlying DNA sequences, while epistasis describes the

“interactions between different genes,” (Cordell, 2002, p.2463). With respect to FA studies, epigenetics has been discussed as the “interactions of gene products,” (Evans and

Marshall, 1996, p.718) that cause a disruption to the developmental trajectory resulting in increased DN as observed through FA. FA has been described as representing an epigenetic measure of the organism’s ability of the organism to buffer genetic and environmental stressors during development (Leary and Allendorf, 1989, Parsons, 1990;

Hallgrimsson, 1999; Leamy et al., 2002). Leamy and Klingenberg (2005) hypothesize

“that FA has a pre-dominantly nonadditive genetic basis with substantial dominance and

especially epistasis,” (p. 13). Thus, the genetic basis of FA rests on several different

genes, which interact with each other. Furthermore, these authors postulate that genes in

these interactions are likely character-specific and are probably involved in the development of the character, but do not code directly for FA (Leamy and Klingenberg,

2005). Untangling the relationship between epigenetics and FA is still in its adolescence, but as the field of genetics expands so will our understanding of if FA represents a valid reflection of the outcome of “interaction of gene products” (Evans and Marshall, 1996, p.718).

Finally, feedback mechanisms that potentially restore bilateral symmetry by correcting deviations that caused one side of a bilateral trait to deviate from the ideal developmental trajectory during development have been researched (Emlen et al., 1993;

Kellner and Alford, 2003). Emlen and colleagues (1993) argue that bilateral structures experiencing developmental perturbations are likely to randomly drift during growth and that evolved ‘checking mechanisms’ should naturally hold any resulting FA within bounds. Since the work of these authors, others have expanded the idea leading to what is now known as the compensatory growth hypothesis (Swaddle and Witter, 1997).

Swaddle and Witter (1997) hypothesized that the interaction between sides of a bilateral structure should compensate for any asymmetries that arise during development, which are not part of the developmental plan. Two hypothetical mechanisms have been proposed for how unplanned asymmetries are compensated. First, the side of the bilateral character which is deviating from the ideal developmental trajectory is buffered in an attempt to suppress asymmetrical development (Emlen et al., 1993; Kellner and Alford,

2003, Dongen, 2006). Second, catch-up ‘growth’ occurs on the side of the bilateral

character that could not buffer developmental perturbations (Emlen et al., 1993; Kellner

and Alford, 2003, Dongen, 2006).

If researchers want to use FA as one way to assess the role of genetics in sustaining DS, then it is important to understand the genetic basis for FA in order to accurately utilized FA. Presently, the connection between genetic mechanisms and FA remains unclear. From what is known, though, little evidence supports a specific gene or

genes influencing FA. Rather, evidence lends support to the hypotheses that FA

magnitude is influenced by dominance and epistatic interactions among genes

(Klingenberg and Nijhourt, 1999; Leamy and Klingenberg, 2005).

Directional Selection, Fluctuating Asymmetry, and Sexually Selected Structures

Directional selection is a form of genomic stress proposed to have an association

with elevated FA in morphological structures. The homeostatic mechanisms of

morphological structures under strong directional selection, or selection that tends to

favor phenotypes at one extreme of the phenotypic range, are believed to be more

susceptible to stress because these developmental control mechanisms are relaxed in

order to expedite the response to selection (Waston and Thornhill, 1994). Relaxation of

homeostatic mechanisms results in reduced buffering during development and an increase

in DI (Parsons 1992; Palmer 1994; Watson and Thornhill 1994).

For a long period of time, all morphological structures were considered to be

equally sensitive to developmental perturbations. Over the last several decades, however,

some structures have been shown to be more sensitive to developmental perturbations as

well as exhibiting greater FA when compared to structures that are not as sensitive to

developmental perturbations (e.g. Soule and Cuzin-Roudy, 1982; Emlen et al., 1993;

Clarke, 1995, 2003; Bowyer et al., 2001). Clarke (2003) has described a structure’s

sensitivity to stress as ‘stress sensitivity’. Even though a procedure for accurately detecting a structure’s ‘stress sensitivity’ has yet to be designed, structures under the influence of sexual selection do appear to be more sensitive to stress than non-sexually selected structures (Moller and Pomiankowski, 1993; Swaddle et al., 1994). Directional

selection is argued to be the reason for why sexually selected structures are more

sensitive to stress and exhibit greater FA than non-sexually selected structures (Bubenik

and Bubenik, 1990; Moller, 1990, 1992, 1997; Moller and Pomiankowski, 1993; Watson

and Thornhill, 1994; Moller and Swaddle, 1997; Bjorksten et al., 2000). Sexually

selected structures are therefore considered more susceptible to ‘developmental

destabilization’ resulting from an increase in ‘stress sensitivity’ because of reduced

effectiveness of developmental processes to buffer developmental disruptions (Watson

and Thornhill, 1994). Thus, the relaxation of control mechanisms in structures under

intense directional selection is believed to account for sexually selected structures being

more prone to developmental perturbations and exhibiting greater FA (Moller 1990,

1992; Watson and Thornhill 1994; Moller and Swaddle 1997).

FA of sexually selected structures is proposed as providing reliable information to

females in mate choice and for males while assessing weaponry of potential opponents

(e.g. Moller, 1992; Thornhill et al., 1998). Moller (1990) found that, within a population

of barn swallows, the sexually selected structure of tail length exhibited greater FA than did the non-sexually selected structures. Additionally, Moller (1990) found that males with the largest sexually selected structure expressed the lowest FA, therefore signaling the highest quality among males. Several studies following Moller’s (1990) work found that females select males with lower FA, or more symmetric structures, than those males with greater asymmetry (e.g. Thornhill, 1992; Hunt and Simmons, 1997). Two years later, Moller (1992) investigated weaponry and reported that weapons (e.g. bird spurs and

beetle horns) exhibited greater FA than structures considered non-weapons. Moller’s

(1992) work also demonstrated that the individuals with the largest weapons had the lowest FA. Other researchers (Manning and Harley, 1991; Ditchkoff et al., 2000) have confirmed Moller’s (1990, 1992) findings that sexually selected characters exhibit greater

FA than do non-sexually selected characters and that there is a relationship between FA and the size of a structure.

With respect to structure size, condition-dependency has been proposed as the reason sexually selected structures show a negative relationship between FA and structure size (Moller and Pomiankowski, 1993). Individuals capable of producing large sexually dimorphic structures are hypothesized to be in prime condition with superior DS and, thus, capable of maintaining symmetrical sexually dimorphic structures. Individuals possessing the largest sexually selected structures have been reported as exhibiting the lowest FA because they successfully buffer developmental perturbations due to their prime condition (Moller, 1992; Moller and Swaddle, 1997). Therefore, FA of a sexually selected structure has been proposed as representing a phenotypic cue for females during

mate choice and males in conflict assessment (Moller, 1992; Thornhill, 1992; Hunt and

Simmons, 1997; Moller and Swaddle, 1997).

Evans and Hatchwell (1993) suggest that the symmetry of larger ornaments in some species (e.g. birds) is not only connected to an organism’s quality, but may be associated with the functional importance of the structure. In their paper, Evans and

Hatchwell (1993) argue that as ornaments become exaggerated, they are constrained into development, which is more symmetrical in order to maintain their function. Swaddle and

Witter (1997) further expanded on the relationship between FA, size, and structures of mechanical and aerodynamic importance (e.g. horns, wings, antlers). These authors argue that a trade-off exists between the life history benefits of fast growth (e.g. earlier age at maturity) and the possible consequences of developing asymmetry in a morphological structure such as lower reproductive fitness and/or mechanical problems (Swaddle and

Witter, 1997). Swaddle and Witter (1997) propose that in some species a developmental mechanism restores symmetry to a structure of functional importance as growth is ending. The organism, therefore, gains the benefits of fast growth such as an earlier age at

maturity as well as symmetry of the functional structure. In support of their assertion,

Swaddle and Witter (1997) studied the development of primary feathers in starlings and

demonstrated that the level of FA varies during development and, by the end of growth, the primary feathers exhibited low FA.

Because some sexually selected structures are also of functional importance, it is

important to consider what increased FA of these structures might be conveying. If a developmental mechanism that restores a structure’s symmetry does exist but the

structure which is sexually selected and of functional importance expresses elevated FA at the end of growth, the question becomes: “what does this mean?” Swaddle and Witter

(1997) among others (e.g. Moller, 1992) suggest that FA of some sexually selected structures might be part of an organism-wide signaling system designed to convey information to choosy females and competing males. If this is the case, elevated FA in sexually selected structures relative to non-sexually selected structures might be conveying information about quality. For example, Moller (1992) suggests that males of a species with the lowest FA but of the ‘highest’ quality might have a developmental mechanism that is able to restore symmetry or effectively buffer developmentally perturbations better than among the males of the species with elevated FA.

Although the above argument by Moller and fellow researchers (e.g. Moller,

1990, 1992; Manning and Harley, 1991; Moller and Hoglund, 1991; Moller and

Pomiankowski, 1993; Moller and Swaddle, 1997; Swaddle and Witter, 1997; Ditchkoff et al., 2000) has been supported in the literature, not all studies agree. Some studies have not found that sexually selected structures exhibit elevated FA relative to non-sexually selected structures or that a relationship between FA and size of sexually selected structures is true for all species (e.g. Balmford et al., 1993; Evans et al., 1995; David et al., 1998; Bjorksten et al., 2000; Hosken, 2001; Ditchkoff and deFreeze, 2010).

Furthermore, other studies claim that not only is it hard to test if choosy females and competing males are using a structure’s FA to assess quality, but that even when tested, not all studies have found that FA is used for quality assessment (e.g. Evans, 1993; Fiske et al., 1994; Tomkins and Simmons, 1995, 1996; Moller et al., 1996; Hunt and Simmons,

1997; Ligon et al., 1998). Due to these varying results, the question emerges as why some, but not all, studies find a relationship between sexually selected structures and elevated FA.

Growth Processes and Fluctuating Asymmetry

Size can be achieved through sex differences in growth rates or growth duration

(bimaturism) or a combination of both. In the literature, particularly on avian species,

focus has been placed on the tentative association between FA and growth rates. Little

attention, however, has been directed at an association between bimaturism and FA.

The skewed focus on growth rates may be a result of the type of species that

permeate the FA literature (e.g. birds, plants, and insects). Not only can structures of

these species (e.g. wings) be manipulated much easier than structures of mammalian

species, but rates of development are readily available for avian species. Birds, for

example, tend to experience rapid growth rates early in life (Ricklefs et al., 1968; Schew

and Ricklefs, 1998; Searcy et al., 2004). In addition to birds, growth rates of certain

plants are also well known leading to a handful of studies investigating the relationship

between growth rates and FA in plants (e.g. Martel et al., 1999; Lempo et al., 2000;

Kozlov et al., 2003).

In reviewing developmental stability and fitness, Moller (1997) states that

evidence from FA studies support an association between fast growth and symmetrical

phenotypes, but does not go into detail about why this association exists. Some later

studies (e.g. Lemp et al., 2000; Shakarad et al., 2001) also lend support for an association

between low FA and fast growth rates; while other studies have not found an association

between FA and growth rates (Searcy et al., 2004).

Although conflicting results complicate understanding the potential association

between growth rates and FA, the term ‘growth rate’ further complicates an evaluation of

this potential association. A distinction between growth rate and growth duration is not always made clear. For instance, it is unclear if the studies Moller (1997) cites as evidence for an association between fast growth rates and symmetrical phenotypes evaluated growth rate or growth duration. Also, phrases such “shifts in developmental timing,” (Kegley and Hemingway, 2007, p.47) and “rapidly growing” (Martel et al.,

1999, p.212) are commonly used to describe growth rather than distinguishing between growth rates and bimaturism or providing a clear definition of ‘growth’.

Furthermore, ‘growth rate’ has also been applied as a measure of fitness (Mitton and Grant, 1984; Thornhill, 1992). ‘Growth rate’ being viewed as a measure of fitness is not surprising because rapid growth entails ‘costs’ to the organism (Rose et al., 2009).

Some researchers (Perrin and Sibly, 1993; Iwasa, 2000; Rose et al., 2009) suggest that

‘costs’ due to rapid growth are ‘assumed in theoretical studies’ (Rose et al., 2009, p.

1379) and that quantifying such ‘costs’ is a challenging feat (Arendt 1997, 2003; Rose, et

al., 2009). With respect to FA studies, one can only assume that when growth rates are used to represent a measure of fitness they are referring to how well an organism maintained its growth rate while experiencing developmental disruptions; however, such an explanation is not supplied in these studies (Mitton and Grant, 1984; Thornhill, 1992).

Vrijenhoek (1985) suggested that relative to body structures that form over short periods of time, those that take longer to form have a greater “widow of vulnerability”

(WOV) to accumulate disruptions during development. Prolonged periods of growth could be providing an opportunity for developmental perturbations to accumulate and steer development off an ideal trajectory resulting in increased DN observed through elevated FA.

Studies addressing the association between FA and structures not under sexual selection have suggested that growth duration may be influencing FA expression in humans and non-human primates (Garn et al. 1967; Nass 1982; Saunders and Mayhall

1982; Kuswandari and Nishino, 2004; Guatelli-Steinberg et al., 2006). These studies

mention growth duration as a possible explanation for their results, but they do not

directly test the hypothesis that growth duration influences FA. For instance, Nass (1982)

suggested that growth patterns, specifically eruption times, may explain the pattern of FA

observed across the dentition of Japanese macaques while Hallgrimsson (1999) reported that bone FA of Macaca mulatta and Homo sapiens increased over the growth period.

Thus, early on in the growth period it appears that FA is low or absent but over the

duration of the growth period FA of bone increased (Hallgrimsson, 1999). Hallgrimsson

(1999) further states that his results demonstrate that because of their longer growth

period, slow growing mammals express greater FA (Hallgrimsson, 1999). From the

research performed thus far, it is possible that duration of growth could be providing a

WOV (Vrijenhoek, 1985) for structures forming over longer periods of time to

33 experience more developmental perturbations relative to those structures forming over shorter periods of time.

From a developmental perspective, sexual dimorphism or “any consistent difference between males and females beyond the basic functional portions of the sex organs,” (Wilson, 1975, p322), can be achieved through either differences in growth rates, bimaturism, or through a combination of both. In primates, body size dimorphism is achieved through both sex differences in growth rates and bimaturism. For example, body size dimorphism in Cebus apella is achieved through bimaturism, or a mode of growth in which males and females grow for a different amount of time (Leigh, 1992). A large component of body size for Pan troglodytes is achieved through differences in the rate of growth between males and females (Leigh, 1992). Canine dimorphism in primates is primarily achieved through bimaturism (e.g. Schwartz and Dean, 2001; Guatelli-

Steinberg et al., 2009).

Within the FA literature, sexually selected structures have, in some studies, been found to express elevated FA relative to non-sexually selected structures (e.g. Moller,

1990, 1992; Uetz et al., 1996; Hunt and Simmons, 1997; Koshio et al., 2007). However, this pattern does not hold across all studies investigating the relationship between FA and sexually selected structures (e.g. Balmford et al., 1993; Evans et al., 1995; David et al.,

1998; Bjorksten et al., 2000; Hosken, 2001; Ditchkoff and deFreeze, 2010).

The different modes of dimorphic growth – bimaturism and growth rate – might explain why some studies lend support to the hypothesis that sexually selected structures express elevated FA more frequently than non-sexually selected structures, while other

studies do not find evidence to support the hypothesis. Bimaturism, in particular, is

connected to Vrijenhoek’s (1985) WOV since it describes a mode of growth in which

males and females grow for a different amount of time permitting the opportunity for one

sex to accumulate more perturbations during development. Bimaturism might be a better

approach to examining if and to what extent growth duration influences FA since the

relationship between growth rate and FA is unclear and because growth rates could be

hard to quantify in species other than birds and plants. Therefore, bimaturism provides a

strong framework from which to examine if a relationship between developmental timing

and FA exists.

Growth Duration and Fluctuating Asymmetry

The general trend across the primate order is that strepsirrhines have shorter

periods of growth relative to the growth periods of apes and humans (e.g. Smith, 1989;

Godfrey et al. 2001). Moreover, within anthropoids, large-bodied species tend to grow for

longer periods of time than small-bodied species (e.g. Leigh and Shea, 1995). While prolonged growth periods may be advantageous in some respects (e.g., affording time for learning), they may also influence a structure’s developmental stability resulting in a

decreased ability to buffer developmental perturbations. Hallgrimmson (1995) has

demonstrated that within mammals, species of Macaca and humans tend to show

elevated FA in osteometric traits in comparison to mammals with shorter periods of

growth. Thus, prolonged growth periods for some mammalian species, such as slow-

growing primates, could entail a cost to the developmental system in which sources of developmental stress affect body structures resulting in elevated DN.

Although some of studies on FA and non-sexually selected teeth mention growth duration as a possible explanation for their results the hypothesis that growth duration influences FA expression has not been directly tested (e.g. Harris and Nweeia, 1980;

Saunders and Mayhall, 1982; Kuswandari and Nishino, 2004).

Neandertal dental FA has been of interest to researchers for several decades (e.g.

Suarez, 1974; Doyle and Johnston, 1977; Frederick and Gallup, 2007; Barrett et al.,

2012). The study by Frederick and Gallup (2007) found that modern humans and

Neandertals exhibited greater average dental FA than the great apes. These authors argue that, because dental growth is not strongly influenced by environmental factors and that growth of the dentition is dependent on the genome, genetic differences between the

species in their study is the primary reason for the observed FA values (Frederick and

Gallup, 2007). Frederick and Gallup (2007) appeared to have grouped all tooth types

together when calculating dental FA, not taking into account that growth durations might

vary among the tooth types (Macho, 2001; Schwartz and Dean, 2001; Reid and Dean,

2006), that sex differences exist in some tooth types, such as the canine (e.g. Schwartz

and Dean, 2001), or that differences in growth duration could exist among hominin

species (e.g. Dean et al 2001; Guatelli-Steinberg, 2007; Smith et al., 2011). Furthermore,

it is unclear if modern human and Neandertal dental FA differ. A more recent study

found evidence for Neandertals experiencing greater developmental stress relative

prehistoric modern human populations (Barrett et al., 2012). Despite the data on

Neandertal (e.g. Guatelli-Steinberg, 2007; Smith et al., 2011), human (e.g. Reid and

Dean, 2006), and great ape (e.g. Reid et al., 1998; Schwartz and Dean, 2001) dental

growth available in the literature, both of these studies (Frederick and Gallup, 2007;

Barrett et al., 2012) did not address dental growth data in relation to their FA results,

leaving several questions unanswered.

In studies addressing non-human primate and dental FA, Nass (1982) suggested

that eruption times may explain the pattern of FA observed across the dentition of rhesus

macaques, but did not directly state how or why eruption time explained the observed

FA. In skeletal series of rhesus macaques, Hallgrimsson (1999) found an ontogenetic pattern of asymmetry in which FA of bone was shown to increase over the growth period.

If, and to what extent, growth duration is associated with elevated FA in primates has yet to be tested systematically across the primate order or even formally tested within a primate genus. Because FA is used to infer information on developmental precision, individual quality and stress experienced during development and since crown formation times are known to vary both across and within species, it is important to understand what underlying variables might affect the expression of FA in morphological structures.

In addition to explaining the pattern observed in non-sexually selected structures and FA, growth duration could explain the association between FA and sexually selected structures. Sexually selected structures may be destabilized by directional selection. They are particularly prone to exhibiting elevated FA leading to an enhanced ability to convey

information to choosy females and competing males about male fitness/quality (Moller

1990; Watson and Thornhill 1994). The primate canine has been given as one example

(Manning and Chamberlain 1993): males of species with sexually dimorphic canines tend to exhibit greater FA than males of species with sexually monomorphic canines.

However, the mechanism which explains the association between canine sexual dimorphism and FA may not be the destabilization of developmental processes associated with sexual selection. Research on adult canine sexual dimorphism in primate species demonstrates that canine dimorphism is achieved through prolonged periods of canine growth in males relative to females (Swindler et al., 1982; Sirianni and Swindler, 1985;

Swindler, 1985; Schwartz et al. 1999; Schwartz and Dean 2001; Schwartz et al., 2001;

Guatelli-Steinberg et al. 2009). Thus, instead of ‘developmental destabilization’ being the reason for an increase in FA magnitude observed in primate canines, male canines of sexually dimorphic primate species may simply have a greater opportunity to accumulate deviations from symmetry because their canines take longer to form than canines of primate males of monomorphic species (Schwartz et al. 1999; Schwartz and Dean 2001;

Schwartz et al., 2001; Guatelli-Steinberg et al. 2009). This opportunity to accumulate more developmental perturbations because of prolonged growth periods was initially described by Vrijenhoek (1985) as the “window of vulnerability”.

Filling in the Gaps

FA of a morphological structure has been of interest to researchers for decades because of the hypothesis that FA conveys information about quality, fitness, and stress experienced during development. The research interest in FA has also generated several unanswered questions including if duration of growth affects the magnitude of FA.

Information on how canine dimorphism is achieved in primate species has expanded through studies on a variety of developmental factors, including but not limited to, histological markers of tooth growth. Schwartz and Dean (2001) found that large- bodied apes achieve canine dimorphism through bimaturism. Using the spacing and number of perikymata on the mandibular canine crown, Guatelli-Steinberg and colleagues (2009) found that males in three catarrhine genera and two platyrrhine genera form their large canines over longer periods of time relative to females of the same genera. Recent advances in the study of FA coupled with the information on crown formation times in primate species provide an opportunity to examine the potential association between growth duration and FA.

The mechanism(s) which underlie the association FA and structures which are not sexually selected are of interest because FA is commonly used as an indicator of stress placed upon the system during development. This dissertation aims to elucidate the mechanism(s) which underlie the association between FA and structures that are and are not influenced by sexual selection through hypotheses that are designed to test the possible effects of growth duration on FA of morphological structures. Moreover, this dissertation aims to tease apart effects of ‘developmental destabilization’ and growth duration by evaluating FA expression in a sexually selected structure. This study will examine catarrhine and platyrrhine species and make comparisons within and between species in order to gain a full view of if, and to what extent, growth duration influences

FA expression. Although the results of study are important for anthropology, particularly since FA is used to assess stress experienced during development of fossil specimens

(e.g. Neandertals and Australopithecus), the results of this study will be applicable

beyond the discipline of anthropology. Disciplines such as evolutionary biology, botany,

genetics, ornithology, and entomology could investigate if and to what extent growth

duration is influencing FA in structures in species typically exmained in their disciplines.

All of these disciplines commonly use FA as an indicator of stress or as a signal of

quality in both extant and extinct species (e.g. Roy and Stanton, 1999; Bateman, 2000;

Carchini et al. 2000; Goddard and Lawes, 2000; Hogg et al., 2001; Prentice et al., 2008;

Dongen et al., 2009). Typically, it is assumed that a population expressing a greater FA

relative to another was under greater stress during development. However, if growth

duration is shown to influence the expression FA, then greater FA in one population

relative to another may not be due to greater stress experienced during development but

rather to a longer period of growth in which to experience stress. Therefore, reearchers

can apply of results of this study when formulating hypotheses on species within their

disciplines when comparing between species or within a species.

Overall, the results of this study will provide critical information towards not only understanding FA in primate dentition but also the potential influence of growth duration on FA expression. If a relationship is found, more than likely this relationship is not

constrained to the a single mammalian order or even within the mammalian taxa. Thus,

researchers in other disciplines will be able to apply the results of this study to their own investigations of FA.

CHAPTER 3: LITERATURE REVIEW – ESTIMATING FLUCTUATING

ASYMMETRY

Fluctuating asymmetry (FA) or subtle, random, differences between the left and

right sides of a bilateral structure (Ludwig, 1932; Van Valen, 1962; Palmer and Strobeck,

1986) represents the outcome of developmental noise (DN). FA estimates are argued to

provide insight into the amount of stress placed upon the developing system and are applied by researchers to infer information about developmental precision of an individual or population and the ability of the developmental system to resist stress experienced during development.

There are several issues involved in quantifying FA including procedures to validate FA data, indices (or equations) to calculation of FA, and analyses to test for differences within and between individuals, populations, or species. This chapter reviews key issues associated with quantifying FA.

Generally, FA measurements are non-invasive and easily attainable (e.g. from field studies or museum collections). Despite the ease of taking FA measurements, FA studies require careful and accurate experimental design including a comprehensive measurement protocol and appropriate statistical analyses. A primary reason why much forethought is necessary for FA studies is because as a biological signal, FA is

41 exceedingly small, on the order of approximately 1-2% of trait size or less (Palmer and

Strobeck, 1986; Palmer, 1994, 1996; Lens et al., 2002). For this reason, repeated measures must be done and correctly analyzed to ensure that the observed asymmetry represents ‘real’ FA and not errors that occurred during measurement or analysis (Palmer,

1994; Palmer and Strobeck, 2003). Measurement error (ME) has the potential to greatly affect the final calculation of FA if measurement and analysis protocols are not established. In addition to ME, other forms of asymmetry and the morphological structure being examined including structure type and size are primary issues affecting both measurement and analysis of FA.

Several steps are involved in quantifying FA beginning with validating the data and concluding with using the appropriate index to calculate FA (e.g. Palmer and

Strobeck, 1986; Palmer, 1994). Depending on the organism under investigation as well as the structures being measured for FA, the methodological protocol might differ slightly from study to study. The discussion that follows outlines the essential recommendations put forward by Palmer (1994) and colleagues (Palmer and Strobeck, 1986; Parsons, 1990;

Palmer and Strobeck, 1992; Swaddle et al., 1994; Merila and Bjorklund, 1995; Leung and

Forbes, 1996; Swaddle and Witter, 1997; Whitlock, 1998; David et al., 1999; Van

Dongen, 1999; Kellner and Alford, 2003; Palmer and Strobeck, 2003; Knierim et al.,

2007) for a methodological and statistical protocol that, if adhered to, will result in FA estimations that most closely represent ‘real’ FA.

Validating the Data Prior to Calculating Fluctuating Asymmetry

The following discussion addresses five issues viewed as essential considerations in collecting data for FA studies and in assessing as clearly as possible ‘real’ FA of either

individuals or populations. Palmer (1994) and other scholars (Palmer and Strobeck, 1986;

Parsons, 1990; Palmer and Strobeck, 1992; Swaddle et al., 1994; Merila and Bjorklund,

1995; Leung and Forbes, 1996; Swaddle and Witter, 1997; Whitlock, 1998; David et al.,

1999; Van Dongen, 1999; Kellner and Alford, 2003; Palmer and Strobeck, 2003; Knierim et al., 2007) have addressed these issues in great detail because not all studies have been performed in a rigorous manner or accounted for the sensitivity of FA to several factors

(e.g. Siegel and Doyle, 1975; Felley, 1980; Balmford et al., 1993; Tomkins and

Simmons, 1995; Veiga et al., 1997; Anne et al., 1998; David et al., 1998; Bjorksten et al.,

2000). After Palmer’s (1994) significant paper on FA methods, a renewed interest in

employing both measurement and analytical procedures appropriate for the study of FA

was generated. Despite the focus on appropriate procedures, inconsistencies still persist

in the literature leading several researchers to suggest that a strict methodological

protocol be established in order for both inter- and intra-disciplinary comparisons of FA estimates (e.g. Green, 1984; Palmer and Strobeck, 1986; Palmer, 1994; van Dongen et al.,

1999).

The following discussion describes the influence that factors such as ME, other forms of asymmetry, trait size, and trait shape can have on data collection and FA calculation. These descriptions are summaries from the work of Palmer and colleagues

(Smith et al., 1982; Green, 1984; Palmer and Strobeck, 1986; Palmer, 1992, 1994; van

Dongen et al., 1999; Palmer and Strobeck, 2003; Knierim et al., 2007). Additionally, the

discussion that follows addresses methodological recommendations of Palmer and

colleagues (Smith et al., 1982; Green, 1984; Palmer and Strobeck, 1986; Palmer, 1992,

1994; van Dongen et al., 1999; Palmer and Strobeck, 2003; Knierim et al., 2007) for

studies investigating FA.

Measurement Error

FA estimations tend to be small (Palmer and Strobeck, 1986; Palmer, 1994, 1996;

Lens et al., 2002) resulting in a similar magnitude to ME (Palmer, 1996). The sensitivity of FA to ME results in inflated FA estimations in both individual and population level between-sides variance (Green, 1984; Palmer and Strobeck, 1986; Palmer, 1994; Merila and Bjorklund, 1995; Swaddle et al., 1995; Bjorklund and Merila, 1997; Van Dongen et al., 1999; Van Dongen, 2000). For instance, scholars have reported ME as accounting for high percentages of the total between-sides variation that is commonly considered to be

representative of FA (Fields et al., 1995; Van Dongen and Lens, 2000). If ME is not controlled for, it is difficult to determine if FA estimates represent biological asymmetry or a combination of biological asymmetry and the variance resulting from ME.

The most frequently recommended step for minimizing ME is to repeatedly

measure right and left structures (Lundstrom, 1960; Green, 1984; Palmer and Strobeck,

1986; Knierim et al., 2007; Palmer and Strobeck, 2003). The recommended minimum

number of repeated measures is two (Moller and Swaddle, 1997). If ME is suspected to

be high for a particular morphological structure, the suggested number of repeated

measures increases to 4 to 6 (Swaddle et al., 1994; Van Dongen et al., 1999). Repeated

measures should be taken at different times to ensure that measurement replication is

‘blindly’ performed. When taking measurements ‘blindly’, researchers should measure

their samples at random so that specimens of similar species or sex are not being

measured in order (Knierim et al., 2007). Taking the challenge of sample access into

considation, David and colleagues (1999) suggest that if repeated measures need to be

taken during the same measuring session that methodological protocols are established to

reduce ‘session bias’.

Although repeated measures are argued to be the best procedure for decreasing

the risk of ME being incorporated into FA by separating out ME from ‘real’ FA (Green,

1984; Merila and Bjorklund, 1995; Palmer and Strobeck, 1986; Palmer, 1994; Swaddle et

al., 1994; Van Dongen et al., 1999; Van Dongen, 2000; Palmer and Strobeck, 2003),

applying a measuring technique with a low probability of ME should be built into the

measurement protocol (Knierim et al., 2007). To achieve this recommendation, proper

training in the project’s equipment is needed and the same person should perform both

initial and repeated measurements (Palmer and Strobeck, 1986, 2003; Knierim et al.,

2007). Moreover, the equipment should be appropriate for the traits being measured in

order to ensure that measurements are taken accurately. Accounting for precision in measurements through training of researchers and equipment selection will reduce the potential for ME incorporation during the data collection phase. This is an essential recommendation for all studies, but particularly those studies where structures may differ in size (Palmer and Strobeck, 2003). Taking this recommendation into account when

45 designing a methodological protocol will decrease the likelihood of ME being part of the

FA estimation.

Forms of Asymmetry

Bilateral organisms possess asymmetries which are adaptive and as such are considered to have a genetic basis (Palmer, 1994; Klingerberg, 2003). These adaptive asymmetries, which include directional asymmetry (DA) and antisymmetry (AS), are argued to contain little to no information which would be useful for interpretation of a morphological structure’s DN because of their genetic origin (Palmer and Strobeck,

1992; Palmer, 1994; Klingerberg, 2003; Palmer and Strobeck, 2003).

Accounting for different forms of asymmetry will avoid skewed FA estimates since both DA and AS have the potential to alter FA estimates (Palmer and Strobeck,

1986, 1992; Palmer, 1994; Van Dongen et al., 1999; Klingenberg, 2003; Palmer and

Strobeck, 2003). For instance, a morphological structure may be characterized by DA resulting in an inflated FA value. A distribution of the right minus left differences (R-L) that appears normal could have underlying AS resulting in a decrease in FA expression

(Palmer and Strobeck, 1986, 1992, 2003). Therefore morphological structures exhibiting

DA or AS will not yield reliable information on the underlying DN since FA expression is distorted by the presence of another form of biological asymmetry (Palmer and

Strobeck, 1992; Palmer, 1996).

Some researchers, however, argue that FA, DA, and AS are interrelated (Graham et al., 1993, 1998; Leamy, 1999) and that all three types of asymmetry can provide

46 information about DN (Leary and Allendorf, 1989; Graham et al., 1993; Moller and

Swaddle, 1997; Rowe et al., 1997). DA has been found in several studies on wing asymmetry (Simmons and Ritchie, 1996; Smith et al., 1997; Klingenberg et al., 1998;

Goulson et al., 1999; Windig and Nylin, 1999; Pither and Taylor, 2000) and recorded in mouse jaws (Leamy et al., 1997; Klingenberg et al., 2001). Studies on insect wings suggest that when DA is present it is not consistent in direction (e.g. left or ride side), between species, or within species among populations (Simmons and Ritchie, 1996;

Klingenberg et al., 1998; Goulson et al., 1999). The results of these studies imply that DA does not convey information about DN (Simmons and Ritchie, 1996; Klingenberg et al.,

1998; Goulson et al., 1999). After the random variation representative of DN is factored out DA provides information “only for the systematic difference between sides,”

(Klingenberg, 2003, p.17). DA cannot provide information on developmental disruptions resulting from developmental perturbations because it represents the mean asymmetry of a sample (Klingenberg, 2003).

With respect to AS, the resulting pattern is such that approximately half the population has a larger right side while the other half develops a larger left side (Palmer,

1994). Because AS has a genetic origin (Klingerberg, 2003) it is believed that AS is not associated with processes that maintain or disrupt the stability of the developmental system.

Since these two types of asymmetry are believed to represent a genetic component of the developmental trajectory, their statistical significance should be carefully evaluated in order to avoid misrepresentation of FA. The influence of DA on FA has received

considerable attention (e.g. Graham et al., 1993; Leung and Forbes, 1997; Klingenberg et

al., 1998; Pither and Taylor, 2000; Kark et al., 2004). Morphological structures exhibiting

DA complicate both analysis and interpretation of FA (Palmer and Strobeck, 1986, 2003;

Klingenberg, 2003; Van Dongen, 2006). As noted, analyses are complicated since a number of FA indices are inflated by DA (Palmer, 1994; Palmer and Strobeck, 1986).

Also because left and right of structures associated with DA develop differently, the influence of developmental perturbations may not be identical (Klingenberg, 2003). To avoid such problems, either structures expressing significant DA should be removed from the study (Palmer and Strobeck, 1992; Palmer, 1994; Klingenberg, 2003; Van Dongen,

2006) or the asymmetry of interest should be shifted to DA (Klingenberg et al., 1998;

Lens and Van Dongen, 2000; Pither and Taylor, 2000; Van Dongen, 2006). Cases where

very slight DA is present could also result in statistical problems during analysis

particularly in large sample sizes (Palmer and Strobeck, 2003). In such cases, factoring

out DA before FA analysis is favored over removing the morphological structure(s) from

the study sample. It is possible to statistically correct for mean DA by subtracting the

average amount of asymmetry from individual signed asymmetry values (Palmer and

Strobeck, 1986, 2003; Van Dongen, 2006). Statistically correcting for DA has emerged as

an essential step in any FA analysis where DA is suspected to be a factor or in studies

where it is unclear if DA could be present (Palmer, 1994; Palmer and Strobeck, 1986;

Palmer and Strobeck, 2003; Knierim et al., 2007).

To account for potential confounding effects prior to FA calculation, it is

necessary to test for AS (Palmer and Strobeck, 2003; Knierim et al., 2007). AS can cause

48 platykurtosis, or a distribution of right minus left differences (R-L) which is flatter than a normal distribution, in the data output (Van Dongen et al., 1999; Van Dongen, 2006).

The frequency distribution associated with platykurtosis exhibits a valley between two, equally sized peaks which are the same distance from zero (otherwise known as bimodal distribution). The flat valley part of the distribution which is centered on zero does not contain observations. Both bimodal and multimodal distributions are examples of platykurtosis. In a multimodal distribution, there are several valleys as well as equally sized peaks on either side of the valley. Testing for kurtosis in the data set will detect the presence of AS.

Type and Number of Structures

Generally there are four important factors to consider when determining if a structure is appropriate for an FA study. The structure should be: 1) accessible; 2) have identifying landmarks or dimensions; 3) permit repeated measurements; and 4) not exhibit DA or AS. Accessibility of a structure is important because pieces of equipment, such as calipers, need to be correctly positioned on the structure to obtain an accurate measurement. If a structure is easily accessible, the task of taking repeated measurements will not be difficult or time consuming since the structure can be accurately positioned each time a measurement is taken. Structures should have identifiable landmarks (e.g. tip of a bird’s feather) or dimensions (e.g. buccal-lingual and basal circumference).

Landmarks or dimensions are helpful because they identify where a measurement needs to be taken permitting not only repeated measurements to be accurately taken but for

comparisons to be made between different species. For example, antler landmarks are

similar across several species (citation).

Taking repeated measurements is easier on structures that are accessed without

difficulty and present identifiable landmarks or dimensions. Successfully repositioning

equipment to conduct repeated measurements is important because the inclusion of

repeated measurements in the data set factors out ME (Green, 1984; Palmer and

Strobeck, 1986; Palmer, 1994; Swaddle et al., 1995; Van Dongen et al., 1999; Van

Dongen, 2000; Palmer and Strobeck, 2003; Knierim et al., 2007). Repeated measurements are also useful in assessing intra-observer error (e.g. Smith et al., 1982).

The type of structure selected is extremely important in designing a FA study

(Soule and Cuzin-Roudy, 1982; Palmer and Strobeck, 1986; Palmer, 1994; Leung and

Forbes, 1996; Palmer and Strobeck, 2003; Knierim et al., 2007). Although every

specimen has a number of structures available for examination, some structures may be

better suited for examining underlying DN than others.

In the early FA literature, all morphological structures were considered to be

equally sensitive to developmental perturbations. Over the last several decades, research

has demonstrated that some structures are not equally sensitive to developmental

perturbations. Rather, certain structures may be more sensitive to developmental

perturbations resulting in those structures exhibiting elevated FA relative to structures

believed not to be sensitive to developmental perturbations (e.g. Soule and Cuzin-Roudy,

1982; Emlen et al., 1993; Clarke, 1995; Bowyer et al., 2001; Clarke, 2003). Clarke

(2003) has termed a structure’s sensitivity to stress as ‘stress sensitivity’. Structures of

functional importance and those under intense directional selection are proposed as

having a high ‘stress sensitivity’ to developmental perturbations, suggesting that these

structures are more likely to accumulate perturbations, deviate from the ideal developmental trajectory, and express DN.

In the initial steps of formulating a methodological protocol, whether a structure

is, or could be, sensitive to stress should be taken into account (Moller, 1990, 1992;

Moller and Pomiankowski, 1993; Swaddle et al., 1994; Clarke, 1995, 2003). A procedure for accurately detecting a structure’s ‘stress sensitivity’ has yet to be developed; however, there does appear to be a pattern for both structures of functional importance (Clarke,

1995, 2003) and those under intense directional selection, such as sexually selected structures (Moller and Pomiankowski, 1993; Swaddle et al., 1994).

Structures of functional importance (e.g. tail feathers, wings of birds and insects) might be more sensitive to stress during early stages of development because growth rate is accelerated leaving the processes that buffer developmental perturbations without sufficient time to react to developmental perturbations (Swaddle eta l., 1995; Swaddle and Witter, 1997). These structures are therefore more likely to exhibit greater FA early in development relative to later in development. Although there are studies that lend support to avian tail feathers exhibiting greater FA during early development and lowered

FA as development proceeds (e.g. Swaddle and Witter, 1997) the evidence to support a relationship between growth rates and elevated FA is not well supported outside of avian

FA studies (Shakarad et al., 2001; Searcy et al., 2004).

In addition to structures of functional importance, sexually selected structures are

also believed to be more prone to developmental perturbations resulting in greater FA in

sexually selected structures relative to non-sexually selected structures (Moller, 1990,

1992; Moller and Hoglund, 1991; Moller and Pomiankowski, 1993; Tomkins and

Simmons, 2003). The relaxation of control mechanisms in structures under intense

directional selection may account for some sexually selected structures exhibiting greater

FA than non-sexually selected structures (Thoday, 1958; Watson and Thornhill, 1994).

Wear and Damage

It has long been recognized that wear or damage to a structure can skew FA estimates (e.g. Doyle and Johnston, 1977; Townsend and Garcia-Godoy, 1984; Palmer and Strobeck, 1986; Moller, 1991; Swaddle and Witter, 1994, 1995; Swaddle, et al.,

1996). FA estimates based on data collected from morphological structures exhibiting wear and/or damage do not represent differences between R-L sides that are due to underlying DN. Rather, these FA estimates represent either asymmetry resulting from wear or a combination of asymmetry partly from the underlying DN as well as asymmetry resulting from wear and/or damage. Asymmetry that results from wear and/or damage is not associated with stress upon the developmental system and thus does not reflect underlying DN. Furthermore, because equivalent degrees of wear do not necessarily occur bilaterally in several morphological structures, such as teeth and antlers, it is possible that FA of a morphological structure with wear does not reflect FA resulting from underlying DN.

Because the amount of asymmetry due to wear and/or damage is difficult to estimate and factor in after measuring is complete, including an examination for wear and/or damage in the methodological protocol is an important consideration (Cuthill et al., 1993; Moller, 1993; Swaddle et al., 1994). Standards for assessing wear and/or damage of a morphological structure are generally discipline-specific. Regardless, the methodological studies on FA (e.g. Palmer, 1994; Palmer and Strobeck, 2003) recommend visually inspecting morphological structures for wear or damage prior to measuring. If wear or damage is found to be extensive or would prevent accurate measurement, then the structure should not be measured. Approximal wear is an example of extensive wear because it causes the measurement point of the mesio-distal diameter to become undefined (Kieser, 1990; Hillson, 1996).

Several studies have incorporated an assessment of wear and damage into their methodological protocol. For example, teeth exhibiting damage including caries and attrition have been removed from the sample (Angelopoulou et al., 2009). Scholars examining antlers for FA remove damaged or extremely worn antlers from their studies to avoid skewed asymmetry results (e.g. Ditchkoff and deFreese, 2010). Similar to antlers, damaged avian wings are removed from the sample prior to measurement

(Swaddle and Witter, 1997).

Structure Size

The relationship between FA and structure size has received considerable attention in the literature because FA is argued to vary with trait size leading to the

possibility of FA analysis and interpretation being complicated if size variation is not

considered (Palmer and Strobeck, 1986; Palmer, 1994; Palmer and Strobeck, 2003). One of the most important reasons to take size variation into account is because when the

same ‘level’ of DN is being experienced by morphological structures of different sizes

the larger morphological structure is expected to exhibit greater asymmetry on average

compared to smaller structures (Palmer and Strobeck, 2003; Knierim et al., 2007). For a

multiple-structure FA study, if structure size is not corrected for prior to FA analysis the

resulting average FA reflects not only the underlying DN but also any size-dependent

variation (Palmer and Strobeck, 1986; Palmer, 1994; Rowe et al., 1997; Palmer and

Strobeck, 2003).

A positive relationship between FA and structure size has been noted (e.g. Moller

and Swaddle, 1997); however, the relationship of FA and structure size is not always

positive. Sexually selected structures have exhibited a negative FA-structure size

relationship which differs from the positive relationship typically expressed by non-

sexually selected structures (Moller, 1990; Manning and Hartley, 1991; Moller and

Hoglund, 1991; Moller, 2000). To further complicate the relationship between FA-

structure size, not all sexually selected structures show a negative relationship between

FA and structure size (e.g. Balmford et al., 1993; Tomkins and Simmons, 1995; Jennions,

1996; Bjorksten et al., 2000). These opposing results might be connected to the size of

the sexually selected structure; however, a definitive explanation for why some but not all

sexually selected structures exhibit a negative relationship between FA and structure size

has yet to be presented.

Scholars recommend correcting for trait size effects through appropriate models

to ensure that differences in FA are preserved in the measurements (Palmer and Strobeck,

2003; Leung, 1998; Graham et al. 2003; Van Dongen et al., 2005; Van Dongen and

Moller, 2007). Testing for size dependence prior to testing for FA is recommended because the influence of size-dependence in asymmetry calculations could result in a leptokurtosis frequency distribution as well as obscuring any presence of AS in the distribution. Several FA indices – originally constructed by Palmer and Strobeck (1986) and Palmer (1994) – correct for structure size effects by expressing deviations as a proportion of structure size.

Unlike biological variation, ME is unaffected by the average differences between sides of a morphological structure (Palmer and Strobeck, 2003). Therefore, the presence or absence of ME needs to be determined prior to making size-adjusted estimates of FA.

If ME is minimal, applying |ln/| to scale out size variation is recommended

(Palmer, 1994). Leung (1998) suggests that relative FA be used when the coefficient of variation in structure size is small. If, however, ME exceeds 10% of the estimated average of the difference between the sides, Palmer and Strobeck (2003) suggest either 1) using a t-test if the slope of the proportional FA versus structure size is steeper than the slope of the proportional ME versus structure size; or 2) dividing the size range into three

or more size categories and then applying the appropriate index to factor out ME from

each category.

Indices and Analysis: Fluctuating Asymmetry

Choosing the appropriate FA index is one part of the methodological protocol and

involves having adequate information concerning sample size, presence of measurement

error, other forms of asymmetry, and the possible influence of trait size. Understanding the limitations of one’s study is important in selecting a FA index since many factors

such as ME can influence the resulting FA estimate. Therefore, selecting a FA index that best suits the needs of the study being conducted is an essential component to any FA study. Furthermore, the choice of index determines the choice of analysis. For example, several indices are generated from a sides x individual ANOVA while other indices cannot be generated from an ANOVA. In this section, FA indices proposed by Palmer and colleagues (Palmer and Strobeck, 1986; Palmer, 1994; Klingerberg and McIntyel,

1998; Leung et al., 2000; Palmer and Strobeck, 2003) will be discussed followed by recommended statistical analyzes for FA.

FA Indices

Before discussing specific FA indices, two terms need to be addressed. Signed asymmetry (R – L) is the difference between the right (R) and left (L) sides of a bilateral trait of an individual. Information on the direction of asymmetry is provided through the use of signed asymmetry. Absolute asymmetry, or unsigned asymmetry (|R – L|), is the absolute value of the difference between R and L sides of a bilateral trait for an individual.

Palmer and Strobeck (1986) provided a summary of nine fundamental indices. FA indices were grouped into categories based on absolute asymmetry and signed asymmetry, type of size correction, and whether the index can be applied to single or multiple traits per individual. Palmer (1994) added three additional indices to address multiple traits per individual. Other scholars (Klingerberg and McIntyel, 1998; Leung et al., 2000) have contributed additional indices including a landmark method index. Palmer and Strobeck (2003) published an updated summary of FA indices (Table 2) which expanded on their original summary (Palmer and Strobeck,1986) as well as indexes proposed by other scholars (e.g. Palmer, 1994; Klingerberg and McIntyel, 1998; Leung et al., 2000). A brief summary of the most widely used FA indices, as discussed by Palmer and Strobeck (2003), is provided below. FA indices are labeled according to Palmer and

Strobeck (2003). After discussing these FA indices, a summary of all FA indices is provided in Table 2.

FA1 is the most commonly used index for FA studies (Palmer, 1994; Palmer and

Strobeck, 2003) because it is easily used in the ANOVA procedure for testing differences among samples. This index, however, does not include a size correction. Because FA2

|| ( ) includes a size correction at the individual level it is widely used in / studies on FA variation. Tests for significant of FA variation are restricted for FA2 if ME is not accounted for because the replicate measurements are averaged prior to applying the index (Palmer and Strobeck, 2003). Palmer (1994) and colleagues (Palmer and

Strobeck, 1986, 2003; Leung et al., 2000; Palmer and Strobeck, 2003), recommend using

FA2 only when it is clear that a size dependence of || among individuals within a

Indices Equation Pros and Cons of Index (As explained by Palmer and Strobeck (1986, 2003) and Palmer (1994))

1 || Not very sensitive to outliers Size correction not included Should not be used if DA or AS are present

|| 2 Not very sensitive to outliers / Size correction at individual level Replicate measures are averaged prior to calculation Sensitive to DA and AS Recommended only for use when a size dependence of ||among individuals is present

|| 3 Not very sensitive to outliers / Sensitive to DA and AS Recommended when a size dependence of ||among sample is present

4 √ Sensitive to outliers Effective at estimating between-sides variation Size correction not included Sensitive to AS Not sensitive to DA Recommended for studies where two samples are compared

5 √Σ / Hard to compute Strong index for small samples Sensitive to DA and AS Size correction not included

6 √ Recommended only for use when a size dependence of / || among individuals is present Not sensitive to DA Sensitive to AS Sensitive to outliers

Continued

Table 2: Indices for Fluctuating Asymmetry

Table 2 continued

7 √ Not sensitive to DA / Sensitive to AS Sensitive to outliers Recommended when a size dependence of ||among samples is present

8 |ln/| Easy to compute but hard to apply Not widely used in FA studies Not biased by size dependence

9 1 Recommended for use in conjunction with other indices Easy to compute Sensitive to AS Dependent on overall trait size

10a √2 Time consuming to compute but worth it Describes magnitude of non-directional asymmetry after measurement error has been factor out Not sensitive to DA Sensitive to AS Sensitive to size dependence of || Sensitive to outliers Recommended for use with either FA1 or FA4

11 Σ Addresses multiple traits per individual Sensitive to DA and AS

12 Addresses multiple traits per individual Recommended for use with meristic traits Recommended for use in parallel with FA11

13 det Multivariate measure for meristic traits Difficult to compute DS among traits cannot be distinguished Sensitive to size dependence of ||

Continued

Table 2 continued

14 Σ Independent on trait size Independent on average trait FA More powerful than FA15 when leptokurtosis is present Results are not directly comparable to other studies

15 Σ Independent on trait size Independent on average trait FA Nonparametric Results are not directly comparable to other studies

16 MANOVA Lacks statistical power in comparison to FA14 and FA15

17 Σ Powerful tests for heterogeneity of DI among individuals Resulting FA values can be compared to single trait indices

18 Σ Potential to provide robust information on individual Di Measurement error is a concern Confounded by size-dependence changes in structure shape

sample exists.

FA4 () is the second most commonly used FA index (Palmer, 1994;

Palmer and Strobeck, 2003). FA4 is recommended for studies in which two samples are being compared (Palmer, 1994; Palmer and Strobeck, 2003); however, because size correction is not built into this index it is sensitive to size dependence of ||.

Although FA5 (ΣRL/N) is argued to be difficult to compute in comparison to FA1 and FA4 it is considered to be a strong index for small samples sizes (Palmer,

1994; Palmer and Strobeck, 2003). FA5 is a strong index for studies with a small sample because there is an additional degree of freedom in the estimation of between-sides

variance that increases statistical power (Palmer, 1994; Palmer and Strobeck, 2003).

Similar to the recommendation of Palmer and Strobeck (1986) for FA1 and FA 4, FA5

should only be used if independent from character size since size correction is not

applied.

Size correction is done by individual and the index is not biased by size-

dependence of || in FA6 ( ). Therefore, FA6 is used when size dependence / of || among individuals is present. When FA increases proportional to character

size, FA6 becomes more reliable than FA1, FA4, and FA5 (Palmer, 1994).

FA10 index was first reported by Palmer (1994) and has since been expanded

upon by Palmer and Strobeck (2003) to include FA10a and FA10b. Both FA10a and

FA10b are generated from the table produced through a sides x individual ANOVA on

untransformed replicate measurements of R and L sides. These two ‘sub’ indices of FA10

are applied to studies examining single structures/traits. FA10a and FA10b can be more

time consuming to compute than other indices; however, because they address a common

problem within FA studies they possess a major advantage over indices. These FA10

indices are the only indices which describe the magnitude of non-directional asymmetry

after ME has been factored out (Palmer, 1994; Palmer and Strobeck, 2003). Despite how powerful FA10a and FA10b are for researchers, these indices do have limitations (Palmer and Strobeck, 1986; Palmer, 1994). The degrees of freedom are approximate and depend heavily on relative sizes of non-directional asymmetry as well as ME variances (Palmer and Strobeck, 1986; Palmer, 1994). These indices are sensitive to outlines when testing for differences among three or more samples, which is why FA10a and FA10b are best

used when examining differences in FA between two samples (Palmer, 1994; Palmer and

Strobeck, 2003)

Palmer and Strobeck (2003) added FA10b to Palmer’s (1994) original FA10

index. FA10a should be used with untransformed replicate measurements while FA10b is

applied to transformed replicate measurements. Both FA10 indices are generated from a

sides x individual ANOVA. Palmer and Strobeck (2003) present a modified equation for

FA10 indices that assumes two replicate measurements were performed (p. 286). The

equation listed in Table 2 represents FA10a and can be used with two or more replicated

measurements. The equation for FA10a is: . FA10b is computed in a

similar way to FA10b but the analyzed data are log transformed replicated measurements

(e.g. ln and ln).

Each FA index described above and outlined in Table 2 offers its own unique

method by which to evaluate FA. It is essential that researchers are aware of which FA

index best suits the needs of their study. Because indices differ in their sensitivity to

several factors (e.g. outliers, trait size variation, DA, AS, and ME) it is also important to

acknowledge the limitations of each index. Of the indices for individual FA based on single trait per individual, Palmer and Strobeck (1986) argue that FA4, FA5, FA6, and

FA8 are better at detecting true differences in FA among samples in comparison to indices that are based on absolute values of R – L (e.g. indices FA1, FA2, and FA3).

Furthermore, FA5 is better at detecting true differences in FA among small sample sizes as long as DA and AS are absent and FA is independent of character size (Palmer and

Strobeck, 1986). Palmer (1994) recommends that if researchers use two different indexes,

that one of the indices should be FA10 since this index effectively removes ME from the between-sides variance prior to calculation and can be easily derived from the recommended statistical analysis for FA of sides x individual ANOVA.

Recommendations Given in the Literature for Statistical Analysis of FA

Because FA represents an estimation of variance, tests for differences in FA at all levels are considered tests for heterogeneity of variance (Palmer and Strobeck, 2003).

The between-sides variance in a sample has the possibility of being confounded by factors that FA is sensitive to such as ME, DS, AS, and structure size. Due to the potential of skewing FA estimates by one, or all, of these factors it is recommended that size dependence be tested for and that an assessment of ME, DA, and AS be performed prior to applying any of FA index (e.g. Palmer and Strobeck, 1986, 1992, 2003; Knierim et al., 2007).

Addressing Potential Confounding Factors

A handful of FA indices correct for structure size effects through expressing deviations from bilateral symmetry as a proportion of structure size. Information concerning the relationship between FA and structure size continues to grow in the literature (e.g. Waynforth, 1998; Hosken et al., 2000; Kruuk et al., 2003; Palmer and

Strobeck, 2003; Bartos et al., 2007; Knierim et al., 2007). Overall, the goal of any FA study is to gain information about ‘real’ differences in FA among or between samples.

Therefore, it Palmer and Strobeck (2003) recommended that the relationship between FA

and structure size for every character in a study should be considered.

Palmer and Strobeck (2003) recommend that to determine if FA varies due to

structure size, one should first examine plots of (Ri – Li) versus size (e.g. [Ri + Li)/2]).

The level of size correction (e.g. individual or sample) will determine the type of correction. For studies examining FA of individuals the most common transformation is to divide the difference of |Ri – Li| or (Ri – Li) by the mean ((Ri+Li)/2). This

transformation also allows for direct comparison among traits of different size. Indices

FA2 and FA6 include this common transformation for structure size. For structure-size

correction that occurs at the sample level, indices FA3 and FA7 apply a similar

transformation to that of FA2 and FA6.

In some cases, the pattern of size dependence may require a different type of

transformation (Leung, 1998). While in other cases, correcting for size dependence may

generate FA differences that do not reflect true biological variation but rather include ME

(Palmer and Strobeck, 1986, 2003). One way to handle the possible incorporation of ME due to size-scaling is to divide the size range into a few categories then apply FA10a to each category in order to factor out ME. After factoring out ME, each category should be

evaluated by the ratio of FA10a to see if a decline in the ratio occurs (Palmer and

Strobeck, 2003). A decline in the ratio is argued to “be due to a true decline in

proportional FA,” (Palmer and Strobeck, 2003, 289).

Using the standard sides x individuals ANOVA, the significance of FA relative to

ME can be tested for to determine if the difference in between-sides variation among

individuals is due to ‘true’ biological asymmetry. Because ME can contribute high

percentages of the total between-sides variation resulting in a decrease in the correlation between observed FA and inferred underlying DI (Fields et al., 1995; Van Dongen and

Lens, 2000) it is necessary to know if ME is contributing to differences in R – L among individuals. Palmer and Strobeck (2003) have quantified ME into five descriptors (Table

3). The first two descriptions, ME1 and ME2, report ME in the units of measurement originally used by the researcher (e.g. millimeters) and, have the ability to be compared to FA1. The number of repeated measurements, however, determines which descriptor is compared to FA1. ME1 should only be used when FA1 is determined using two measurements per side while ME2 is not limited to the number of repeated measurements. Both ME1 and ME2 report true ME for a trait, despite the limited number of repeated measurements required for ME1. ME3 reports a percentage of average difference between-side that is independent of the units of measurements (Palmer and

Strobeck, 2003). However, it does not provide true ME unless information is gained from

FA1 or MSinteraction (sides x individual interaction MS that is generated through the

ANOVA). The final two descriptions (ME4 and ME5) measure repeatability through

reporting FA variance as a proportion of the total between-sides variation, which

included ME (Palmer and Strobeck, 2003). These two descriptors provide a standardized

measure that is easy to understand even though they do not directly describe ME (Palmer

and Strobeck, 2003).

Descriptor Equation (Outlined by Palmer and Strobeck, 2003)

ME1 Σ| |/

ME2 Σ,,,…./ = √

ME3 %ME = 100 = 100

ME4

ME5

Table 3: Indices for Measurement Error

Because almost every FA index is sensitive to DA, a major question regarding

DA in FA studies has emerged (Palmer and Strobeck, 2003): At what point does DA

become so large that it confounds any interpretations of FA variation? Although a

consensus on how to handle DA has not emerged in the literature, several scholars suggest applying a simple test to examine if the mean (R – L) differs significantly from

zero is necessary (Lande, 1977; Palmer and Strobeck, 1986; Palmer, 1994; Palmer and

Strobeck, 2003). Determining if a significant difference between the mean (R – L) and

zero can be achieved in a few different ways including a one-sample t-test of mean (R –

L) versus zero or the sides x individual ANOVA procedure (Palmer, 1994). With respect

to AS, examining the dataset for the presence of platykurtosis can be easily accomplished

through normal probability plots (Aitken et al., 1989; Swaddle et al., 1994).

Detecting Fluctuating Asymmetry Variation

By selecting the appropriate index, differences in FA among samples can be

accurately detected. A nonparametic ANOVA is most applicable for indices which focus

on a single trait per individual and are based on| | (Palmer and Strobeck, 1986).

Indices that are appropriate for data collected on a single trait per individual are generally considered a form of variance (Palmer and Strobeck, 1986). Therefore, a standardized F- test is the most powerful parametric test available for examining differences if the two

samples are normally distributed (Palmer and Strobeck, 1986). FA is evaluated

using the F statistic by employing the difference in variance between the mean square of

the remainder and error divided by the number of replications (M) from

two-way mixed model ANOVA, resulting in the following equation:

Since the degrees of freedom for the F-test are dependent on how FA is estimated,

it is important to note that if replicated measurements were not taken, the degrees of

freedom for each FA estimate will be the . However, if replicate measurements

were taken, is adjusted following the Satterthwaite formula (Palmer and Strobeck,

1986; Sciulli, 2003). The Satterthwaite formula for is the variance component due to

non-directional asymmetry ( ) (Palmer and Strobeck, 1986; Sciulli, 2003).

Satterthwaite formula reduces the degrees of freedom for the sample making it an

67 appropriate calculation for when degrees of freedom are small. The correction is as follows:

When multiple structures are considered, an independent FA estimate is provided by each structure. After confounding factors are considered, a two-way traits x individual

ANOVA on replicate measurements of |ln ln| will address the differences among individuals when information from multiple traits is combined.

CHAPTER 4: MATERIALS AND METHODS

This chapter describes the non-human primate species used to test the hypotheses

of this dissertation and explains the criteria utilized in selecting species samples.

Additionally, this chapter discusses the variables used, methods of measurement,

statistical approaches, and calculation procedure for fluctuating asymmetry (FA).

Materials

Sample Selection of Non-human Primate Species

Species included in this dissertation sample were selected based on four criteria:

1) species with known first molar crown formation times (CFTs); 2) species used in

previous research on primate canine FA; 3) species used in previous research that

included competition levels as measure of sexual dimorphism; and 4) species with known

canine lateral enamel formation times (EFTs). Included in the sample are catarrhine and

platyrrhine species. Since some species do not fulfill all four criteria, each hypothesis is tested using a different array of primate species.

Taxonomy Considerations

A major condition for the selection of primate species was the inclusion in previous studies on canine FA and competition levels. Manning and Chamberlain (1993) examined 21 primate species in their canine FA study while Plavcan and colleagues (Kay et al., 1988; Plavcan, 1990; Plavcan and van Schaik, 1992) examined several primate

species while researching canine dimorphism. Plavcan and colleagues (Kay et al., 1988;

Plavcan, 1990; Plavcan and van Schaik, 1992) developed a classification scheme used to

classify the intensity and frequency of male-male competition among primates and

referred to these as competition levels. Since publications of these works, adjustments to

primate taxonomy have occurred resulting in some subspecies being separated into

distinct species or placed into different genera. For example, Cerocebus albigena is now

Lophocebus albigena (Groves, 2001; Grubb et al., 2003; Grubb, 2006).

Following Groves’ (2001) and other sources (Hershkovita, 1949; Hayes et al.,

1990; Gippoliti, 2001; Grubb et al., 2003; Fragaszy et al., 2004; Groves, 2005; Brandon-

Jones et al., 2004; Grubbs, 2006; Groves, 2007; Ruiz-Garcia et al., 2010), the most current classification of primate species is reflected in this dissertation. With respect to families and subfamilies of platyrrhines, Groves’ (2001, 2005) taxonomy does differ from the taxonomy of Rylands and colleagues (Rylands et al., 2000; Rylands et al., 2009;

Alfaro et al., 2012; Rylands et al., 2012). The differences are minor between the two taxonomies and it appears that museums have adopted Grove’s (2001) platyrrhine taxonomy more often than Rylands and colleagues (Rylands et al., 2000; Rylands et al.,

2009; Alfaro et al., 2012; Rylands et al., 2012). Table 4 depicts changes to taxonomic

In 1990s Studies Current Classification Genus Species Subspecies Genus Species Subspecies Cercocebus albigena Lophocebus albigena Cercocebus albigena johnstoni Lophocebus albigena johnstoni Hylobates lar agilis Hylobates agilis Hylobates syndactylus Symphalangus syndactylus Hylobates syndactylus syndactylus Symphalangus syndactylus syndactylus Table 4: Taxonomic Classification – Changes from 1990s to Present

classification that have occurred since the early 1990s studies (Plavcan 1990; Plavcan and

van Schaik 1992; Manning and Chamberlain, 1993). Only species for which taxonomic

changes have occurred are listed in Table 4. Table 5 reflects the most current taxonomic

classification of the non-human primate species used in this dissertation. During analysis,

subspecies were combined to represent a single primate species. For example, the sample

sizes of the six subspecies listed for Colobus guereza were combined to represent a single

species.

Some on-line museum databases as well as collection labels have not been

updated to reflect current taxonomic classifications resulting in discrepancies between

current taxonomic classification and taxonomic classifications in museum collections.

Great efforts were taken to identify outdated taxonomic classifications and/or mislabeled specimens prior to data collection. The problem of mislabeled specimens was frequently found among Papio (e.g. Papio anubis) and Cercopithecus species.

Sample Size

Fluctuating asymmetry is exceedingly small, representing approximately 1-2% of trait size or less (Palmer and Strobeck, 1986; Palmer, 1994, 1996; Lens et al., 2002) and 71

Platyrrhines Catarrhines Ateles geoffroyi Cercopithecus cephus Hylobates hoolock leuconedyus Ateles geoffroyi ornatus Cercopithecus cephus cephodes Hylobates lar Ateles geoffroyi vellerosus Cercopithecus cephus cephus Hylobates lar carpenteri Ateles geoffroyi yucatanensis Cercopithecus mitis stuhlmanni Hylobates lar entelloides Cebus albifrons Colobus guereza Hylobates lar lar Cebus albifrons aequatorialis Colobus guereza caudatus Hylobates lar vestitus Cebus albifrons cuscinus Colobus guereza gallarum Lophocebus albigena Cebus albifrons trinitatis Colobus guereza guereza Lophocebus albigena johnstoni Cebus albifrons unicolor Colobus guereza kikuyuensis Macaca mulatta Cebus albifrons versicolor Colobus guereza matschiei Macaca mulatta mulatta Cebus apella Colobus guereza occidentalis Macaca nemestrina Cebus apella macrocephalus Gorilla gorilla Macaca nemestrina nemestrina Cebus apella paraguayanus Gorilla gorilla gorilla Pan troglodytes Cebus apella versutus Hylobates agilis agilis Pan troglodytes troglodytes Hylobates hoolock Papio anubis Hylobates hoolock hoolock Symphalangus syndactylus Table 5: Primates Included in the Dissertation Sample

is extremely sensitive signal of bilateral asymmetry (Palmer and Strobeck, 1986;

Klingenberg, 2003). To accurately measure FA, sample sizes must be large enough to discern a biological signal statistically (Smith, 1994; Palmer, 1994; Clarke, 1995; Van

Dongen, 1999; Knierim et al., 2007). Using the recommendations of Palmer (1994), minimum number of 30 specimens per grouping (e.g. sex or species) was selected.

In testing the hypotheses of this dissertation, there are several limitations. First, information on first molar and canine growth is limited to a small number of primate species. Second, sample sizes are limited by the number of specimens available in museum collections. Finally, wear, breakage, and other forms of damage to the dentition further limited the sample sizes of primate species. Taking these limitations into consideration, the sample size minimum of 30 specimens per species, or sex, was relaxed in some stages of testing in order to expand the species sample. Sample sizes never fall 72

below 10 specimens because the ability to statistically detect FA dramatically decreases

when sample sizes are within single digits (Smith et al., 1982; Palmer, 1994). In stages

where the sample size of some species falls below 30 specimens, the results of the

analysis are considered to be tentative.

Depending on the hypothesis being tested, specimens are arranged in different

groupings (e.g. sex or species). Some researchers have combined sexes when estimating first molar CFTs (e.g. Macho, 2001). Continuing with this procedure, male and female

specimens of a species were combined to calculate first molar FA for hypothesis 1 (H1).

Because the primate canine is a sexually selected structure, male and female specimens

were not combined when determining canine FA. Sample sizes are therefore different for

primate first molar and canine samples.

H1 is tested in two phases (H1a and H1b). Within the first phase of testing, H1 is

further divided into two stages. In testing H1, a minimum sample size of 30 specimens

per species was applied. To test hypothesis 2 (H2) two stages are employed. In the first

stage, only species with a minimum canine sample size of 30 specimens were used to test

H2. The sample size minimum was then lowered to a minimum of N=10 in stage 2 of H2

to expand the species sample to include additional platyrrhine and catarrhine species.

Species used to test hypothesis 3 (H3) are constrained by the availability of known lateral

EFTs. The sample size minimum was relaxed for testing H3 in order to increase the species sample used. Listing of species and sample sizes used to test the three hypotheses can be found in the respective results chapters.

Methods

Variables

Non-metric Variables

This dissertation utilizes several non-metric variables including 1) CFTs of

1 primate maxillary first molars (M ) and mandibular first molars (M1) ; 2) life history

(LH) schedules; 3) weaning ages; 4) lateral EFTs of maxillary and mandibular canines

1 (C and C1) ; and 5) competition levels. The following discussion details why these

variables were selected and the literature sources from where the information was

retrieved. Additional details are available in the results chapters.

Eruption sequences and histological evidence has provided information on the

pattern of tooth formation in several primate species. Initially, studies on radiographs

evaluated eruption sequences and estimated crown formation timing of teeth (e.g. Beynon

et al., 1991; Reid et al., 1998). A pivotal study on CFTs of extant non-human hominoid

genera provided the first histological estimated CFTs (Reid et al., 1998). Since the

publication of Reid and colleagues (1998), further evidence has emerged demonstrating

that radiographs tend to underestimate CFTs (Schwartz et al., 1996). To ensure the use of

accurate first molar CFTs, the most recent first molar CFTs available in the literature are

utilized (Table 6).

In studies where the first molar CFTs are given for only two or three individuals,

mean CFTs were used to represent the CFTs of species. For instance, Dirks’ (2003) study

provides first molar CFTs for two individuals of Papio anubis. Several studies on CFTs

First Molar CFTs (yrs) References Kelley Beynon Reid Dirks Kelley and Schwartz Smith and CFTs et al et al Shellis Dirks et al Dirks Schwartz et al et al Schwartz Utilized in Species (1991) (1998) (1998) (1998) (2002) (2003) (2005) (2006) (2007) (2010) this study

M1 Gorilla gorilla 2.85 2.53 2.53 2.217‐ Pan troglodytes 2.73 2.32 2.417 Ateles geoffroyi 1.59 1.59 75

M1 Gorilla gorilla 2.90 2.30 2.81 2.81 2.175‐ Pan troglodytes 2.85 1.46 2.40 2.63 Hylobates lar 1.32 1.10 1.10 Macaca mulatta 1.00 1.00 1.28, Papio anubis 1.36 1.44

Table 6: References and First Molar Crown Formation Times for Testing H1a

average the resulting individual CFTs to produce a single number representative of the

species or sex of a species (e.g. Macho, 2001). Other studies provide CFT ranges for a

1 species. Of all the primate species in this study, only M and M1 CFTs of Pan were given

as ranges in the literature (Smith et al., 2007). The first molar mean CFT range for Pan

(Smith et al., 2007) will be used when making comparisons between species Pan’s first

molar FA and the first molar FA of other species. Using the mean of Smith and colleagues’ (2007) CFT range for Pan troglodytes allows for P. troglodytes’ first molar

CFT to be represented by a single age instead of an age range. Because other species’

CFTs were not represented by age ranges, calculating an average CFT for Pan allows for comparisons between Pan and other primate species.

H1b further tests if growth duration is associated with variation in FA of the

primate first molar by employing life history (LH) schedules as a proxy for

developmental timing. First molar CFTs are limited to a small set of primate species

(Table 6). As such, the pace of LH is utilized to achieve a broader sampling of primate

species. LH schedules are evaluated on a continuum of ‘slow’ to ‘fast’. Although this

classification prevents comparisons within genera or between genera of the same subfamily, it does allow for phylogeny to be considered because first molar FA is examined in 13 primate species.

In addition to LH schedules, weaning ages were also used as a variable in testing

H1b (Table 7). Weaning ages have been reported to be tightly correlated with first molar

CFTs in anthropoid primates (Macho, 2001). Similar to the other non-metric variables used to test the hypotheses, weaning ages were obtained from the literature

Weaning Age (yrs)* Harvey and Godfrey Species Clutton‐Brock et al (1985) (2001) Ateles geoffroyi 2.25 Cebus albifrons 0.75 Cebus apella 1.14 Colobus guereza 1.08 Gorilla gorilla 3.50 Hylobates hoolock 1.92 Hylobates lar 1.50 Lophocebus albigena 0.58 Macaca mulatta 0.88 Macaca nemestrina 1.00 Pan troglodytes 5.00 Papio anubis 1.60

Table 7: Weaning Ages of Primate Species for Testing H1b

(Harvey and Clutton-Brock, 1985; Godfrey et al., 2001). When a species’ weaning age was available from more than one source the weaning age reported in the most recent source was used.

Both H2 and H3 utilized canine lateral EFTs. Hard tissues, such as enamel, are characterized by circadian rhythms (Hillson, 1996; Smith et al., 2006). During tooth development, amelobasts secrete enamel. At the enamel-dentine junction, ameloblasts differentiate and move towards what will eventually become the tooth crown surface. As the ameloblasts migrate they create a developing enamel front which is preserved as long-period incremental structures known as striae of Retzius (Hillson, 1996; Hillson and

Bond, 1997). The striae of Retzius are structures resulting from periodic interruptions occurring during ameloblast secretion. The portion of the tooth enamel that covers the

77 lateral surfaces of the tooth is the imbricational, or lateral, enamel. In the lateral enamel, striae contact the enamel surface and form circumferential rings called perikymata

(Hillson, 1996; Hillson and Bond, 1997). Perikymata represent external manifestations of the underlying striae of Retzius (Guatelli-Steinberg, 2001; Guatelli-Steinberg et al.,

2009; Hillson, 1996; Reid and Dean, 2006) (Figure 2). Because perikymata occur at regular intervals in the teeth of individuals, counting perikymata provides an estimation of time taken to form enamel (Guatelli-Steinberg et al., 2009; Reid and Dean, 2006; Reid and Ferrell, 2006; Ten Cate, 1994). Periodicity refers to the number of days each perikymata represents (Guatelli-Steinberg et al., 2009).

Figure 2: Tooth Section Depicting the Relationship of Striae of Retizus to Perikymata

(Figure courtesy of Guatelli-Steinberg)

Lateral EFTs were taken from the literature (e.g. Schwartz and Dean, 2001;

Guatelli-Steinberg et al., 2009) or determined through raw data provided by 78

Average Average Average Mean Periodicitiy Estimated Mean Periodicitiy Estimated Periodicitiy Estimated Age Age Mean Age 80% N Range Age 90% N Range Age N Range Age (days; (days; pk (days; pk (Avg) Range pk (Avg) Range (Avg) Range Species yrs) yrs) yrs) Ateles 655.2; 729.2; 163.8 5 4 (4) 655.2 182.3 3 4 (4) 729.2 ‐‐ 4 (4) ‐‐ geoffroyi 1.80 2.00 Cebus 862.5‐ 948.75; 172.5 4 5, 6 (5.5) ‐‐5, 6 (5.5) ‐‐‐‐5, 6 (5.5) ‐‐ albifrons 1035 2.60 741.6; 760.5; Cebus apella 164.8 5 4,5 (4.5) 659.2‐824 169 3 4,5 (4.5) 676‐845 ‐‐4,5 (4.5) ‐‐ 2.03 2.08 Cercocebus 231.5 4 ‐‐‐252 1 ‐‐‐‐‐‐‐‐ atys Cercocebus 1081.2; 245 4 4 (4)+ 980 980; 2.68 270.3 3 4 (4) 1081.2 ‐‐ ‐ ‐ ‐ torquatus 2.96 Cercopithecus 1004; 1228; 79 225.8 4 4 (4)+ 903 903; 2.47 251 2 4 (4) 1004 307 1 4 (4) 1228 mitis 2.75 3.36 Hylobates 274 8 ‐‐‐281 2 ‐‐‐‐‐‐‐‐ agilis Hylobates lar 4 (4) ‐‐‐‐4 (4) ‐‐‐‐4 (4) ‐‐ Symphalangus 1110‐ 1248.75; 1386; 277.5 2 4,5 (4.5) 308 1 4,5 (4.5) 1386 ‐‐4,5 (4.5) ‐‐ syndactylus 1387.5 3.42 3.80 Macaca 889.2‐ 1000.35; 1093.5; 1165.5; 222.3 3 4,5 (4.5) 243 1 4,5 (4.5) 972‐1215 259 1 4,5 (4.5) 1036‐1295 nemestrina 1111.5 2.74 3.00 3.19 1057.2; 1212; Papio anubis 176.2 5 5,7 (6) 881‐1233 202 3 5,7 (6) 1010‐1414 ‐‐5,7 (6) ‐‐ 2.90 3.32 Pan 1995; 2198; ‐‐ ‐ ‐ ‐‐ ‐ ‐ ‐‐ ‐ ‐ ‐ troglodytes 5.47+ 6.02+ 2443; 2755; ‐‐ ‐ ‐ ‐‐ ‐ ‐ ‐‐ ‐ ‐ ‐ Gorilla gorilla 6.72+ 7.55+ Table 8: Mean Lateral Enamel Formation Times for 80% and 90% Crown Height* *Information for this table was primarily obtained from Guatelli-Steinberg and colleagues (2009) or from unpublished data collected by Dr. Guatelli-Steinberg. +Both periodicity information for C. torquatus and C. mitis and lateral EFTs of the great apes were provided by Dr. Schwartz.

Guatelli-Steinberg and Schwartz (Table 8). Only male lateral EFTs are listed in Table 8.

With the exception of the great apes, data collected on perikymata (pk) by Guatelli-

Steinberg were used to determine C1 lateral EFTs (Table 8). Because data on pk/striae

counts were not available for the full crown height of primate species studied by Guatelli-

Steinberg and colleagues (2009), pk/striae counts for 80% crown height and

90% crown height was used. Periodicities for each species were applied to both mean

pk/striae counts for 80% crown height or 90% crown height to determine an average C1 lateral EFT estimate for each species. Mandibular canine lateral EFTs of great apes were derived from data available in Schwartz and Dean (2001) and confirmed through personal communication with Schwartz. Average lateral EFTs for both mean pk/striae counts for

80% crown height or 90% crown height of C1 were determined for G. gorilla and P. troglodytes. Table 8 outlines mean pk/striae counts for 80% crown height and 90% crown height, the number of specimens from which those means were generated, range and average periodicities, estimated C1 lateral EFTs, and average C1 lateral EFT of all primate

species for which C1 lateral EFTs are available. Due to sample size restrictions, not all of

the species listed in Table 8 were used to test H3.

Comparisons used in H3 control for lateral EFTs (Schwartz and Dean, 2001;

Guatelli-Steinberg et al., 2009) and competition levels (CL) (Kay et al., 1988; Plavcan

and Kay, 1988; Plavcan, 1990; Plavcan and van Schaik, 1992). Canine lateral EFTs are

discussed above and available in Table 8. Competition levels represent a classification

scheme for the strength of sexual selection. Unlike using mating systems, the traditional classification of the strength of sexual selection, the classification scheme using CLs

80 incorporates information on behavior and demography (Plavcan and van Schaik, 1992;

Plavcan, 2011). Therefore exaggerated male traits are assumed to be associated with the frequency and intensity of male-male competition (Plavcan, 2011). Thus, CLs represent an empirical measure of competition among primate species based on intensity and frequency of intra-male competition (Plavcan, 1990; Plavcan and van Schaik, 1992).

Furthermore, when monogamous species are removed from the analysis, a strong relationship between CLs and dimorphism is still present (Plavcan, 2011). This result is not found in the mating system classification of the strength of sexual selection (Harvey et al., 1978).

The classification of primate species into CLs for this dissertation is based on the work by Plavcan and colleagues (Kay et al., 1998; Plavcan, 1990; Plavcan and van

Schaik, 1992). Subspecies fall under the same CL as their species. For example,

Hylobates lar entelloides is classified under the same CL as Hylobates lar. Primate species H3 are listed in Table 9 under their respective CLs. Competition level one (CL1) represents low frequency of inter-male competition and low intensity behavior. High frequency and low intensity describes competition level two (CL2) while low frequency and high intensity represent competition level three (CL3). Finally, high frequency inter- male competition and high intensity behavior represent competition level four (CL4).

Metric Variables

As a tooth grows from cusp to cervix, there is potential for growth to be disrupted over the course of development. Because mesio-distal (MD) and bucco-lingual (BL)

CL1 CL2 CL3 CL4 Ateles Hylobates lar Cebus albifrons Cebus apella geoffroyi Pan Cercopithecus Macaca nemestrina troglodytes mitis Gorilla gorilla Papio anubis

Table 9: Competition Levels of Primate Species Used to Test H3

canine maximum dimensions of the canine crown occur close to the cervix, these

dimensions should reflect the cumulative effect of growth disruptions through the entire

length of crown formation. Canine crown height has been reconstructed from basal canine crown dimensions, suggesting that MD and BL dimensions do reflect sexual selection (Plavcan et al. 2009).

In several studies utilizing canine dimensions, canine height is the primary dimension used (e.g. Plavcan, 1990; Greenfield and Washburn, 1991; Greenfield, 1992;

Plavcan and van Schaik, 1992; Manning and Chamberlain, 1993, 1994; Plavcan et al.,

1995; Plavcan, 2000, 2001, 2004; Leigh et al., 2008). Because wear associated with the measurement of canine height could result in inflated values of canine FA this study will utilize canine dimensions not affected by use-related wear. MD and BL dimensions are used to accurately isolate developmental asymmetry. MD and BL dimensions of the first molar and canine were measured following standardized methods for collecting dental measurements using a fine-tipped Mitutoyo digitmatic caliper calibrated to the nearest

0.01mm.

Following the definitions of Plavcan (1990) and Plavcan and colleagues (2009), measurements of the MD and BL dimensions of the primate first molar and canine were

taken. MD measurement of the first molar is taken along the mesio-distal axis at the

1 greatest dimension of the molar (Plavcan, 1990). The BL measurement of M and M1 is

taken at “greatest dimension orthogonal to the mesiodistal length,” (Plavcan et al., 2009,

p.4).

1 The length of the canine teeth (C and C1), or MD dimension, is defined as the

“longest axis as viewed in the occlusal plane,” (Plavcan, 1990, p.38). This definition applies to all canine teeth other than the C1 of catarrhines because the prominent mesial

groove of this tooth type requires a slightly differ definition for the MD dimension. As

such, the MD dimension of catarrhines C1 is described as “from the distal edge of the

‘blade’ of the tooth to the portion of the tooth buccal to the mesial groove,” (Plavcan,

1 1990, p.38). The breadth, or BL dimension, of the canine teeth (C and C1) for all species

included in the dissertation is “the greatest dimension perpendicular to the length,”

(Plavcan, 1990, p.38).

Data Collection

Museum and University Collections

The number of specimens per species studied at each museum and university

collection is listed in Appendix A. Museum on-line databases were utilized prior to

arrival at the collection in order to estimate the availability of species and approximate

sample sizes. Such information allowed for research trips to be successfully planned .

These databases allowed several taxonomic discrepancies to be identified prior to

arriving at the collection. Of all the databases available, the database at National Museum

of Natural History was the most informative because it was up-to-date on current taxonomic classification and also contained detailed information on previous

classification schemes.

Although generally reliable, museum on-line databases, collection boxes, and/or skull tags can contain inaccurate information on age and/or sex. Out of all the specimens examined a very small percentage showed discrepancies in age or sex. When discrepancies did occur they were commonly a result of information not matching between the online database, collection boxes and/or skull tags. When discrepancies were identified, the skull tag or collection box label was used to determine the age and/or sex of the specimen. If demographic features could not be determined, the specimen in question was measured but excluded from the analysis.

Examination of Dentition

Prior to measuring, the dentition of each specimen was examined for anomalies. If anomalies were observed on first molars or canines then that tooth was not measured for the specimen. If another tooth type, such as the premolar, exhibited an anomaly, canines and first molars were measured as long as they were not affected by the anomaly. The developmental anomaly commonly observed was the appearance of a fourth molar. Teeth of specimens with fourth molars were measured but not included in testing of the hypotheses because it is possible that specimens with an additional tooth could either be prone to developmental perturbations resulting in a skewed FA estimate or may exhibit

FA that does not reflect underlying developmental noise. The location (e.g. quadrant) and

any descriptive information that could be pertinent for future studies were recorded in my notes.

Each specimen was also examined for dental wear. Since equivalent degrees of tooth wear are not known to occur bilaterally, measuring a tooth with wear could result in

the incorporation of measurement error into measurement. The presence of measurement

error in the measurement could cause a skewed or inflated FA estimate that is not a result

of developmental perturbations. Due to this concern, tooth wear is ranked on a three

category system following Plavcan (1990) where the extent of wear is defined “by the

proportion of dentin exposed on the tooth crown,” (Plavcan, 1990, p.42). The three

categories used to classify wear are light wear, moderate wear, and heavy wear. Only the

canines and first molars were assessed for wear. For both tooth types, when light wear

was observed the tooth was measured. In cases where moderate or heavy was observed

but MD and BL dimensions were not influenced, both measurements were recorded.

However, when MD or BL dimensions were affected by moderate or heavy wear, that dimension was not recorded for the specimen. Thus, in some cases a specimen may have a canine MD measurement but not a BL dimension for that canine tooth.

Data Collection Procedure for Metric Variables

Fine-tipped Mitutoyo digitmatic sliding calipers were used to measure MD and

BL dimensions of the primate canine and first molar to the nearest 0.01mm. By following the definitions of MD and BL dimensions provided by Plavcan (1990) for both primate tooth types, the tips of the sliding calipers will be placed in the same location on all specimens measured. 85

To ensure that FA was estimated accurately, a measurement protocol was

established to minimize measurement error while also sufficient for a study requiring repeated measurements. The first part of the measurement protocol focuses on the pattern in which canines and first molars are measured to ensure that each dimension for every specimen is done in the same order. The left side followed by the right side of all mandibular dentition is measured first. Next, maxillary dentition is measured beginning with the left side and concluding with the right side. For both mandibular and maxillary dentition, canines are measured first followed by first molars. Following this measurement protocol, the left mandibular canine is the first tooth measured while the maxillary right first molar is the last tooth measured for every specimen. Since each measurement is taken three times, the pattern described above was repeated three times for each specimen. This step follows the recommendation that repeated measurements should be taken ‘blindly’ (Palmer and Strobeck, 2003; Knierim et al., 2007). By performing the measurement protocol three times in a row, repeated measurements are not being taken immediately after each other and session bias is being taken into account as recommended by David and colleagues (1999). A total of 48 measurements (six per canine; six per first molar) were taken per specimen. If a particular tooth was not available, the measurement protocol was not deviated from. Rather, dentition unavailable for measurement was ‘skipped’ in the measurement pattern. Notes were taken to clarify why the tooth was ‘skipped’ during measurement.

Following the methodological recommendations in the literature (e.g. Palmer and

Strobeck, 2003; Knierim et al., 2007), specimens were measured at random so that

individuals of similar species and sex are not measured in order. In museums collections,

where more than one species could be out of the cabinets at once, at least two species of different sizes or genera were taken to the workspace and measured alternatively.

Following this measurement protocol achieved the methodological recommendations of

Palmer and colleagues (e.g. David et al., 1999; Palmer and Strobeck, 2003; Knierim e t al., 2007) because it prevented a rhythmic pattern of measuring the dentition from developing.

Analytical Phase

Prior to FA being calculated, several important steps to evaluate the dataset were conducted to ensure that FA estimates were more likely to reflect developmental noise.

Following the recommendations of Palmer and colleagues (Greene, 1984; Palmer and

Strobeck, 1986; Palmer, 1994; Sokal and Rohlf, 1995; Van Dongen, 1999; Palmer and

Strobeck, 2003; Knierim et al., 2007), the following protocol was followed: 1) examining the dataset(s) for departures from normality; 2) calculating skew and kurtosis; 3) accounting for measurement error; and 4) examining the dataset(s) for directional asymmetry (DA) and antisymmetry (AS) other than FA. All statistical analyses were performed in Statistical Analysis Software (SAS) unless otherwise noted.

Accounting for Departures from Normality

Although measurement error, DA, and AS all contribute to departures from normality, they are not the only reasons why a distribution might deviate from normality.

First, the distribution of was visually examined for departures from

normality. In cases where departures were observed, the raw data were reevaluated to

determine if a data entry error had been made. In all cases where the data departed from

normality a data entry mistake had been made resulting in the distribution departing from

normality. These mistakes were corrected and the distribution was rechecked for

normality. Following a visual examination of the distribution, both skew and kurtosis of

the frequency distribution were computed. Equations for computing both skew and

kurtosis were taken from literature sources (Sokal and Rohlf, 1995; Palmer and Strobeck,

2003). Skew was computed as:

The equation for skew was taken from Palmer and Strobeck’s (2003) book

chapter which follows Sokal and Rohlf’s (1995) explanation for skew. In this equation, N is the sample size, represents the value of X for individual , is the sample mean and SD is the standard deviation of the sample (Palmer and Strobeck, 2003).

The variables (e.g. sample size, standard deviation, etc.) for skew and kurtosis

equations are similar. Kurtosis was computed as: 3. The constant 3

in the kurtosis formula is an arbitrary correction (Palmer and Strobeck, 2003). If left

uncorrected, 3 for a normal distribution. Therefore, this correction ensures that

0 for a normal distribution and, since skew is zero for a normal distribution without

a correction, the correction also makes the values of kurtosis parallel to the values of

skew (Palmer and Strobeck, 2003).

Palmer and Strobeck (2003) recommend first computing skew and kurtosis for the

smallest subsamples of interest followed by repeating computations for skew and kurtosis

at the next highest subsample of analysis. This procedure was followed. In most cases, the sex of a species represented the smallest subsample in this dataset. The highest

subsample in the dataset is represented by the combination of male and female specimens of a species for determining first molar FA in H1.

Accounting for Measurement Error

It has long been recognized that FA can be easily confounded by measurement error (Greene, 1984; Palmer and Strobeck, 1986; Palmer, 1994). The significant of measurement error relative to FA is commonly accessed through repeated measurement of at least part of the dataset and the use of a two-way mixed model ANOVA (sides x individual) (Palmer and Strobeck, 1986; Van Dongen et al., 1999). In this dissertation,

repeated measurements were performed three times for each dental dimension of every

1 1 tooth examined. When all four teeth (C , C1, M , and M1) of a specimen were measured,

a total of 48 measurements were taken.

The two-way mixed model ANOVA (sides x individual) will be performed for

1 1 each tooth (C , C1, M , and M1). A significant sides x individual interaction illustrates the

significance of FA relative to ME (Palmer and Strobeck, 1986).

Accounting for Other Forms of Bilateral Asymmetry

Testing for the presence of DA and AS represents an important step in any FA

study for two reasons. First, both of these forms of asymmetry are not believed to

represent the underlying DN (Klingenberg, 2003). Since FA indices are sensitive to these

forms of asymmetry if DA and AS are not taken into account inflated FA estimations

might result (Palmer and Strobeck, 2003).

Testing for DA in a dataset was done through one-sample t-test comparing

to zero (Palmer and Strobeck, 1986; Palmer, 1994; Palmer and Strobeck,

2003). The results of this comparison illustrates if differs significantly

from zero. A distribution that differs significantly from a mean of zero could indicate the presence of DA. If the direction of the distribution leans towards one side, then the dataset is believed to contain significant DA (Palmer and Strobeck, 2003). However, if the distribution is not directed towards one side of zero then either DA is weak but still present or DA is not present in the dataset.

If DA is weak the distribution will be asymmetrically distributed around the mean instead of being distributed to only one side. An asymmetrical distribution could represent a mixture of ideal FA and weak DA (Palmer and Strobeck, 2003). With a weak signal of DA, it can still possible to determine FA estimates for a dataset as long as a FA index not sensitive to DA is applied. Because a universal rule for determining when DA is too weak to influence FA variation is not available, Palmer and Strobeck (2003) suggest that if DA is not larger than FA4 √ then more than likely DA is not significant enough to inflate FA variation.

If AS is present in the distribution the will show a distinctive valley

between two peaks that are equal distance from zero (Palmer and Strobeck, 2003). The

distribution of signed asymmetry will be platykurtically distributed if AS is not present

(Leung and Forbes, 1997; Van Dongon, 2006).

Direction asymmetry and antisymmetry were not detected in any of the primate

samples used in this dissertation. As mentioned above, the deviations observed in the

distribution were due to data entry errors. These errors were corrected prior to FA being

calculated.

Overview of Statistical Analysis for Fluctuating Asymmetry ( )

A two-way mixed-model ANOVA with repeated measures, where sides are fixed

and individuals are random was used to determine FA ( ) (Knierim et al. 2007; Palmer and Strobeck 1986, 2003). Size and shape variation was eliminated as sources of

variation by dividing each side by . This calculation was built into the SAS

program for analysis of FA ( ).

Calculation of Fluctuating Asymmetry ( )

FA ( ) was evaluated by employing the difference in variance between the mean

square of the remainder and error divided by the number of replications

from two-way mixed model ANOVA.

Size variation was eliminated by using a size correction of each measurement as

/ /2. An F-test with the degrees of freedom adjusted to follow the 91

Satterthwaite’s formula for for independent variances was used to determine if

difference in were significant (Satterthwaite, 1946; Palmer and Strobeck 1986; Sciulli

2003). Satterthwaite formula reduces the degrees of freedom for the sample making it an appropriate calculation to use when degrees of freedom are small. The Satterthwaite

formula is:

Using the information provided from the two-way mixed model ANOVA, FA

estimates were calculated by hand. Calculation of FA will be done using index FA10a:

Palmer and colleagues (Palmer and Strobeck, 1986; Palmer, 1994; Van Dongen,

1999; Palmer and Strobeck, 2003; Knierim et al., 2007) note that even though FA

estimates based on FA10a can be time consuming to compute the benefits of using this

FA index outweigh any potential pitfalls. The major advantage of FA10a is that it describes the average difference between sides after ME has been factored out (Palmer

and Strobeck, 1986; Palmer, 1994; Palmer and Strobeck, 2003).

Depending on the hypothesis being tested, dental FA will be compared among

primate species or between sexes of a single primate species. A difference in FA between

two primate species, or the sexes of a primate species, is considered significant at α =

0.05.

Summary

This chapter provided descriptions on the materials and methods common to the

results chapters. The selection protocol for non-human primate species was presented in

addition to taxonomic concerns within museum collections. The rationale behind the

exclusion of a tooth or specimen was discussed as well as the protocol for assessing wear

and/or damage of the dentition. Also, the measurement protocol for collecting dental

metric data was outlined. The final section of this chapter reviewed analytical protocols

for calculating FA which are specific to this dissertation. Any additional methods used in

this dissertation are described in the appropriate results chapter.

CHAPTER 5: FLUCTUATING ASYMMETRY OF PRIMATE FIRST MOLARS: ASSOCIATION WITH GROWTH DURATION

Introduction

This chapter meets one of the main objectives of this dissertation: it tests the

association between fluctuating asymmetry (FA) and first molar growth duration. To

1 meet this objective, first molar (M and M1) crown formation times (CFTs) are used to

predict variation in first molar FA for eight primate species.

Two important limitations are associated with using first molar CFTs of primate species as the basis for testing for an association between FA and growth duration. First,

this chapter is limited to testing Hypothesis 1a (H1a) on a small number of primate

species because CFTs are available for only a few species (Table 6). Moreover, for those

species for which M1 CFTs are known sample sizes were limited by what was available

in museum collections and what was available in museums was further limited by wear,

breakage, or other forms of damage to the dentition. This limitation resulted in a small

sampling of primate species (N=8) to test H1a. The small number of species samples

precluded phylogenetically controlled comparisons.

Hypothesis 1a (H1a) states that species with longer first molar CFTs will exhibit

greater FA than species with shorter first molar CFTs. H1a is tested in two stages. In both

stages of testing only species with a minimum sample size of 30 or more are analyzed. In

stage 1 of testing, sample sizes among the species are not equal. FA estimates for M1 and

M1 were calculated and compared among one platyrrhine and five catarrhine species. In

stage 2, samples sizes are reduced to be equivalent with the lowest sample size of the six

1 species analyzed in stage 1 (Table 10). Thus, in stage 2 H1a is tested using M and M1

FA calculated from one platyrrhine and five catarrhine species, but the sample sizes among the six species are equal. Based on CFT data available (Table 10; Figure 3), the following predictions for testing H1a under the framework of stages 1 and 2:

1. Prediction 1a.1: FA of M1 should be lower in Hylobates lar relative to Gorilla

gorilla and Pan troglodytes.

1 2. Prediction 1a.2: Gorilla gorilla should exhibit the greatest FA for M and M1.

3. Prediction 1a.3: M1 FA of Ateles geoffroyi should fall below M1 FA of Gorilla

gorilla and Pan troglodytes.

4. Prediction 1a.4: M1 FA of Papio anubis should fall between M1 FA of

Hylobates lar and the great apes, represented by Gorilla gorilla and Pan

troglodytes.

5. Prediction 1a.5: Macaca mulatta should express the lowest M1 FA.

Stage One Description

1 Table 6 (see Chapter 4) lists M and M1 CFTs available in the literature for three

Papio species (Shellis, 1998; Dirks et al., 2002), Symphalangus syndactylus (Dirks,

2003), and Pongo pygmaeus (Beynon et al., 1991; Kelley and Schwartz, 2010).

Unfortunately, it is not possible to include Papio cynocephalus, Papio hamadryas, Pongo

pygmaeus, and Symphalangus syndactylus in testing H1a due to small sample sizes of

these species. Prediction 1a.1 is examined using species of lesser and great apes.

Although all six species will be used to investigate Prediction 1a.2, a different

combination of species will be examined for each first molar (e.g. M1 = three species;

1 M1= five species). To examine Prediction 1a.3, M FA estimates are compared between

Ateles and the two great ape species. To test predictions 1a.4 and 1a.5, M1 FA estimates

of all catarrhine species are compared. For all predictions, bucco-lingual (BL) and mesio- distal (MD) dental dimensions are examined separately as well as multiplied together to represent molar crown (CA) area.

Stage Two Description

Stage 2 uses the same predictions as Stage 1 but sample sizes among the species are equivalent (Table 10). As noted in Chapter 4, sample size variation among different groups has the potential to greatly influence the interpretation of results (Smith et al.,

1982; Palmer, 1994). For example, comparing a FA estimate of a species represented by over 100 specimens (e.g. G. gorilla) to a FA estimate of a species with a sample size of less than 70 specimens (e.g. A. geoffroyi), may not provide a clear picture on the variation

1 of M and M1 FA across these species.

Samples sizes of species were matched to the lowest sample size for each first

molar. For M1, A. geoffroyi had the lowest sample size (Table 10). P. troglodytes (N=69) has the lowest sample size for the MD dimension of M1 while P. troglodytes and M.

mulatta both had the lowest sample size for M1 BL (N=69) (Table 10). During data

Sample Sizes Crown Formation Time (yr)* Stage 1 Stage 2

1 1 1 1 1 1 1 M BL M MD M1 BL M1 MD M CA M1 CA M BL M MD M1 BL M1 MD M CA M1 CA M M1 Species Gorilla 143 145 143 144 142 142 41 43 69 69 40 68 2.53 2.81 gorilla Pan 72 74 69 69 72 68 41 43 69 69 40 68 2.31 2.40 troglodytes Hylobates - - 126 128 - 123 - - 69 69 - 68 - 1.10 lar 97 Macaca - - 69 71 - 68 - - 69 69 - 68 - 1.00 mulatta Papio - - 99 99 - 97 - - 69 68 - 68 - 1.36 anubis Papio ------1.47 hamadryas Ateles 41 43 n/a n/a 41 - 41 43 - - 40 - 1.59 - geoffroyi

Table 10. Sample Sizes and CFTs of Primate Species Used to Test H1a

Maxillary First Molar Mandibular First Molar

Low FA Magnitude Ateles geoffroyi Macaca mulatta

Pan troglodytes Hylobates lar

Gorilla gorilla Papio anubis

Pan troglodytes

Gorilla gorilla

Elevated FA Magnitude

Figure 3. Predicted Fluctuating Asymmetry Magnitudes Among Platyrrhine and Catarrhine Species

collection each specimen was assigned an individual (IND) number. IND numbers

eliminate the possibility of conflicting museum specimen numbers while also identifying the specimen in statistical analyses. Using IND numbers, G. gorilla and P. troglodytes

sample sizes were reduced to that of A. geoffroyi by randomly selecting 43 individuals

and 41 individuals for the MD and BL dimensions of the M1, respectively. For M1, the sample sizes of species were reduced to match the sample size of P. troglodytes (N=69).

The same IND numbers randomly obtained for M1 and 26 additional IND numbers were used to construct the sample size for G. gorilla’s mandibular first molar. Sixty-nine IND numbers of H. lar, M. mulatta, and P. anubis were randomly selected to match the M1 sample size of P. troglodytes. IND numbers were randomly selected using the

RANDBETWEEN command in Microsoft® Excel. After IND numbers were selected,

MD and BL data for those individuals were pulled from the database and organized for

SAS input. Following the guidelines of Palmer and Strobeck (1986, 2003), dental metric 98

data for each species were evaluated for the presence of outliers. Through an evaluation of the data, a single outlier for both H. lar (M1 BL) and P. anubis (M1 MD) were identified as being associated with data entry errors. Both errors were fixed by replacing the incorrect dental dimension with the correct one from original data sheets.

Results

Stage 1

Results of the two-way mixed model ANOVA for stage 1 of H1a are available in

1 Appendix B. Table 11 lists the FA estimates of M and M1 for species included in stage 1.

Table 12 summarizes the results of the F-tests used to determine the significance of differences between FA estimates in the primate species included in stage 1 of Ha1.

Stage 1, H1a Maxillary Mandibular SpeciesBLMDCABLMDCA Gorilla gorilla 1.68x10‐4 1.85x10‐4 2.59x10‐4 1.35x10‐4 2.38x10‐4 6.81x10‐4 Pan troglodytes 3.45x10‐4 2.27x10‐4 5.78x10‐4 4.68x10‐4 6.50x10‐4 9.94x10‐4 Hylobates lar ‐‐‐1.18x10‐4 8.52x10‐5 1.25x10‐4 Macaca mulatta ‐‐‐1.24x10‐5 3.97x10‐5 1.52x10‐5 Papio anubis ‐‐‐2.34x10‐5 6.21x10‐5 5.94x10‐5 ‐5 ‐5 ‐5 Ateles geoffroyi 2.37x10 2.18x10 4.71x10 ‐‐‐ Table 11. Maxillary and Mandibular First Molar FA Results

G. gorilla vs. A. G. gorilla vs. P. geoffroyi troglodytes G. P. H. M. P. A. gorilla troglodytes lar mulatta anubis geoffroyi Tooth & Dimension df df df df df df F ‐ratio PF‐ratio P M1 BL 142 71 ‐‐ ‐ 36 7.09 0.0001 2.05 0.0002 M1 MD 142 73 ‐‐ ‐ 35 8.49 0.0001 1.23 0.1447 M1 Crown Area 142 71 ‐‐ ‐ 35 5.50 0.0001 2.23 0.0001

M1 BL 142 67 121 60 93 ‐ 3.46 0.0001

M1 MD 138 68 108 56 97 ‐ 2.73 0.0001

M1 Crown Area 103 67 113 66 97 ‐ 1.46 0.0415

100

Continued Table 12. F-tests Stage 1, H1a Bolded p-values are statistically significant

100

Table 12 continued

G. gorilla vs. H. G. gorilla vs. M. G. gorilla vs. P. P. troglodytes vs. P. troglodytes vs. P. troglodytes vs. P. troglodytes vs. lar mulatta anubis A. geoffroyi H. lar M. mulatta P. anubis

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P 14.56 0.0001 10.44 0.0001

101 12.28 0.0001 1.15 0.2145 109.08 0.0001 5.79 0.0001 3.98 0.0001 37.76 0.0001 20.05 0.0001 2.79 0.0001 59.90 0.0001 3.83 0.0001 76.31 0.0001 163.77 0.0001 10.46 0.0001 5.46 0.0001 44.80 0.0001 11.46 0.0001 7.96 0.0001 65.37 0.0001 16.73 0.0001

Continued

101

Table 12 continued

H. lar vs. M. H. lar vs. P. M. mulatta vs. P. mulatta anubis anubis

F ‐ratio PF‐ratio PF‐ratio P

9.48 0.0001 5.04 0.0001 1.88 0.0048 2.14 0.0010 7.29 0.0001 15.65 0.0001 8.21 0.0001 2.1 0.0001 3.91 0.0001 102

102

103

Figure 4. Mandibular First Molar FA Estimates of Apes, H1a Stage 1

103

Prediction 1a.1

Results support prediction 1a.1: M1 FA is lower in Hylobates lar relative to Pan troglodytes and Gorilla gorilla (Figure 4). Differences in M1 FA between H. lar and P.

troglodytes were found to be significantly different in all three dimensions (Table 12).

With the exception of M1 BL, statistically significant differences were found between H.

lar and G. gorilla. The results of this prediction lend support to the hypothesis that first

molar crowns forming over a long period of time are associated with elevated FA

estimates.

Prediction 1a.2

The results do not support prediction 1a.2: G. gorilla does not exhibit the greatest first molar FA (Table 11; Figures 5 and 6). As outlined in prediction 1a.2, G. gorilla

1 should express the greatest M and M1 FA because their first molars take the longest

amount of time to form relative to the other five species used in stage 1 (Schwartz and

Dean, 2001; Schwartz et al., 2006). Rather, the greatest FA is expressed in the first molars of P. troglodytes. FA estimations of G. gorilla and P. troglodytes differ

1 significantly in both the BL and CA dimensions of M and M1 (Table 12; Figures 5 and

6). First molar FA in the MD dimension does not differ significantly between P.

troglodytes.

Results of prediction 1a.2, at least in reference to FA estimates of the great apes,

do not lend support to the WOV hypothesis that growth duration is associated with first

molar FA. However, it is important to note that results do indicate that G. gorilla and P.

104

0.00060000

0.00050000

0.00040000 Estimate

0.00030000 105 Asymmetry

Fluctuating 0.00020000

0.00010000

0.00000000 P. troglodytes G. gorilla A. geoffroyi

Species BL MD CA

Figure 5. Maxillary First Molar FA Estimates, H1a Stage 1

105

0.00120000

0.00100000

0.00080000 Estimate

0.00060000 106 Asymmetry

0.00040000 Fluctuating

0.00020000

0.00000000 P. troglodytes G. gorilla H. lar M. mulatta P. anubis

Species BL MD CA

Figure 6. Mandibular First Molar FA Estimates of Catarrhines, H1a Stage 1

106

troglodytes exhibit M1 FA estimates that are significantly greater than the other species

used to test H1a (Table 12).

The results of prediction 1a.2 also indicate that M1 FA of P. troglodytes not only

exceeds M1 FA of the other primate species examined in stage 1 (Table 11) but that M1

FA estimates of P. troglodytes are significantly greater thanM1 FA of the other

catarrhines (Table 12). Differences observed between P. troglodytes M1 FA and A.

geoffroyi M1 were statistically significant at p= 0.0001 (Table 12).

Prediction 1a.3

1 Because M and M1 CFTs are not available for all primate genera used to test H1a

1 in stage 1, predictions were constructed to address either M or M1 in order to ascertain if

and to what extent growth duration is associated with the expression of first molar FA.

1 By looking at M and M1 separately, a greater understanding of the relationship between

growth duration of the first molar and FA can be achieved. This section addresses results

for predictions associated with M1.

Prediction 1a.3 is supported: M1 FA of Ateles geoffroyi is lower than M1 FA of

both G. gorilla and P. troglodytes (Figure 5). Significant differences were observed in FA

1 estimates of M and M1 between G. gorilla and A. geoffroyi as well as P. troglodytes and

A. geoffroyi (Table 12). The M1 CFT of A. geoffroyi is approximately one year shorter

than either of the great ape M1 CFTs. The finding that A. geoffroyi expresses M1 FA that is lower than both great ape species is consistent with the hypothesis that growth duration is associated with the expression of first molar FA.

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Predictions 1a.4 and 1a.5

This section focuses on FA of mandibular first molars. Of the six primate species

used to test H1a, M1 CFTs are available only for catarrhines.

With the exception of M1 MD, prediction 1a.4 is not supported. FA of P. anubis’

M1 MD falls between M1 FA of H. lar and great ape species, which lends support to

prediction 1a.4. However, in the BL and crown area dimensions P. anubis exhibits M1

FA that is less than that of all the apes. All FA estimates of P. anubis differ significantly from the lesser and greater apes (Table 12).

Macaca mulatta exhibits the lowest M1 FA in all three dimensions, supporting

prediction 1a.5. Among the catarrhines examined in stage 1, M. mulatta has the shortest

CFT (Table 10). The results of this analysis, therefore, lend support to H1a. Because of

the close similarity in CFTs between M. mulatta (M1 CFT = 1year) and H. lar (M1 CFT

= 1.10 years) (Table 10), M1 FA estimates of these species should not differ significantly

from each other. This pattern is not confirmed: M1 FA estimations of M. mulatta and H.

lar are significantly different from each other (Table 12).

Summary of Results for Stage 1

Three of five predictions for H1a were confirmed. Of the two predictions not confirmed, the results for prediction 1a.4 differ depending on which crown dimension is

examined. A progressive increase in FA from monkeys to lesser apes to great apes is

observed in M1 BL dimension and crown area (Figure 6). This progression is in

opposition to prediction 1a.4 in which P. anubis was predicted to exhibit FA of M1

108 between lesser and great apes. Mandibular FA in the MD dimension does not illustrate the same progressive increase from monkeys to lesser apes to great apes (Figure 6).

Rather, M1 FA in the MD dimension follows the pattern predicted for H1a stage 1: FA of

M1 MD for M1 H. lar falls between the Old World monkey species.

Prediction 1a.2 was also not confirmed. Even though this prediction was not supported by the data, the results were consistent across the three crown dimensions for

1 both M and M1: P. troglodytes exhibited the greatest M1 FA estimates. The possible reason(s) for why P. troglodytes exhibited greater FA than G. gorilla despite having a shorter M1 CFT will be discussed below. An important conclusion from testing prediction 1a.2, however, is that both great ape species exhibited greater M1 FA than the other species included in stage 1 (Figure 6).

Discussion

Stage 1

These Results in the Context of Previously Reported First Molar FA

Of the primates used to test H1a, FA of the primate first molar has only been investigated in M. mulatta (Hallgrimsson, 1999). Hallgrimsson (1999) found that rhesus macaques exhibited significantly higher FA of the first molar diameter relative to osteometric measurements. Hallgrimsson (1999) connects the greater first molar FA to

Siegel and colleagues’ (1992) assertion that dental traits tend to be more sensitive to environmental stress in comparison to osteometric traits.

109

Hallgrimsson (1999) also examined sex differences in osteometric FA and

predicted that male and female rhesus macaques should differ in FA because males take

longer to complete growth. The results of Hallgrimsson’s (1999) study, however, did not

indicate FA differences in male and female osteometric traits. He suggests that these

results are due either to the magnitude of FA not being strong enough to be detected in

the macaque sample or because the difference between male and female rhesus macaques

might be offset by other factors not associated with growth (Hallgrimsson, 1999). It is

unclear, however, if first molar FA was included in Hallgrimsson’s (1999) discussion of

sex differences in osteometric FA and the relationship between FA and ontogeny.

Regardless of the lack of a sex difference in osteometric FA, Hallgrimsson (1999) did

find a relationship between osteometic FA and ontogenetic timing. This finding is similar

to a previous study conducted by Hallgrimsson (1995) where evidence for hominoids

exhibiting greater FA in osteometric traits relative to mammals with shorter periods of

growth was reported.

The current study represents the first to compare M1 FA of M. mulatta to other

catarrhines. The results are consistent with the WOV hypothesis: the shorter M1 CFT of

M. mulatta decreases this species’ window of opportunity to experience developmental

perturbations. The determination that growth duration is associated with the opportunity

for M. mulatta to experience perturbations that disrupt development has implications for future asymmetry studies. Fluctuating asymmetry and directional asymmetry have been investigated in the dentition and skeleton of M. mulatta (Falk et al., 1988; Falk et al.,

1990; Hopkins et al., 1992; Hallgrimsson, 1999; Hauser and Akre, 2001; Hallgrimsson et

110 al., 2002). If growth duration influences the expression of FA in the first molar of M. mulatta, it is possible that skeletal growth duration, including bone remodeling, could be associated with the expression of asymmetry in the limb bones of M. mulatta.

Furthermore, additional research on the rest of the dentition is needed to determine if the association between first molar CFT and FA is isolated to the mandibular molars or if the pattern persists in other tooth types.

Developmental Perturbations and Increased Developmental Noise

The WOV hypothesis proposes a window of opportunity during which perturbations can act on the development system resulting in an increase in developmental noise. In an ideal situation, individuals of all species would encounter similar perturbations at the same rate during development. Relative to an individual with a shorter period of growth, a longer period of growth increases an individual’s chances of encountering a greater number of perturbations.

Although three of the five predictions for stage 1 were upheld supporting the hypothesis that a longer period of M1 crown formation provides a greater window of vulnerability (Vrijenhoek, 1985), growth duration does not determine the severity of the developmental perturbations an individual might experience during development.

Furthermore, the WOV hypothesis does not consider whether or not the developmental system was able to buffer developmental perturbations or, if buffering did occur, if the result was effective at preventing developmental noise. For example, the degree to which species can effectively buffer developmental stress may differ due to past developmental

111

insults or a highly stressful environment. Thus, a species with a shorter WOV might

express greater FA relative to a species with a greater WOV as a result of experiencing

severe perturbations and/or buffering ability.

Even though G. gorilla did not exhibit the largest FA estimates, both G. gorilla

and P. troglodytes express greater first molar FA than the other species used to test H1a.

Furthermore, F-tests indicate that FA values of both G. gorilla and P. troglodytes are

1 statistically significant different from FA M and M1 of the NW and OW monkey species

(Table 12). This result is important because both G. gorilla and P. troglodytes take longer than two years to form their M1 crowns whereas the other species used in stage 1 form their M1 crowns in less than 2 years (Table 10). Because only the two great ape species did not follow the pattern predicted by prediction 1a.2, the results of this prediction do

lend limited support to the hypothesis that growth duration is associated with first molar

FA in primates.

Differences in susceptibility to developmental perturbations between specimens

of G. gorilla and P. troglodytes examined here could explain why prediction 1a.2 was not

confirmed. Although it is not possible to determine the precise stressor(s) which

contributed to Pan exhibiting greater M1 FA than Gorilla from the data collected for this

dissertation, it is clear that specimens representing P. troglodytes may have experienced

greater number of developmental perturbations during crown formation of the first molar

(in contradiction to the WOV hypothesis), encountered more severe developmental

perturbations, or had a compromised developmental system that was unable to effectively

buffer developmental perturbations relative to G. gorilla. For instance, an individual

112 whose developmental system is not predisposed to stress is more likely to be able to effectively buffer developmental perturbations and thus exhibit less developmental noise.

G. gorilla is likely encountering developmental perturbations but is able to buffer perturbations because the developmental system is not compromised. The developmental system of P. troglodytes could be compromised, or strained, because of prior insults resulting in a decrease in the effectiveness of the system to buffer perturbations during growth.

A second result from the analysis of P. troglodytes’ first molar FA is the large

1 1 difference between the FA estimates of M and M1. To utilize the M and M1 CFT ranges of P. troglodytes provided by Smith and colleagues (2007), the average was taken

(Tables 7 and 10). The M1 CFT (e.g. 2.217-2.417 years) range of P. troglodytes is shorter than the CFT range for M1 (2.175-2.63 years) by approximately three months (Smith et al., 2007). Averaging each M1 CFT range for P. troglodytes minimized the variation in

1 crown formation. The slightly longer CFT range of M1 may account for why FA of M and M1 are significantly different from each other (Table 13).

G. gorilla M1 vs. P. troglodytes M1 vs.

G. gorilla P. troglodytes G. gorilla M1 P. troglodytes M1 Tooth & F ‐ratio PF‐ratio P Dimension df df Dimension M1 BL 142 71 BL 1.24 0.1006 1.36 0.1014 M1 MD 142 73 M1 Crown 142 71 Area MD 1.29 0.0664 2.86 0.0001

M1 BL 142 67

M1 MD 138 68 Crown M Crown 2.63 0.001 1.72 0.0001 1 103 67 Area Area 1 Table 13. F-tests for M and M1 FA Comparisons 113

Alternatively, M1 of P. troglodytes may be more susceptible to developmental

1 1 perturbations relative to M . FA G. gorilla’s M1 is also greater than M in the MD and

1 1 CA dimensions. An F-test was conducted on M and M1 of P. troglodytes and M and M1

1 of G. gorilla to determine if a significant difference between FA of M and M1 exists.

Results of these F-tests (Table 13) indicate that M1 MD and CA of P. troglodytes exhibit

1 significantly greater FA than M MD and CA. With respect to G.gorilla, M1 CA is

significantly greater than M1 CA (Table 13).

A recent study investigating dental FA in Neanderthals and modern humans also found that the mandibular dentition exhibited greater dental FA relative to the maxillary dentition (Barrett et al., 2012). In particular, Barrett and colleagues (2012) found that M1 of the Inupiat sample (a prehistoric sample from Point Hope Alaska) exhibited greater dental FA relative to the M1.

FA estimates (Table 11) and F-tests presented here (Tables 12 and 13) lend tentative support to the possibility that primate M1 are more susceptible to developmental

perturbations relative to M1. Because the species sample for which data on both M1 and

M1 CFTs is limited to great apes (e.g. Schwartz and Dean, 2011; Smith et al., 2007), it is

not possible to test if the greater M1 FA is a result of a greater WOV or if M1 is more

susceptible to growth disruptions for some other reason. Thus the results presented here

provide preliminary evidence for M1 of both Pan and Gorilla exhibiting greater

susceptibility to developmental perturbations relative to the M1. Reason(s) for this

1 susceptibility remain unknown for the time being. Once M and M1 CFTs are available

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for other primate species, it will be possible to test if the M1 FA pattern observed in great apes continues in other primate species.

Results

Stage 2

Appendix B contains the results for the two-way mixed model ANOVA of M1

and M1 for stage 2 of H1a. Maxillary and mandibular first molar FA estimates for each species are available in Table 14. Table 15 summarizes the results of the F-tests used to determine the significance of differences between FA estimates in the primate species included in stage 2 of Ha1. Figure 7 provides a visual illustration of the results for stage 2 of H1a.

Stage 2, H1a Maxillary Mandibular SpeciesBLMDCABLMDCA Gorilla gorilla 1.07x10‐4 7.36x10‐5 2.59x10‐4 1.59x10‐4 4.21x10‐4 9.50x10‐4 Pan troglodytes 4.26x10‐4 2.77x10‐4 5.78x10‐4 4.68x10‐4 6.50x10‐4 9.94x10‐4 Hylobates lar ‐‐‐6.14x10‐5 9.90x10‐6 6.18x10‐5 Macaca mulatta ‐‐‐1.24x10‐5 4.02x10‐6 1.52x10‐5 Papio anubis ‐‐‐1.76x10‐5 8.56x10‐6 2.55x10‐5 ‐5 ‐5 ‐5 Ateles geoffroyi 2.37x10 2.18x10 4.71x10 ‐‐‐ Table 14. FA Estimates, H1a Stage 2

Prediction, Stage 2 1a.1

Prediction 1a.1 for stage 2 of testing H1a is confirmed. H. lar exhibits M1 FA that is lower than M1 FA of either P. troglodytes or G. gorilla.

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G. gorilla vs. A. G. gorilla vs. P. geoffroyi troglodytes G. P. H. M. P. A. gorilla troglodytes lar mulatta anubis geoffroyi Tooth & Dimension df df df df df df F ‐ratio PF‐ratio P M1 BL 40 40 ‐‐ ‐ 36 4.51 0.0001 3.99 0.0001 M1 MD 42 42 ‐‐ ‐ 35 3.38 0.0002 3.76 0.0001 M1 Area 40 40 ‐‐ ‐ 35 4.70 0.0001 3.22 0.0002

M1 BL 68 67 65 67 64 ‐ 2.94 0.0001

116 M1 MD 67 68 59 55 62 ‐ 1.55 0.0371 M1 Area 67 67 60 59 63 ‐ 1.05 0.4212

Continued Table 15. F-tests Stage 2, H1a Bolded p-values are statistically significant

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Table 15 continued

G. gorilla vs. H. G. gorilla vs. M. G. gorilla vs. P. P. troglodytes vs. P. troglodytes vs. P. troglodytes vs. P. troglodytes vs. lar mulatta anubis A. geoffroyi H. lar M. mulatta P. anubis

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P 17.98 0.0001 12.72 0.0001 15.13 0.0001 2.60 0.0001 12.05 0.0001 9.06 0.0001 7.63 0.0001 37.76 0.0001 26.61 0.0001

117 42.49 0.0001 41.73 0.0001 75.95 0.0001 65.67 0.0001 64.50 0.0001 54.70 0.0001 15.35 0.0001 62.43 0.0001 37.28 0.0001 16.08 0.0001 65.37 0.0001 39.04 0.0001

Continued

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Table 15 continued

H. lar vs. M. H. lar vs. P. M. mulatta vs. P. mulatta anubis anubis

F ‐ratio PF‐ratio PF‐ratio P

4.95 0.0001 3.49 0.0001 1.42 0.0788 118 1.02 0.4691 7.17 0.0001 1.16 0.2885 4.07 0.0001 2.43 0.0002 1.67 0.0242

118

0.00120000

0.00100000

0.00080000 Estimate

0.00060000 119 Asymmetry

0.00040000 Fluctuating

0.00020000

0.00000000 P. troglodytes G. gorilla H. lar M. mulatta P. anubis A. geoffroyi

Species

UM1 BL UM1 MD UM1 CA LM1 BL LM1 MD LM1 CA

Figure 7. Maxillary and Mandibular First Molar FA Estimates, H1a Stage 2 Note: Both maxillary and mandibular FA estimates were only calculated for P. troglodytes and G. gorilla

119

Prediction, Stage 2 1a.2

The result of predication 1a.2 in stage 2 mirror those reported for stage 1. G.

1 gorilla does not exhibit the greatest M or M1 FA estimates. Rather, P. troglodytes has

1 1 the greatest M and M1 FA. Furthermore, M FA and M1 FA of P. troglodytes are

1 significantly greater than M FA and M1 FA of G. gorilla (Table 14). These results do not support prediction 1a.2 of stage 2.

Prediction, Stage 2 1a.3

Prediction 1a.3 is confirmed: Ateles geoffroyi exhibits M1 FA which falls below

that of G. gorilla and P. troglodytes (Table 13). Both great apes exhibit M1 FA that is

significantly different from Ateles’ M1 FA (Table 14).

Predictions, Stage 2 1a.4 and 1a.5

Prediction 1a.4 is not confirmed. Instead of falling between the greater and lesser

apes, as predicted, P. anubis exhibits FA that is less than the M1 FA of all three ape

species (Table 13). Thus, the resulting continuum of M1 FA estimates for these four

catarrhines is P. anubis – H. lar – G. gorilla – and P. troglodytes.

Macaca mulatta exhibits the lowest M1 FA among the five catarrhines species

examined in prediction 1a.5. This result lends supports to an association between growth

duration of the first molar and FA.

M. mulatta and H. lar FA estimates do not differ significantly in all tooth

dimensions. This is an important result because M. mulatta and H. lar exhibit M1 CFTs

120

that are close together (Table 10). However, this result differs from what was found in

stage 1 (Appendix B; Tables 11 and 13), where M1 FA of M. mulatta and H. lar was

found to differ significantly.

Discussion

Stage 2

Results of three tests support the hypothesis that a longer duration of first molar

crown formation is associated with elevated FA. Two predictions of stage 2 testing did

not follow the pattern predicted by using first molar CFTs for developmental timing.

These predictions are the same ones that were not supported in stage 1. A brief discussion

focusing on the similarities and differences between stages 1 and 2 for the two

predictions that were not supported is provided below.

With respect to the great ape species included in H1a, results of stages 1 and 2 are

similar. These results suggest that P. troglodytes either experienced a greater number of

perturbations or severe perturbation(s) relative to G. gorilla.

In both stages 1 and 2, prediction 1a.4 was not supported. In stage 1, M1 MD did

support prediction 1a.4; however, in stage 2 of testing that is not the case. In stage 2, P.

anubis’ M1 MD FA is less than H. lar, G. gorilla, and P. troglodytes. Although there is a difference in the placement of P. anubis among the apes in stages 1 and 2 for M1 MD FA,

F-tests indicate that FA of P. anubis differs significantly from FA of both the lesser and greater apes (Tables 12 and 14). The indication that results of M1 MD FA differ

significantly between P. anubis and the apes in both stages of testing produce conflicting

121 results: M1 MD FA supports prediction 1a.4 in stage 1 while in stage 2 the prediction is not upheld. It is possible that because the P. anubis sample was reduced for stage 2, the individuals who expressed more developmental noise were removed from the sample decreasing the overall M1 MD FA of P. anubis.

Summary

The results of the analysis of the association between FA and growth duration in the first molars of non-human primates can be summarized as follows:

1. Of the 10 predictions across two stages of testing H1a, six predictions were

fully upheld lending support to the hypothesis that a longer duration of growth

provides a greater opportunity to experience developmental perturbations.

2. Four predictions were not confirmed. It is possible that the difference in

growth duration between species might be offset by other factors which either

increases or decreases a species’ sensitivity to developmental perturbations.

3. Of the four predictions not upheld, one was upheld in MD dimension of M1.

1 4. In both stages of testing H1a, greatest M and M1 FA was expressed by P.

troglodytes.

5. Ateles geoffroyi exhibited less M1 FA than the great apes.

6. Macaca mulatta exhibited the lowest M1 FA.

A consistent and unexpected result from testing H1a is FA of P. troglodytes’ first molars. Since the data collected for this study cannot address the precise stressor

122

experienced by P. troglodytes, nor any other species examined in H1a, all explanations

1 provided merely represent possibilities. What can be said with certainty is that M and M1

FA estimates of P. troglodytes do not follow the pattern predicted by H1a. Moreover,

since FA is an indicator of developmental perturbations experienced during development,

P. troglodytes appears to represent a species under great stress because it’s M1 FA far

exceeds that predicted by the WOV hypothesis.

FA estimates between species should be proportional to the difference in the first

molar CFTs. First molar CFTs of P. troglodytes and G. gorilla are different but not by a

substantial amount (Table 10). Despite the fact that prediction 1a.2 was not confirmed,

the difference in FA estimates should be not be significantly different between P.

troglodytes and G. gorilla since their average M1 CFTs are within months of each other

(Schwartz et al., 2006; Smith et al., 2007). This result was not confirmed: M1 FA of P.

troglodytes and G. gorilla differ significantly (Tables 12 and 14).

A limited number of primate species were used to test H1a. Even though six out

of 10 tests were upheld, the results of testing H1a lend tentative support to the WOV

hypothesis. Furthermore, because of the small number of species sampled,

phylogenetically controlled comparisons were not possible when testing H1a. In the

following chapter, a broader assessment will conducted by comparing first molar FA

among species based on life history profiles and age at weaning.

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CHAPTER 6: EXTENDING THE TEST OF THE ASSOCIATION BETWEEN GROWTH DURATION AND DENTAL FLUCTUATING ASYMMETRY

Introduction

The hypothesis that growth duration is associated with variation in first molar

(M1) fluctuating asymmetry (FA) is further tested in this chapter. Primates are considered to have one of the slowest life histories among mammals (Harvey et al., 1987; Charnov and Berrigan, 1993). Once body size is controlled for, primates exhibit long gestations, small litters, large neonate size, long interbirth intervals, slow postnatal growth rates, relatively late ages at maturity, and long life spans (Charnov, 1991; Ulijaszek, 2002;

Kappeler et al., 2003). Primate life histories have been modeled in a continuum of ‘slow’ through ‘fast’ life history paces (Martin and MacLarnon, 1985; Purvis et al., 2003).

Some scholars (Bogin, 1997, 2001; Leigh, 2001; Pereira and Leigh, 2003; Leigh and Blomquist, 2007) argue that the slow-fast continuum does not account for tradeoffs, which are fundamental to life history, in the timing and duration of growth. Modes of ontogeny, or differences in trajectories in different body systems, represent an alternative view to the slow-fast continuum (Pereira and Leigh, 2003; Leigh and Blomquist, 2007).

Leigh and colleagues (Pereira and Leigh, 2003; Leigh and Blomquist, 2007; Blomquist et al., 2009) propose that differences in timing and rate of growth result in a dissociation between different structures during development. The manner in which structures are

124

interrelated during development changes through the developmental period, a concept

called modularity (Leigh and Blomquist, 2007). Blomquist and colleagues (2009) state that “this dissociation of development structures is a core concept for understanding how ontogeny can be modeled into adaptive patterns, and contrast remarkably with traditional

‘fast vs. slow’ models for mammalian life history evolution in which development is entirely absent or is the vacant space between neonatal and adult endpoints.”

Although Leigh and colleagues (Pereira and Leigh, 2003; Leigh and Blomquist,

2007; Blomquist et al., 2009) make an excellent point, it is possible to broadly arrange primates across the order on a slow-fast continuum. Doing so provides a foundation to develop predictions about the association between developmental timing and dental FA in primates.

A specific ontogenetic period – in which first molars crowns form – was used in the previous chapter to test the hypothesis that growth duration is associated with FA.

However, the use of crown formation times (CFTs) in this analysis limited the number of species that could be examined. The relationship between molar CFTs and developmental timing, measured through the pace of primate life histories and age at weaning (Macho,

2001), makes it possible to expand the analysis of FA across primates to more than those species for whom first molar CFT data exist. Thus, in this chapter, I use the pace of primate life histories, as well as weaning age, as proxies for the duration of first molar

CFT.

Using a slow-fast continuum of life histories as a proxy for developmental timing is not as rigorous a test as using first molar CFTs because a particular ‘time’ is not

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known. Among primates, there is a diversity of life history features including differences

in brain size, weaning age, mode of infant care, and diet (Ross, 1998; Ross and

MacLarnon, 1995; Godfrey et al., 2001; Kappeler et al., 2003). In addition to using a

slow-fast continuum of life history schedules, an additional test will be conducted using a critical life history characteristic – age at weaning. Using a single variable as a proxy for a position along the slow-fast continuum is a more straight forward approach to examining if there is an association between growth duration and elevated FA.

Weaning is a process in which complementary foods are gradually introduced while the dependence on breast milk is reduced over time (Humphrey, 2008). Across primates, the pattern and timing of dental development are closely associated with life history attributes (Smith, 1989, 1992; Smith et al., 1994; Macho, 2001; Dean, 2006).

Smith (1989) showed that the timing of emergence of first permanent molar was highly and isometrically correlated with weaning age. Additionally, Macho (2001) found that weaning age also scaled isometrically with molar CFTs of anthropoid primates and that average molar CFT were significantly correlated with several life history traits especially age at weaning. Age at weaning is therefore a life history variable that can effectively

serve as a proxy for first molar crown formation times.

This chapter applies both a continuum of life history paces within the primate

order as well as a specific ontogenetic event to test if developmental timing is associated

with first molar FA estimates. Moreover, comparing M1 FA estimates among a greater

sample of primate species, is important because it will provide a broader, though

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tentative, picture of whether or not an association between developmental timing and M1

FA exists.

Hypothesis 1b (H1b) states that species with prolonged life history schedules will

exhibit greater FA than species with short life history schedules. By applying a slow-fast continuum, a broad life history framework is used as the theoretical foundation to develop predictions of variation in first molar FA among thirteen primate species. The first set of comparisons for testing H1b will be conducted on the basis of a slow-fast continuum.

Predictions of Hypothesis 1b

First Set of Comparisons

Table 16 lists the 13 primate species used to test H1b in the first set of

comparisons. Data on life history schedules were available for other primate species (e.g.

Pongo pygmaeus); however, sample sizes of these primate species fall below the minimum requirement of N=30. Relative to Hypothesis 1a (see Chapter 5), the sampling

of species for testing H1b has expanded to include species of Cebidae and Colobus as well as additional species of Cercopithecidae and Hylobatidae.

H1b will first be tested using a set of comparisons constructed from the slow-fast

continuum of primate life histories. Three predictions used in the first set of comparisons of H1b are:

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1. Prediction 1b.1: Great apes, because of their prolonged LH schedules, will exhibit

statistically significantly greater M1 FA relative to both catarrhine and

platyrrhines species.

2. Prediction 1b.2: The fast-growing folivorous Colobus guereza will express M1

FA that is significantly less than M1 FA of the other Old World monkeys.

3. Prediction 1b.3: Hylobates species will exhibit M1 FA estimates that fall within

the M1 FA range of Old World monkeys, not great apes.

Sample Sizes 1 Species M M1 Gorilla gorilla 39 31 Pan troglodyes 39 31 Hylobates lar 39 31 Hylobates hoolock 39 31 Colobus guereza 39 31 Cerceopithecus mitis 39 31 Lophocebus albigena 39 31 Macaca mulatta 39 31 Macaca nemestrina 39 31 Papio anubis 39 31 Ateles geoffroyi 39 31 Cebus albifrons 39 31 Cebus apella 39 31 Table 16. Sample Sizes of Primate Species Used to Test H1b

Across primate species, great apes have the slowest life history schedules (e.g.

Harvey and Clutton-Brock, 1985; Ross and Jones, 1999; Kelley, 2004; Kappeler et al.,

2003; Dean, 2006). Thus, G. gorilla and P. troglodytes are hypothesized to exhibit greater M1 FA than the other primate 11 species examined here. With respect to

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prediction 1b.2 of H1b, folivores have been shown to have accelerated dental development (on an absolute scale) relative to like-sized fruitvores (e.g. Godfrey et al.,

2001). Therefore, the folivorous C. guereza is hypothesized to exhibit less M1 FA than the other Old World monkeys who are not primarily categorized as folivores. Only catarrhine species (N=10) were used to examine prediction 1b.3. For all predictions, FA

1 estimates of maxillary (M ) and mandibular (M1) molar crown area (CA) were used as

the basis for comparisons between primates.

Sample sizes of species are equivalent for testing H1b. To achieve equivalency, sample sizes of some primate species were reduced to match the lowest sample size for

each first molar. For the maxillary first molar, Macaca nemestrina exhibited the smallest

sample size (N=39). Lophocebus albigena had the lowest mandibular first molar sample

size (N=31). Using individual (IND) specimen numbers, all maxillary first molar sample

sizes were reduced to 39 specimens per species by performing the RANDBETWEEN

function in Microsoft ® Excel. The same procedure was used to reduce the mandibular

first molar sample sizes to 31 specimens per species. The 31 specimens for the

mandibular first molar analysis were randomly selected from the 39 specimens used to

1 1 calculate FA crown area for M . This was done to ensure that M and M1 CA estimates were calculated for the same specimens for each species. Because the sample sizes are

1 1 not equivalent for M and M1, a species’ M sample size has eight additional specimens.

Following the guidelines of Palmer and Strobeck (1986, 2003), data for each species were evaluated for the presence of outliers using scatter plots. The scatter plot of

L. albigena (M1 BL) was identified as having three outliers. Review of the data showed

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that these outliers were in fact data entry errors. The errors were corrected by using the

original data sheets to replacing the incorrect dental dimensions with the correct ones.

Second Set of Comparisons

Weaning ages of 12 of the 13 species included in this chapter will serve as the basis for the second set of comparisons for testing H1b. Table 17 reports the weaning

ages and the references from which they were taken for 12 primate species (Harvey and

Clutton-Brock, 1985; Godfrey et al., 2001).

To test if a relationship between M1 FA and weaning age exists, linear

1 regressions for both M and M1 were conducted. A species’ M1 FA represents the

dependent variable while weaning age was the independent variable. Eleven primate

species were used in the second linear regression analysis. In testing hypothesis 1a, P.

troglodytes was found to express first molar FA that far exceeded the expected

asymmetry predicted by its first molar CFTs. A second linear regression analysis was

performed to investigate if a difference in adjusted R2 if found when P. troglodytes is removed. The following prediction was used to test H1b in this second set of

comparisons:

Prediction 1b.4: The variation observed in primate first molar FA is expected to

be strongly related to age at weaning.

Because first molar FA estimates are considerably smaller than weaning ages, first molar FA estimates were multiplied by 10,000 prior to conducting the linear regression analyses.

130

Age at Weaning Species Reference (yrs) L. albigena 0.58 Harvey and Clutton‐Brock, 1985 C. albifrons 0.75 Godfrey et al., 2001 M. macaca 0.88 Godfrey et al., 2001 M. nemestrina 1.00 Godfrey et al., 2001 C. guereza 1.08 Godfrey et al., 2001 C. apella 1.14 Godfrey et al., 2001 H. lar 1.50 Godfrey et al., 2001 P. anubis 1.60 Godfrey et al., 2001 H. hoolock 1.92 Harvey and Clutton‐Brock, 1985 A. geoffroyi 2.25 Godfrey et al., 2001 G. gorilla 3.50 Godfrey et al., 2001 P. troglodytes 5.00 Godfrey et al., 2001 Table 17. Weaning Age of Primate Species Used to Test H1b

Results

1 The two-way mixed model ANOVA tables of M and M1 CA for each species can

1 be found in Appendix C. Each species’ M and M1 CA FA estimates are provided in

Table 18. Table 19 summarizes the results of all F-tests performed. First molar FA results

1 are displayed in Figures 8 (M ) and 10 (M1). For these figures, species are listed from high to low FA estimates. Graphs of the linear regression line are displayed as Figures 9

(M1) and 11 (M1). Finally, the ANOVA tables of the linear regressions are located in

Table 20.

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1 Species M CA M1 CA Gorilla gorilla 2.32x10‐4 1.45x10‐4 Pan troglodyes 7.46x10‐4 1.68x10‐3 Hylobates lar 4.52x10‐5 1.80x10‐5 ‐6 Hylobates hoolock 7.22x10 8.69x10‐6 ‐6 Colobus guereza 6.12x10 5.96x10‐6 ‐5 Cerceopithecus mitis 3.86x10 4.35x10‐5 ‐5 Lophocebus albigena 1.79x10 1.25x10‐5 ‐5 Macaca mulatta 2.73x10 1.12x10‐5 ‐6 Macaca nemestrina 6.73x10 1.16x10‐5 ‐6 Papio anubis 5.70x10 1.16x10‐5 ‐5 Ateles geoffroyi 3.64x10 1.23x10‐4 ‐6 Cebus albifrons 7.90x10 1.39x10‐5 ‐5 ‐5 Cebus apella 2.46x10 1.75x10 Table 18. FA Estimates of Maxillary and Mandibular First Molar Crown Area

Maxillary First Molars

Prediction 1b.1 is confirmed (Tables 18 and 19; Figure 8): Gorilla gorilla and

Pan troglodytes exhibit M1 CA FA estimates that are statistically greater than both OW

and NW monkeys. These results were expected because great apes are known to have

prolonged LH schedules relative to both Old World and New World monkeys (e.g.

Harvey and Clutton-Brock, 1985; Watts, 1990; Kelley, 1997; Kelley and Smith, 2003) as well as have a shared relationship that is separate from of OW and NW monkeys. Even though apes and OW monkeys are classified as catarrhines primates, the great apes are further distinguished within the Hominidae clade. The results of prediction 1b.1 support an association between developmental timing and M1 FA.

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G. P. H. H. C. C. L. M. M. P. A. C. C. gorilla troglodytes lar hoolock guereza mitis albigena mulatta nemestrina anubis geoffroyi albifrons apella Tooth & df df df df df df df df df df df df df Dimension 1 CA 38 38 35 28 27 34 31 33 28 31 33 14 29 M M1 CA 30 30 25 22 17 27 21 25 25 26 28 24 19

133 G. gorilla vs. P. G. gorilla vs. H. G. gorilla vs. H. G. gorilla vs. C. G. gorilla vs. C. G. gorilla vs. L. G. gorilla vs. M. G. gorilla vs. M. troglodytes lar hoolock guereza mitis albigena mulatta nemestrina

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

3.22 0.0002 5.13 0.0001 32.14 0.0001 37.92 0.0001 6.02 0.0001 12.77 0.0001 8.51 0.0001 34.48 0.0001 11.57 0.0001 8.08 0.0001 16.74 0.0001 24.40 0.0001 3.35 0.0011 11.66 0.0001 12.94 0.0001 9.03 0.0001

Continued Table 19. Maxillary and Mandibular F-tests

133

Table 19 Continued

G. gorilla vs. P. G. gorilla vs. A. G. gorilla vs. C. G. gorilla vs. C. P.troglodytes vs. H. P.troglodytes vs. H. P.troglodytes vs. C. anubis geoffroyi albifrons apella lar hoolock guereza

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

40.17 0.0001 6.37 0.0001 29.38 0.0001 9.45 0.0001 16.51 0.0001 103.38 0.0001 121.96 0.0001 15.71 0.0001 1.13 0.3739 10.43 0.0001 8.29 0.0001 93.56 0.0001 193.68 0.0001 282.40 0.0001

134

P.troglodytes vs. C. P.troglodytes vs. L. P.troglodytes vs. M. P.troglodytes vs. M. P.troglodytes vs. P. P.troglodytes vs. A. mitis albigena mulatta nemestrina anubis geoffroyi

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

10.35 0.0001 41.06 0.0001 27.37 0.0001 110.91 0.0001 130.09 0.0001 20.49 0.0001 38.74 0.0001 134.97 0.0001 149.74 0.0001 104.46 0.0001 181.76 0.0001 14.92 0.0001

Continued

134

Table 19 Continued

P.troglodytes vs. C. P.troglodytes vs. H. lar vs. H. H. lar vs. C. H. lar vs. C. H. lar vs. L. H. lar vs. M. H. lar vs. M. albifrons C. apella hoolock guereza mitis albigena mulatta nemestrina

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

94.48 0.0001 30.38 0.0001 6.26 0.0001 7.39 0.0001 1.17 0.3243 2.49 0.0058 1.66 0.0733 6.72 0.0001 120.59 0.0001 96.12 0.0001 2.07 0.0455 3.02 0.0108 2.42 0.0147 1.44 0.1997 1.60 0.1234 1.55 0.1400

135

H. lar vs. P. H. lar vs. A. H. lar vs. C. H. lar vs. C. H. hoolock vs. C. H. hoolock vs. H. hoolock vs. L. H. hoolock vs. anubis geoffroyi albifrons apella guereza C. mitis albigena M. mulatta

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

7.93 0.0001 1.24 0.2684 5.72 0.0006 1.84 0.048 1.18 0.3346 5.34 0.0001 2.52 0.0078 3.78 0.0002 1.94 0.0497 7.13 0.0001 1.29 0.2678 1.03 0.481 1.46 0.2149 5.00 0.0001 1.39 0.2245 1.29 0.2749

Continued

135

Table 19 Continued

H. hoolock vs. M. H. hoolock vs. H. hoolock vs. H. hoolock vs. H. hoolock vs. C. guereza vs. C. C. guereza vs. L. C. guereza vs. nemestrina P. anubis A. geoffroyi C. albifrons C. apella mitis albigena M. mulatta

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

1.07 0.4296 1.27 0.258 5.05 0.0001 1.09 0.4065 3.4 0.0009 6.3 0.0001 2.97 0.0026 4.46 0.0001 1.34 0.2457 1.07 0.440 14.76 0.0001 1.6 0.1359 2.01 0.0644 7.29 0.0001 2.09 0.0637 1.89 0.0888

136

C. guereza vs. C. guereza vs. P. C. guereza vs. C. guereza vs. C. C. guereza vs. C. C. mitis vs. L. C. mitis vs. M. C. mitis vs. M. M. nemestrina anubis A. geoffroyi albifrons apella albigena mulatta nemestrina

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

1.10 0.4032 1.03 0.4652 5.95 0.0001 1.29 0.2756 4.01 0.0003 2.12 0.0187 1.41 0.1631 5.73 0.0001 1.95 0.0788 1.55 0.1755 21.52 0.0001 2.34 0.0376 2.94 0.0149 3.48 0.0024 3.87 0.0005 3.74 0.0007

Continued

136

Table 19 Continued

C. mitis vs. P. C. mitis vs. A. C. mitis vs. C. C. mitis vs. C. L. albigena vs. L. albigena vs. L. albigena vs. L. albigena vs. anubis geoffroyi albifrons apella M. mulatta M. nemestrina P. anubis A. geoffroyi

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

6.77 0.0001 1.05 0.445 4.88 0.0013 1.57 0.1094 1.50 0.1298 2.7 0.0048 3.19 0.0009 2.00 0.0277 4.69 0.0001 2.95 0.0031 3.12 0.0031 2.48 0.0221 1.11 0.3978 1.07 0.4316 1.35 0.2318 10.29 0.0001

137

L. albigena vs. L. albigena vs. M. mulatta vs. M. mulatta vs. M. mulatta vs. M. mulatta vs. M. mulatta vs. M. nemestrina C. albifrons C. apella M. nemestrina P. anubis A. geoffroyi C. albifrons C. apella vs. P. anubis

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

2.3 0.0502 1.35 0.2065 4.05 0.0002 4.78 0.0001 1.34 0.2025 3.45 0.0083 1.11 0.3900 1.18 0.3257 1.12 0.3992 1.37 0.2413 1.03 0.4708 1.21 0.316 11.41 0.0001 1.24 0.2982 1.58 0.1408 1.25 0.2877

Continued

137

Table 19 Continued

M. nemestrina M. nemestrina M. nemestrina P. anubis vs. A. P. anubis vs. vs. A. geoffroyi vs. C. albifrons vs. C. apella geoffroyi C. albifrons

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

5.41 0.0001 1.17 0.3484 3.65 0.0005 6.39 0.0001 1.39 0.216 11.05 0.0001 1.20 0.3266 1.51 0.1656 13.05 0.0001 1.51 0.153

138

P. anubis vs. C. A. geoffroyi vs. A. geoffroyi vs. C. albifrons vs. apella C. albifrons C. apella C. apella

F ‐ratio PF‐ratio PF‐ratio PF‐ratio P

4.31 0.0001 4.61 0.0019 1.40 0.1804 3.11 0.0143 1.89 0.0656 9.02 0.0001 7.33 0.0001 1.26 0.2930

138

FA estimates illustrate that C. guereza expresses significantly lower M1 FA from

M. mulatta, L. albigena, and C. mitis (Table 19; Figures 8). These results support

prediction 1b.2. However, prediction 1b.2 cannot be fully confirmed because C. guereza

does not exhibit significantly lower M1 FA relative to all OW monkeys. Even though M1

FA of C. guereza is not statistically different from M. nemestrina (Table 19), C. guereza does express less M1 FA relative to M. nemestrina (Appendix C; Table 18; Figure 8).

Although not statistically significant, this result is in the predicted direction.

An unexpected result of testing prediction 1b.2 is that P. anubis expresses slightly

lower M1 FA than C. guereza. The difference in FA estimates between C. guereza and P.

anubis is not significantly different (Tables 18 and 19).

Maxillary FA estimates of H. lar and H. hoolock are closer to M1 FA of the OW

monkeys than to the great apes (Table 18). Both Hylobates species differ significantly

from the great apes (Table 19). Furthermore, H. lar and H. hoolock exhibit M1 FA estimates that differ significantly from each other. H. lar and H.hoolock also express M1

FA that differs significantly from some of the OW monkey species included in this study

(Table 19). Whether or not Hylobates differed significantly from the OW monkeys was

not a condition of prediction 1b.3. What is of interest is if Hylobates’ M1 FA fell within

the range of M1 FA expressed by the OW monkey species rather than the great apes.

Therefore, because M1 FA of H. lar and H.hoolock differ significantly from the great apes (Table 19) and their FA estimates (Table 18) fall among M1 FA of OW monkeys,

prediction 1b.3 is confirmed.

139

The relationship of variables – M1 FA and age at weaning – is statistically

significant (adjusted R2 = 80.89%; p-value =0.0001) (Table 20 and Figure 10). This

means that 80.89% of the observed variation in M1 FA for these 12 primate species can

be explained by weaning age variation.

The second linear regression performed did not include P. troglodytes in the

analysis. The relationship between variables – M1 FA and age at weaning – is significant

even with P. troglodytes removed (adjusted R2 = 66.58%; p-value =0.0024).

Mandibular First Molars

G. gorilla and P. troglodytes exhibit statistically significantly greater M1 FA

estimates than the other catarrhines (N=8) (Table 19). Moreover, M1 FA estimate of P.

troglodytes is significantly greater than the M1 FA estimates of the platyrrhine species

(N=3) (Table 19). With respect to M1 FA of G. gorilla and the three platyrrhine species,

M1 FA estimates of G. gorilla and A. geoffroyi do not exhibit a significant difference

(Table 19); however, their M1 FA estimates are in the expected direction predicted by

H1b. Mandibular first molar FA of G. gorilla is significantly greater than M1 FA of C. apella and C. albifrons (Appendix C; Table 18). Therefore, prediction 1b.1 for M1 is

confirmed in all but one comparison: G.gorilla and A. geoffroyi.

FA of C. guereza is in the direction predicted by H1b: M1 FA is lower relative to

the other OW monkeys (Appendix C; Table 18). However, C. guereza’s M1 FA is only

statistically lower than M1 FA of C. mitis (Table 20). The p-value results (Table 19)

suggest that M1 FA between C. guereza and L. albigena, M. mulatta, and M. nemestrina

140

141

Figure 8. Maxillary First Molar Crown Area FA Results

141

fa 8 Pan

3 142 Gor

1 Hyl Ate LopA MaM CAp CAl MaNCol Pap HylH 0

012345

Figure 9. Regression Graph for Maxillary Molars fa = fluctuating asymmetry; wa = weaning age Ate= A. geoffroyi; CAl = C. albifrons; CAp= C. apella; Col = C. guereza; Gor = G. gorilla; Hyl=Hylobates; HylH= H. hoolock; LopA= L. albigena; MaM= M. mulatta; MaN= M. nemestrina; Pan = P. troglodytes; Pap = P. anubis

142

Maxillary First Molar Source DF SS MS F P Regression 1 41.1215 41.1215 43.34 0.0001 Residual Error 9 8.53906 0.94878 Total 10 49.66056 Adjusted R‐Sq 0.8089

Mandibular First Molar Source DF SS MS F P Regression 1 3.4359 3.43594 49.61 0.0001 Residual Error 9 0.62331 0.06926 Total 10 4.05925 Adjusted R‐Sq 0.8294

Table 20: ANOVA Tables for Linear Regression Analysis (N=12)

are close to being statistically significant. Only between C. guereza and P. anubis is a strong statistically significant difference in M1 not found (Table 19).

Both Hylobates species exhibit M1 FA estimates that fall among M1 FA of OW

monkeys and are statistically lower than M1 FA of great apes (Appendix C; Tables 18

and 19; Figure 9). H. lar differs significantly from P. anubis, C. mitis, and C. guereza

(Table 19). Additionally, M1 FA estimates of H. hoolock and C. mitis are statistically

different with H. hoolock expressing lower M1 FA (Table 19). Finally, M1 FA estimates

of H. lar and H. hoolock differ significantly from each other (Table 19). As mentioned

above in the M1 results section, prediction 1b.3 focuses on whether or not Hylobates

expresses FA that is similar to OW monkeys rather than the great apes. Even though M1

FA of Hylobates differs significantly from M1 FA of some OW monkeys, the FA

143

estimates of Hylobates do fall within the range of OW monkeys and not great apes.

Therefore, prediction 1b.3 is confirmed for the mandibular first molar.

2 The regression of M1 FA and weaning age is significant (adjusted R ) = 82.94%;

p-value =0.0001) (Table 20; Figure 11). In the regression in which P. troglodytes was

removed, the relationship between of M1 FA and weaning age is also significant (adjusted

2 R = 77.84%; p-value =0.0004). The results of both the linear regressions of M1 FA and

weaning age support prediction 1b.4.

Discussion

The hypothesis that species with prolonged LH schedules would exhibit greater

FA relative to those species with shorter LH schedules is supported in all but one test.

Even though prediction 1b.2 is not fully confirmed because C. guereza’s M1 FA is not

statistically lower than M1 FA estimates of all OW monkeys, there are comparisons that do lend support to prediction 1b.2 suggesting that an association between developmental time and M1 FA is tentatively present (Appendix C; Tables 18 and 19).

The results of testing prediction 1b.4 with twelve species indicate that

1 approximately 80% of the variation in both M and M1 FA is explained by variation in

weaning age. The removal of P. troglodytes from the analysis decreases the adjusted R2;

however, the results are still statistically significant, lending considerable support to an

association between developmental period and FA of the primate first molar.

144

0.00180000

0.00160000

0.00140000

0.00120000

0.00100000 Asymmetry

145 0.00080000 Fluctuating

0.00060000

0.00040000

0.00020000

0.00000000

Species

Figure 10: Mandibular First Molar Crown Area FA Results

145

fa Pan 1.7

1.6

1.5 Gor

1.4 Ate 1.3

1.2

1.1

1.0

0.9

0.8

146 0.7

0.6

0.5

0.4

0.3 CAp HylL 0.2 CAl LopA MaMMaN Pap HylH 0.1 Col

0.0

012345

Figure 11: Regression Graph for Mandibular First Molar fa = fluctuating asymmetry; wa = weaning age Ate= A. geoffroyi; CAl = C. albifrons; CAp= C. apella; Col = C. guereza; Gor = G. gorilla; Hyl=Hylobates; HylH= H. hoolock; LopA= L. albigena; MaM= M. mulatta; MaN= M. nemestrina; Pan = P. troglodytes; Pap = P. anubis

146

Great Apes: Life in the Slow Lane

Relative to other primate species, great apes have the slowest life history

schedules (e.g. Harvey and Clutton-Brock, 1985; Ross and Jones, 1999; Kelley, 2004;

Kappeler et al., 2003; Dean, 2006). Therefore, it is expected that P. troglodytes and G.

1 gorilla would exhibit greater M and M1 crown area FA relative to OW monkeys and

NW monkeys. The results from testing prediction 1b.1 of H1b support the hypothesis that extended LH schedules provide a greater window of vulnerability (WOV) (Vrijenhoek,

1985) during which to accumulate developmental perturbations relative to species with shorten LH schedules. As noted above, this result is expected considering the fact that apes have slow LH for body mass while OW monkeys have fast LH for body mass

(Harvey and Clutton-Brock, 1985; Watts, 1990; Kelley, 1997).

Of all the primates used to test H1b, P. troglodytes exhibits the longest LH

schedule as well as the latest weaning age (Table 17). Accordingly, P. troglodytes expresses the greatest first molar FA. Even though this result was expected, the resulting

1 M and M1 FA estimates are much higher than expected under the WOV hypothesis

(Appendix C; Table 19). Within the great apes, G. gorilla expresses significantly lower

first molar FA than P. troglodytes (Table 19). Furthermore, the differences between FA

estimates of P. troglodytes and the monkeys are not proportional to their life history

differences. Thus, P. troglodytes expresses first molar FA that is significantly greater

than what is expected from where their absolute LH schedule or age at weaning relative

to the other primates examined here.

147

It is possible that individuals of P. troglodytes experienced perturbations at an exceptionally high frequency, or severe perturbations, resulting in the destabilization of the developmental system. The dental metric data collected for this dissertation does not permit an assessment of what type of stress or intensity of perturbation (e.g. low vs. high intensity) any of these primate species experienced over the course of developmental

time.

Recent research on H. lar has demonstrated that this ape exhibits a ‘slow’ LH

schedule, which is a trait that commonly unites great apes (Reichard and Barelli, 2008;

Reichard et al., 2012). In particular, Reichard and colleagues (Reichard and Barelli, 2008;

Reichard et al., 2012) point out that H. lar has social flexibility that is similar to what has

been observed in great apes, such as P. troglodytes. Kelley and Smith (2003) also

demonstrate that for age at first breeding in relation to body mass, Hylobates falls above the primate regression line among the other apes while OW monkey are located below the line. Even though H. lar might exhibit commonalties with the slowed life histories of great apes, their overall LH schedule is not as ‘slowed’ or ‘prolonged’ as that of great apes. For example, their weaning age is more similar to the large bodied OW monkeys than the great apes (e.g. Godfrey et al., 2001). Therefore, H. lar as well as other

Hylobatidae species used to test H1b were predicted to exhibit M1 FA that was more similar to OW monkeys than to great apes. The results support prediction 1b.3: both

Hylobates exhibits M1 FA estimates that are more similar to OW monkeys than the great

apes.

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Folivorous and Frugivorous: Old World Monkeys

Across anthropoids, folivores generally exhibit an accelerated dental development

schedule relative to comparably sized frugivores (e.g. Jason and van Schaik, 1993;

Godfrey et al., 2001; Godfrey et al., 2003). Among the OW monkeys examined in H1b, the eastern black and white colobus monkey (Colobus guereza) is primarily classified as folivorous. Colobus species were traditionally thought of as obligate leaf-eaters.

However, over the last few decades research has shown that Colobus species exploit many foods in addition to leaves especially seeds (e.g. Mckey, 1978; Kirkpatrick, 1998;

Fashing et al., 2007). Leaves, however, are still noted to be a substantial part of diets for

several Colobus species (Fashing, 2006; Kirkpatrick, 2006).

With respect to C. guereza, research illustrates that at certain locations this species has a flexible diet that does not follow the traditional view of colobines being obligate folivores (e.g. Kirkpatrick, 1998; Fashing, 2001). At some locations, C. guereza is reported as being highly folivorous (e.g. Champman et al., 2004; Harris, 2005). At other sites, field studies report that the diet of C. guereza is a combination of leaves, fruit, and seeds (Fashing 2001; Poulsen et al., 2002; Fashing et al., 2007).

C. guereza’s M1 FA is significantly different from three OW monkey species

(Table 19). For M1, FA of C. guereza differs significantly from C. mitis and M. mulatta

while C. guereza’s M1 differs significantly from C. mitis. The C. guereza sample consists of individuals from various locations including locations where C. guereza’s diet has been documented as including fruit and seeds. The resulting M1 FA reported could be closer than expected to some OW monkey species (e.g. M. nemestrina and L. albigena),

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and not significantly different, because the sample of C. guereza has both folivorous and foli-frugivorous individuals. Despite the lack of statistical significance between M1 FA of

C. guereza and some OW monkeys, the finding that C. guereza exhibits lower M1 FA than the other OW monkeys is in the expected direction predicted by the WOV hypothesis.

Linear Enamel Hypoplasia, Fluctuating Asymmetry, and the WOV Hypothesis

The prevalence of LEH within the primate order follows the general pattern of prosimians exhibiting a low prevalence of LEH (Guatelli-Steinberg, 1998; Newell, 1998) while a progressive increase of LEH prevalence from monkeys to gibbons to great apes is commonly observed (Skinner and Guatelli-Steinberg, 1997; Guatelli-Steinberg, 1998;

Guatelli-Steinberg, 2000; Guatelli-Steinberg and Skinner, 2000). From the results of these studies, a great ape – monkey dichotomy has been identified. Some authors suggest that differences in developmental timing might be contributing to the great ape – monkey dichotomy of LEH prevalence (e.g. Skinner et al., 1995; Guatelli-Steinberg and Skinner,

2000). In particular, Guatelli-Steinberg (2001) proposes the question “Do taxonomic differences in the prevalence of these defects reflect real differences in stress experience or are they simply consequences of taxonomic differences in enamel development and morphology?” (p. 146). She has since gone on to explore LEH prevalence and developmental timing in primate species (e.g. Hannibal and Guatelli-Steinberg, 2005;

Guatelli-Steinberg et al., 2012).

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As discussed in Chapter 5, whether or not a relationship between greater LEH

prevalence and elevated FA exists has been investigated in a few studies (Hoover et al.,

2005; Martin et al., 2011). Because both FA and LEH are considered indicators of

physiological stress, it has been proposed that individuals with a high prevalence of LEH

should also express elevated FA relative to individuals who exhibit a low prevalence of

LEH (e.g. Hoover et al., 2005; Martin et al., 2011). It is not possible to determine if a

relationship between LEH and FA are present in this study because LEH was not

recorded for specimens. However, a comparison between the pattern of LEH prevalence observed in previous studies (e.g. Vitzthum and Wikander, 1988; Guatelli-Steinberg and

Lukacs, 1998; Hannibal and Guatelli-Steinberg, 2005; Newell et al., 2006; Guatelli-

Steinberg et al., 2012) to the pattern of first molar FA estimates found in this study is feasible.

First molar FA estimates of the primate species examined in this study generally follow the great ape-monkey dichotomy proposed for LEH defects in non-human primates. FA estimates progressively increase from monkeys to great apes (Figures 8 and

9). The primary difference between the FA estimates and LEH defect prevalence is that

FA estimates of gibbons are not between monkeys and great apes but rather fall among the FA estimates of both NW and OW monkeys (Figures 8 and 9). To fully understand if

FA and LEH follow the same taxonomic patterns commonly observed in LEH prevalence additional comparisons within and between families and/or subfamilies of primates are necessary. Whether or not dental FA parallels the pattern observed in LEH prevalence will be discussed in the final chapter.

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Conclusions

The results from testing H1b support the hypothesis that prolonged LH schedules

provide an opportunity to accumulate perturbations over the course of development. Of

the predictions tested Prediction 1b.2 was not confirmed because C. guereza did not

exhibit statistically significant lower M1 FA from all OW monkeys (Appendix C; Table

18). Using LH schedule as a proxy for developmental time allowed for a greater number

of species to be included in the analysis and increased the reliability of the observed first molar FA variation found across these primate species.

The linear regression of first molar FA and weaning age is significant. These results suggest that the variation observed in first molar FA is strongly related to a

primate’s age at weaning. Because age at weaning served as single variable along the

slow-fast continuum of primate LH schedules, the results of the linear regression also

suggest a significant relationship between first molar FA and developmental timing.

Because the overall pace of LH was used to test H1b, the results reported here

provide a less restrictive picture of the association between developmental time and M1

FA among primate species relative to the results when using M1 CFTs as the growth

variable. Until M1 CFTs and weaning ages are established for a greater selection of

primate species comparisons between specific species are limited. Once a greater

knowledge of these variables is gained, comparisons between genera as well as within

strepsirrhine and haplorrhine clades can be performed. Nevertheless, the variation

observed in M1 FA across 13 primate species, including platyrrhines and catarrhines

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species, serves as an initial starting point upon which to interpret an association between elevated FA and developmental timing.

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CHAPTER 7: CANINE FLUCTUATING ASYMMETRY: A COMPARISON BETWEEN MALES AND FEMALES

Introduction

The opportunity for sexually selected structures to experience developmental

perturbations may be influenced by ‘developmental destabilization’ brought about by

sexual selection. Evidence from some fluctuating asymmetry (FA) studies lends support

to the hypothesis that sexually selected structures are more prone to experience

developmental perturbations relative to non-sexually selected structures (Moller, 1990;

Watson and Thornhill, 1994). The primate canine has been given as one example of a

sexually selected trait that is particularly prone to elevated FA (Manning and

Chamberlain 1993). FA in the primate canine, however, might also be influenced by

differences in canine crown formation times (CFTs) between the sexes resulting in

different ‘windows of vulnerability’ (WOV) (Vrijenhoek, 1985) for males and females of

a species. Recent research on adult canine sexual dimorphism in primate species demonstrates that canine dimorphism is achieved through prolonged periods of canine growth in males relative to females (Schwartz et al., 1999, 2001; Schwartz and Dean,

2001; Guatelli-Steinberg et al. 2009). A prolonged period of canine growth may create a

WOV providing males of sexually dimorphic species a longer period of time to experience and accumulate developmental perturbations relative to females of a species.

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Primate canine FA should therefore be greater in males as compared to females of

sexually dimorphic species not only because sexually selected characters are more prone

to perturbations during development but also because males growth their canines for a

longer duration of time than females. For monomorphic species, males and females have

similar durations of canine growth (Guatelli-Steinberg et al., 2009). As such, male and

female canines of monomorphic species have similar WOVs through which to experience

developmental perturbations resulting in similar canine FA estimates. Comparing canine

FA estimates of males and females of a species will shed light on whether or not canine

FA expression is different in monomorphic primate species relative to sexually dimorphic

primate species.

This chapter re-tests the finding of Manning and Chamberlain (1993) that FA in

male canines exceeded FA in female canines. It is necessary to re-test this result because

statistical analyses of FA have advanced since the early 1990s, during which the Manning

and Chamberlain (1993) study was conducted. The use of two-way mixed ANOVA

model to calculate FA is now standard practice in FA studies (e.g. Palmer 1994; Palmer

and Strobeck, 2003). The current study employed rigorous methodology recommended

for calculating canine FA and F-tests (e.g. Palmer 1994; Palmer and Strobeck, 2003; see

Chapter 4). Furthermore, this present study minimized the effects of use-related wear on

the estimation of FA. Manning and Chamberlain (1993) based their calculations of canine

FA on the dimension of canine height, a tooth dimension greatly influenced by use-

related wear. By using bucco-lingual (BL) and mesio-distal (MD) canine dimensions the

resulting FA represents an accurate assessment of dental asymmetry because these

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dimensions are not as influenced by use-related wear and worn teeth were excluded from

the study sample.

An additional component to this study that was not present in Manning and

Chamberlain’s (1993) study is the inclusion of platyrrhine species It is useful to include

platyrrhines species to determine if the same association between FA and canine sexual

dimorphism holds in an independent radiation of primates. However, because platyrrhine

species have not been addressed as frequently in ontogenetic studies (e.g. Guatelli-

Steinberg et al., 2009; Hogg, 2007, 2008; Hogg and Walker, 2011), the number of platyrrhine species included in this study is limited.

Objectives and Hypotheses

Though comparing male and female canine FA from monomorphic and dimorphic primate species, this chapter examines the relationship between sexual selection and FA continues to build on our understanding of factors that affect dental FA expression including the possible influence of ‘developmental destabilization’ and WOV. Canine size dimorphism in primates is a very common occurrence, with males generally exhibiting larger canines than females (Plavcan, 2004; Leigh, 2008).

Hypothesis 2 (H2) is tested through two predictions:

Prediction 2.1: Within each sexually dimorphic primate species, male canines

are expected to exhibit greater FA than canines of females.

Prediction 2.2: Within species with minimal or no sexual dimorphism, male and

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female canines are expected to express similar FA.

H2 is tested in two stages. Stage 1 includes species whose sample sizes meet the minimum requirement of N=30 (Table 21). In order for the species to be included in stage

1, both males and females of a species must meet the minimum sample size. Sample sizes of males and females of a species, however, may not be equivalent in this first stage of testing. For stage 2 of testing H2 the minimum sample size criteria of N=30 was relaxed

(Table 22). Stage 2 of H2 marks the first time that species with sample sizes below N=30 are included in the analysis. Although detecting a difference in variance can be greatly influenced by sample size (e.g. Palmer, 1994), including species with sample sizes less than N=30 will allow for a greater number of species to be included in testing H2. To reduce the potential effect of small sample sizes, male and female sample sizes of a species will be equivalent. To remain consistent within stage 2 of testing, each species has equivalent male and female sample sizes.

Canine Dimorphism Index

The canine dimorphism (CD) index determined which species were categorized as sexually dimorphic or sexually monomorphic (Table 23; Figures 12 and 13). CD indices were calculated by dividing average BL or MD dimensions of males by the average BL or MD dimension of females.

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Sample Sizes Males Females 1 1 1 1 Species C BL C MD C1BL C1MD C BL C MD C1BL C1MD Cebus apella 94 94 103 103 60 60 58 59 Cercopithecus 42 47 48 46 39 41 32 31 mitis Papio anubis 65 64 58 57 35 35 34 34 Hylobates lar 70 69 71 72 52 52 57 57 Pan troglodytes 37 38 34 34 36 37 32 30 Gorilla gorilla 82 86 83 83 57 57 57 58 Table 21. Sample Sizes for Stage 1 of Testing H2

Sample Sizes Males Females 1 1 1 1 Species C BL C MD C1BL C1MD C BL C MD C1BL C1MD Ateles geoffroyi 14 14 15 15 14 14 15 15 Cebus albifrons 28 27 28 26 28 27 28 26 Cebus apella 60 60 58 59 60 60 58 59 Cercopithecus 15 15 12 12 15 15 12 12 cephus Cercopithecus 38 40 31 32 38 40 31 32 mitis Colobus guereza 12 12 13 13 12 12 13 13 Lophocebus 14 14 14 11 14 14 14 11 albigena Macaca mulatta 19 19 15 15 19 19 15 15 Macaca 13 13 11 11 13 13 11 11 nemestrina Papio anubis 35 34 34 32 35 34 34 32 Hylobates 18 16 13 15 18 16 13 15 hoolock Hylobates lar 50 52 57 57 50 52 57 57 Pan troglodytes 37 36 32 30 37 36 32 30 Gorilla gorilla 57 57 57 58 57 57 57 58 Table 22. Sample Sizes for Stage 2 of Testing H2

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In comparison to other catarrhines, Hylobates has minimal canine sexual dimorphism (Plavcan, 2001). Both Hylobates species included in this sample have CD

1 indices that fall below 1.10 (Table 23). The CD index of Hylobates’ C and C1 will serve

as the index distinguishing sexually monomorphic species from sexually dimorphic

species. Of the remaining species, CD indices of catarrhine and platyrrhine species fall above the 1.10 cut-off except for A. geoffroyi (Figures 12 and 13). Because only a single tooth dimension of A. geoffroyi (e.g. C1 BL) falls below a CD index of 1.10, this species

will be considered a sexually dimorphic species for the purpose of testing H2.

Testing Hypothesis 2

FA estimates were calculated for both bucco-lingual (BL) and mesio-distal (MD)

1 dimensions of maxillary (C ) and mandibular (C1) canines.

Stage 1

Table 21 lists the sample sizes of non-human primate species used to test H2 in

stage 1. The number of species used to test stage 1 of H2 is limited to six (1 platyrrhine; 5

catarrhine species) due to the minimum sample size requirement of N=30. Prediction 2.1

is examined between males and females of five primate species while prediction 2.2 is

tested only on the canines of H. lar.

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Maxillary Canines Mandibular Canines Species Sex BL CD MD CD BL CD MD CD M 16.80 19.95 18.03 14.61 G. gorilla 1.4226 1.4172 1.4095 1.3639 F 11.81 14.08 12.80 10.71 P. M 11.91 13.43 13.46 11.35 1.2518 1.2123 1.254 1.1851 troglodytes F 9.51 11.08 10.74 9.58 M6.556.566.655.03 H. lar 1.113 1.0721 1.0699 1.0736 F5.896.126.224.69 M7.367.407.395.21 H. hoolock 1.041 1.0759 1.0505 1.0869 F7.076.887.044.79 M 13.27 13.41 13.83 8.08 P. anubis 1.6386 1.7244 1.6167 1.534 F8.107.788.565.27 M. M 10.52 11.61 10.92 6.66 1.7952 1.7422 1.7075 1.5264 nemestrina F5.866.666.404.36 M7.117.507.994.82 M. mulatta 1.3518 1.4358 1.4976 1.3826 F5.265.235.333.49 M6.307.477.424.50 L. albigena 1.352 1.4101 1.3385 1.1752 F4.665.295.553.83 M7.658.998.385.58 C. guereza 1.2858 1.3593 1.2004 1.0763 F5.956.616.985.18 M6.357.466.874.11 C. mitis 1.3811 1.4378 1.3632 1.2317 F4.605.195.043.34 M5.876.295.723.76 C. cephus 1.3403 1.2696 1.2378 1.1402 F4.384.954.623.30 M6.496.877.226.08 C. apella 1.1491 1.1374 1.1814 1.1988 F5.646.046.115.07 M5.505.936.395.08 C. albifrons 1.1235 1.1426 1.1387 1.2304 F4.895.195.614.13 M5.385.875.764.64 A. geoffroyi 1.0614 1.10751.1003 1.1572 F5.075.305.234.01 Table 23. Maxillary and Mandibular Canine Dimorphism Indices

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i) Maxillary BL 1 1.05 1.1 1.15 1.2 1.25 1.3 1.35 1.4 1.45 1.5 1.55 1.6 1.65 1.7 1.75 1.8

H. hoolock C. albifrons P. troglodytes C. cephus G. gorilla P.anubis M. nemestrina A. geofforyi C. apella C. guereza H. lar L. albigena M. mulatta C. mitis

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ii) Maxillary MD 1 1.05 1.1 1.15 1.2 1.25 1.3 1.35 1.4 1.45 1.5 1.55 1.6 1.65 1.7 1.75 1.8

H. hoolock C. albifrons C. cephus C.guereza L. albigena P. anubis H. lar C. paella P. troglodytes G.gorilla M. nemestrina A.geoffroyi M. mulatta C. mitis

Figure 12. Maxillary Canine Dimorphism Index Scales

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i) Mandibular BL 1 1.05 1.1 1.15 1.2 1.25 1.3 1.35 1.4 1.45 1.5 1.55 1.6 1.65 1.7 1.75 1.8

H. hoolock C. albifrons C. cephus G.gorilla M. mulatta P. anubis M. nemestrina H. lar C. paella P. troglodytes L. albigena A. geoffroyi C. guereza C. mitis

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ii) Mandibular MD 1 1.05 1.1 1.15 1.2 1.25 1.3 1.35 1.4 1.45 1.5 1.55 1.6 1.65 1.7 1.75 1.8

H. hoolock A. geoffroyi G.gorilla M. nemestrina H. lar C. cephus C. paella M. mulatta P.anubis C.guereza L. albigena P. troglodytes C.mitis C. albifrons

Figure 13. Mandibular Canine Dimorphism Index Scales

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Stage 2

Sample sizes of the non-human primate species used in stage 2 of testing H2 are

provided in Table 22. Fourteen primate species representing platyrrhines and catarrhines

are included in stage 2. Twelve primate species are used to test prediction 2.1. Prediction

2.2 is examined in the lesser apes (H. lar and H. hoolock).

In stage 2, sample sizes of males and females of a species are equivalent (Table

22). For each species, sample sizes were reduced to match the lowest sample size of C1

1 and C1. Employing this procedure results in sample sizes not being equivalent for C and

1 C1 (Table 22). In some cases (e.g. A. geoffroyi) the C and C1 female sample was lowered

to equal the male sample size. For other species, the male sample size was reduced in

order to match the female sample size. Sample sizes were reduced by performing a

RANDBETWEEN function in Microsoft ® Excel using the individual (IND) specimen number assigned to each specimen during data collection.

Results

1 Results for the two-way mixed model ANOVA of C and C1 for stage 1 and stage

2 of H2 are located in Appendix D. FA estimates of species used to test H2 are available

in Tables 24 (stage 1) and 27 (stage 2). The results of the F-tests used to determine the significance of differences between canine FA of males and females in Tables 25 (Stage

1) and 28 (Stage 2). Figures 7c through 7i provide a visual description of the results.

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Stage 1

Four out of five sexually dimorphic primate species express C1 FA (MD and BL) that is in the expected direction: males of these sexually dimorphic species exhibit greater

C1 FA relative to their female counterparts (Tables 24 and 26; Figure 14). The

comparison between C1 BL FA of G. gorilla males and females is statistically significant with males exhibiting greater FA (Table 25). Thus, only a single comparison – C1 BL FA of G. gorilla males and females – is statistically significant, confirming prediction 2.1 for only G. gorilla. All other C1 FA comparisons between males and females of a species do

not illustrate a significant difference (Table 25). However, FA of C1 MD of P. troglodytes, G. gorilla, and C. apella are close to being statistically significantly greater in males relative to females (Table 25).

At least one C1 dimension of four out of five sexually dimorphic primate species supports prediction 2.1. Males of G. gorilla and P. anubis exhibit greater C1 FA that is

significantly different from females of G. gorilla and P.anubis respectively (Tables 24

and 25; Figure 15). C. apella males express statistically significantly different C1 BL FA

than females (Table 25; Figure 15). Although C1 FA between male and female chimpanzees is not statistically significant, males of P. troglodytes exhibit greater C1 FA

than females (Tables 24 and 25).

The C1 FA between males and females of C. mitis are not statistically different

from each other. However, males of C. mitis do express C1 FA that is in the expected

direction predicted by H3: male C1 FA is greater than female C1 FA.

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FA Estimates Males Females 1 1 1 1 Species C BL C MD C 1BL C 1MD C BL C MD C 1BL C 1MD

‐5 ‐5 ‐5 ‐5 ‐5 ‐5 ‐5 ‐5 Cebus apella 8.86x102.90x10 7.12x10 3.77x10 3.82x10 3.38x10 5.84x10 2.49x10 Cercopithecus 8.14x10 ‐5 9.14x10 ‐5 9.37x10 ‐5 9.45x10 ‐5 7.92x10 ‐5 8.77x10 ‐5 7.11x10 ‐5 8.84x10 ‐5 mitis Papio anubis 7.59x10 ‐5 7.38x10 ‐5 7.44x10 ‐5 4.66x10 ‐5 1.76x10 ‐5 2.96x10 ‐5 5.72x10 ‐5 4.22x10 ‐5 165 Hylobates lar 5.10x10 ‐5 8.27x10 ‐5 3.12x10 ‐5 8.23x10 ‐5 5.91x10 ‐5 7.89x10 ‐5 4.37x10 ‐5 6.49x10 ‐5 Pan 4.88x10 ‐4 5.53x10 ‐4 1.86x10 ‐4 4.93x10 ‐4 3.42x10 ‐4 3.38x10 ‐4 2.00x10 ‐4 3.18x10 ‐4 troglodytes Gorilla gorilla 4.87x10 ‐4 1.52x10 ‐4 2.98x10 ‐4 4.04x10 ‐4 3.02x10 ‐4 9.75x10 ‐5 1.51x10 ‐4 2.77x10 ‐4

Table 24. Canine FA Estimates – H2, Stage 1

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G. G. P. P. P. P. C. C. C. gorilla gorilla troglodytes troglodytes H. lar H. lar anubis anubis mitis C. mitis apella apella Males Females Males Females Males Females Males Females Males Females Males Females Tooth & df df df df df df df df df df df df Dimension C1 BL 77 56 36 35 50 68 63 32 40 19 55 55 C1 MD 77 56 33 30 67 50 62 33 46 39 87 30

C1 BL 82 56 31 25 70 55 56 32 47 30 55 55 166 C1 MD 77 56 33 30 68 54 54 29 46 29 83 51

P. troglodytes P. anubis G. gorilla Males H. lar Males vs. C. mitis Males C. apella Males Males vs. Males vs. vs. Females Females vs. Females vs. Females Females Females

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

1.61 0.0311 1.43 0.1462 1.16 0.2928 4.31 0.0001 1.03 0.4891 2.31 0.0012 1.56 0.0407 1.64 0.0872 1.05 0.4322 2.49 0.0027 1.04 0.453 1.17 0.2819 1.98 0.0037 0.93 0.5805 1.40 0.0916 1.30 0.2139 1.32 0.2117 1.22 0.2317 1.46 0.0687 1.55 0.1143 1.27 0.1913 1.10 0.3987 1.07 0.4308 1.51 0.057

Table 25. F-tests Stage 1 Bolded p-values are statistically significant

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0.0006

0.0005

0.0004 Asymmetry 167

0.0003 Fluctuating

0.0002

0.0001

0 C. apella C. mitis P. anubis P. troglodytes G. gorilla H. lar Species

Male BL Female BL Male MD Female MD

Figure 14. C1 Canine FA Results, Stage 1 “Stars” indicate significant results. “Stars” are placed on the column of the sex that expresses greater FA.

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0.0006

0.0005

0.0004 Asymmetry

0.0003 168 Fluctuating

0.0002

0.0001

0 C. apella C. mitis P. anubis P. troglodytes G. gorilla H. lar Species

Male BL Female BL Male MD Female MD

Figure 15. C1 Canine FA Results for Prediction 2.1, Stage 1 “Stars” indicate significant results. “Stars” are placed on the column of the sex that expresses greater FA.

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Two unexpected results of prediction 2.1 are observed in P. troglodytes and C. apella.

First, the C1 BL FA estimate of P. troglodytes is slightly greater in females than in males

(Table 24); however the difference in canine FA between the sexes is not significant

(Table 25). The second unexpected result is that females of C. apella express slightly greater, but not statistically significant, FA than males in the MD dimension of C1

(Tables 25 and 26).

1 Prediction 2.2 is confirmed in both C (Figure 7d) and C1 of H. lar (Figure 14).

Males and females of H. lar exhibit FA estimates that are not significantly different from

each other in all dimensions (Table 25).

Male > Female, Male > Female, Female > Male, Tooth Statistically Not Statistically Not Statistically Dimension Significant Significant Significant

C1 BL 1 4 ‐

C1 MD ‐ 5 ‐ C1 BL 32‐ 1 C MD 221 Table 26. Results of Comparisons Between Males and Females of Sexually Dimorphic Species – H2, Stage 1 Numbers indicate species which fell into each results category

Stage 2

With the exception of one dimension of P. troglodytes, C1 of sexually dimorphic

species exhibit FA estimates that are in the expected direction of prediction 2.1 (Tables

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FA Estimates Males Females 1 1 1 1 Species C BL C MD C1BL C1MD C BL C MD C1BL C1MD

Ateles geoffroyi 6.61x10‐5 4.83x10‐5 1.74x10‐5 9.12x10‐5 5.48x10‐5 1.85x10‐5 1.49x10‐5 7.38x10‐5

Cebus albifrons 5.45x10‐5 4.43x10‐5 4.83x10‐5 3.49x10‐5 2.68x10‐5 2.65x10‐5 2.97x10‐5 3.00x10‐5 Cebus apella 7.70x10‐5 2.12x10‐5 6.70x10‐5 3.98x10‐5 3.82x10‐5 3.38x10‐5 5.84x10‐5 2.49x10‐5 Cercopithecus 3.52x10‐5 1.64x10‐5 2.39x10‐5 7.77x10‐5 2.96x10‐5 2.56x10‐5 2.08x10‐5 7.23x10‐5 cephus Cercopithecus 8.57x10‐5 1.02x10‐4 1.21x10‐4 1.43x10‐4 8.34x10‐5 8.77x10‐5 7.11x10‐5 8.84x10‐5 mitis Colobus 6.13x10‐6 9.90x10‐6 6.25x10‐6 1.20x10‐5 8.78x10‐5 4.15x10‐6 4.31x10‐6 5.09x10‐6 170 guereza Lophocebus 3.98x10‐5 3.95x10‐5 1.96x10‐5 2.13x10‐4 1.70x10‐5 3.64x10‐5 1.90x10‐5 6.51x10‐5 albigena Macaca 3.86x10‐5 3.81x10‐4 2.58x10‐5 3.99x10‐5 3.27x10‐5 1.10x10‐4 2.44x10‐5 3.84x10‐5 mulatta Macaca 3.52x10‐4 6.93x10‐5 2.86x10‐5 6.61x10‐5 2.18x10‐5 5.76x10‐5 2.35x10‐5 4.79x10‐5 nemestrina Papio anubis 1.13x10‐5 8.34x10‐5 5.93x10‐5 4.24x10‐5 1.76x10‐5 2.96x10‐5 5.72x10‐5 4.22x10‐5 Hylobates 2.67x10‐4 4.43x10‐5 1.58x10‐5 5.28x10‐5 2.66x10‐5 4.80x10‐5 2.18x10‐5 5.71x10‐5 hoolock Hylobates lar 6.00x10‐5 8.58x10‐5 3.59x10‐5 8.45x10‐5 5.61x10‐5 7.89x10‐5 4.37x10‐5 6.49x10‐5

Pan troglodytes 4.95x10‐4 5.63x10‐4 1.84x10‐4 5.57x10‐4 3.42x10‐4 3.38x10‐4 2.00x10‐4 3.18x10‐4

‐4 ‐5 ‐4 ‐4 ‐4 ‐5 ‐4 ‐4 Gorilla gorilla 5.06x10 9.85x10 1.89x10 3.44x10 3.02x10 9.75x10 1.51x10 2.77x10 Table 27. Canine FA Estimates – H2

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27 and 29; Figures 16 and 17). Two sexually dimorphic species express significant

differences in C1 FA estimates (Table 28). These species are C. apella (C1 BL) and L.

albigena (C1 MD) (Table 28). The remaining sexually dimorphic species (N= 10) express

C1 FA that is in the expected direction but is not statistically significantly different

between the sexes. An unexpected result is observed in P. troglodytes. FA C1 BL

estimate of P. troglodytes females is greater than males (Table 28). The difference in C1

BL FA estimates of P. troglodytes, however, is not significant (Table 28).

The results of C1 FA are divided by canine dimension. Of the sexually dimorphic

species for which males exhibit greater C1 BL FA than females, differences between

males and females are significantly different in the following species: C. albifrons, C.

apella, M. nemestrina, P. anubis, P. troglodytes, and G. gorilla (Table 28; Figure 18).

Male C1 BL FA of L. albigena is close to being statistically greater than female C1 BL

FA. The four other sexually dimorphic species –M. mulatta, C. mitis, C. cephus, and A. geoffroyi – exhibit C1 BL FA that is in the expected direction of prediction 2.1 but do not

express statistically significant differences between males and females. Finally, C1 BL

FA of C. guereza is in an unpredicted direction (Table 27). C. guereza females express significantly greater C1 BL FA than males (Table 28; Figure 18).

Among sexually dimorphic species, prediction 2.1 is confirmed in C1 MD of two

species: M. mulatta, and P. anubis (Tables 27 and 28; Figure 19). Males of these two species express significantly greater C1 MD FA than their female counterparts

respectively (Table 28). A. geoffroyi males express C1 MD FA that is in the expected

direction of prediction 2.1 but is not quite statistically significant (Table 28). Of the

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G. G. P. P. H. H. P. P. M. gorilla gorilla troglodytes troglodytes H. lar H. lar hoolock hoolock anubis anubis nemestrina Males Females Males Females Males Females Males Females Males Females Males Tooth & df df df df df df df df df df df Dimension C1 BL 56 56 35 35 48 47 15 16 34 32 12 C1 MD 56 56 35 36 56 56 15 16 34 33 12

C1 BL 56 56 31 34 56 55 11 12 32 32 10

C1 MD 57 56 29 29 54 54 13 13 30 29 10

M. M. M. L. L. C. C. C. C. C. C. 172 nemestrina mulatta mulatta albigena albigena guereza guereza mitis C. mitis cephus cephus apella Females Males Females Males Females Males Females Males Females Males Females Males df df df df df df df df df df df df

12 17 17 12 11 8 9 36 19 14 13 57 12 18 18 13 12 10 8 40 39 13 13 57 914 13 12 11 10 9313010 10 56 10 13 12 10 9 11 8 30 29 11 10 54

Continued Table 28. F-tests for H2, Stage 2

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Table 28 Continued

G. gorilla P. troglodytes H. lar H. hoolock C. C. C. A. A. Males vs. Males vs. Males vs. Males vs. apella albifrons albifrons geoffroyi geoffroyi Females Females Females Females Females Males Females Males Females df df df df df F ‐ratio PF‐ratio PF‐ratio PF‐ratio P

55 26 25 13 12 1.67 0.0287 1.45 0.1383 1.07 0.3741 10.05 0.0001 55 24 22 12 11 1.01 0.4852 1.11 0.3782 1.09 0.4087 1.08 0.443 173 55 24 23 12 12 1.25 0.2032 1.09 0.3739 1.22 0.2310 1.38 0.3005 51 25 24 13 14 1.24 0.2110 1.75 0.0689 1.30 0.1690 1.08 0.4459

P. anubis M. nemestrina M. mulatta L. albigena C. guereza C. mitis C. cephus Males vs. Males vs. Males vs. Males vs. Males vs. Males vs. Males vs. Females Females Females Females Females Females Females

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

6.40 0.0001 16.17 0.0001 1.18 0.3684 2.35 0.0839 14.33 0.0005 1.03 0.4875 1.19 0.3797 2.82 0.0018 1.20 0.3786 3.45 0.0059 1.08 0.4500 2.31 0.1241 1.16 0.3221 1.56 0.2167 1.04 0.4562 1.22 0.3875 1.06 0.4609 1.03 0.4839 1.45 0.2939 1.72 0.0705 1.15 0.4152 1.00 0.5008 1.38 0.3101 1.04 0.4760 3.27 0.0444 2.35 0.1175 1.62 0.0987 1.07 0.4614

Continued

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Table 28 Continued C. apella C. albifrons A. geoffroyi Males vs. Males vs. Males vs. Females Females Females

F ‐ratio PF‐ratio PF‐ratio P

2.01 0.0051 2.03 0.0404 1.2 0.3793 1.59 0.0678 1.67 0.1081 2.61 0.0614 1.15 0.3025 1.63 0.1229 1.17 0.3860 1.59 0.0487 1.16 0.3593 1.24 0.3466 174

146

0.00035

0.0003

0.00025

0.0002 Asymmetry

175 0.00015 Fluctuating

0.0001

0.00005

0 A. geofforyi C. albifrons C. apella C. cephus C.mitis C. guereza L. albigena M. mulatta M. P. anubis P. G. gorilla nemestrina troglodytes Species

Male BL Female BL

Figure 16. C1 BL FA Results for Prediction 2.1, Stage 2 “Stars” indicate significant results. “Stars” are placed on the column of the sex that expresses greater FA.

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0.0006

0.0005

0.0004 Asymmetry 176 0.0003 Fluctuating

0.0002

0.0001

0 A. geofforyi C. albifrons C. apella C. cephus C.mitis C. guereza L. albigena M. mulatta M. P. anubis P. G. gorilla nemestrina troglodytes Species

Male MD Female MD

Figure 17. C1 MD FA Results for Prediction 2.1, Stage 2 “Stars” indicate significant results. “Stars” are placed on the column of the sex that expresses greater FA.

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0.0006

0.0005

0.0004 177 Asymmetry 0.0003 Fluctuating

0.0002

0.0001

0 A. geofforyi C. albifrons C. apella C. cephus C.mitis C. guereza L. albigena M. mulatta M. P. anubis P. G. gorilla nemestrina troglodytes Species

Male BL Female BL

1 Figure 18. C BL FA Results for Prediction 2.1, Stage 2 “Stars” indicate significant results. “Stars” are placed on the column of the sex that expresses greater FA.

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0.0006

0.0005

0.0004 Asymmetry 0.0003 178 Fluctuating

0.0002

0.0001

0 A. geofforyi C. albifrons C. apella C. cephus C.mitis C. guereza L. albigena M. mulatta M. P. anubis P. G. gorilla nemestrina troglodytes Species

Male MD Female MD

1 Figure 19. C MD FA Results for Prediction 2.1, Stage 2 “Stars” indicate significant results. “Stars” are placed on the column of the sex that expresses greater FA.

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remaining species, six species express C1 MD FA that is in the expected direction;

however, male canine FA is not statistically greater than female canine FA (Tables 27

and 28). An unexpected result is that females of C. apella and C. cephus express greater

FA than males in C1 MD dimension. These results are not statistically significant (Table

28).

To confirm prediction 2.2, differences between males and females should not be

statistically significant. FA of the maxillary canine in H. lar supports prediction 2.2: male

and female C1 FA is not significantly different from each other (Table 28). The MD dimension of C1 of H. lar expresses FA that is not statistically different between males

and females, supporting prediction 2.2 (Table 28; Figure 20). The results of H. hoolock

1 1 C1 FA and C MD FA support prediction 2.2. However, C BL of H. hoolock is

statistically different between males and females (Table 28; Figure 20).

Male > Female, Male > Female, Female > Male, Female > Male, Tooth Statistically Not Statistically Statistically Not Statistically Dimension Significant Significant Significant Significant

C1 BL 0 11 ‐‐

C1 MD 2 10 ‐ 1 C1 BL 561‐ 1 C MD 28‐ 2 Table 29. Results of Comparisons Between Males and Females of Sexually Dimorphic Species – H2, Stage 2 Numbers indicate species which fell into each results category

179

0.0003

0.00025

0.0002 Asymmetry 0.00015 Fluctuating

180 0.0001

0.00005

0 H. hoolock H. lar H. hoolock H. lar Species

Mandibular Male BL Mandibular Female BL Mandibular Male MD Mandibular Female MD Maxillary Male BL Maxillary Female BL Maxillary Male MD Maxillary Female BL Figure 20. C1 and C1 FA Results for Prediction 2.2, Stage 2 “Stars” indicate significant results. “Stars” are placed on the column of the sex that expresses greater FA.

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Discussion

This chapter represents the first step in testing the association between elevated

FA and sexual selection. Through comparing male and female canine FA, it is not possible to tease apart the potential effect of ‘developmental destabilization’ brought

about by sexual selection and the potential effect of prolonged canine crown formation

times in males, also brought about by sexual selection. The primary goal for this chapter is to identify if males and females of sexually dimorphic species exhibit differences in canine FA and if the sexes of sexually monomorphic species express similar canine FA.

The following patterns emerged from testing H2:

1. Males of sexually dimorphic species were found to express significantly greater

C1 FA in at least one dimension than females in three species in stage 1 and seven

species in stage 2.

2. Within sexually dimorphic species, male C1 was found to be significantly greater

than female canine FA in one species in stage 1 and two species in stage 2.

3. Six sexually dimorphic species (stage 1 = 3; stage 2 = 3) exhibited male C1 FA in

at least one dimension that fell just short of being statistically significantly greater

1 than female C1 FA. An additional two species in stage 2 expressed male C FA

that was greater than female C1 FA but was not quite statistically significant.

4. In at least one C1 dimension, three species (stage 1) and ten species (stage 2) of

the sexually dimorphic species included in this study expressed C1 FA in the

expected direction predicted by H2 but these differences were not found to be

statistically different between the sexes.

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5. Among the results for C1 FA, one species (stage 1) and eleven species (stage 2) of

sexually dimorphic species illustrate C1 FA in at least one dimension that is in the

direction predicted by H2. However, these results are not statistically significant.

6. H. lar’s canine FA was in the expected direction predicted by H2 in both stages of

1 testing. While C1 FA of H. hoolock adhered to prediction 2.2 more so than C .

Considering both ‘developmental destabilization’ and WOV, sexually dimorphic species should exhibit differences in canine FA between males and females. Canine FA of sexually dimorphic species supported prediction 2.1 if males exhibited a significantly greater C1 FA than females. By applying this criteria to test H2, not all sexually dimorphic species were found to support prediction 2.1 even when male C1 FA was in the expected direction (e.g. greater than female C1 FA).

For example, males of the sexually dimorphic large-bodied G. gorilla form their canines for approximately twice as long as their female counterparts (Schwartz and Dean,

2001). In both stages of testing, C1 BL FA of G. gorilla males differed significantly from females. Mandibular BL FA estimates of G. gorilla in stages 1 and 2 differ significantly between the sexes. Thus, at least one canine dimension of G. gorilla did not exhibit significant differences between males and females but did express C1 FA in the expected direction predicted by H2. Moreover, in both stages of testing C1 MD of C. apella males

were found to express greater FA relative to C. apella females; however, the difference in

C1 MD FA between the sexes was not significant (Tables 25 and 28; Figures 14 and 17).

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Plavcan and colleagues (1995) present evidence that the forces which shape

female canine size play a role in the evolution of canine dimorphism in primates. These

authors argue that “highly exaggerated canine dimorphism seen in many anthropoid

primates is a function not just of intense intermale competition for access to mates, but also of coalitionary competition among females,” (Plavcan et al., 1995, p. 266). In a later analysis, Plavcan (1998) found evidence that selection acting on female canines explains

some of the variation observed in anthropoid canine dimorphism. Overall, though,

Plavcan (2001) concludes that canine sexual dimorphism results primarily from sexual selection for male weaponry.

Following FA methodology recommendations (e.g. Palmer and Strobeck, 1986,

2003), canine size was controlled for in this FA analysis. However, if females are contributing to canine dimorphism, then male canines might not follow the predictions of the sexual selection and FA hypothesis (Moller, 1990, 1992; Watson and Thornhill,

1998) or Clarke’s (1992) ‘stress sensitively’ proposal for sexually selected structures.

Male canines of sexually dimorphic species might not be exceedingly more sensitive to developmental stress relative to their female counterparts if female canines are also influenced by ‘developmental destabilization’. If coalitionary competition among females contributes to canine dimorphism in sexually dimorphic anthropoids (Plavcan et al.,

1995),both sexes may be influenced by the predictions of the sexual selection-FA

hypothesis (Moller, 1990, 1992; Watson and Thornhill, 1998). Alternatively, both sexes

may be more sensitive to stress experienced during development as predicted by Clarke

(1992). The influence of directional selection on some females of sexually dimorphic

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anthropoid species might explain why significant differences were not found in all

comparisons between males and females of sexually dimorphic species even though male

C1 FA estimates were generally in the predicted direction (Tables 7e and 7g). For

instance, even though the difference between C1 MD FA of C. apella males and females

was not significant, C. apella males did express greater FA relative to females. Moreover,

C1 BL FA of L. albigena did not express a significant difference between males and females but overall males expressed FA in the predicted direction. FA of M. mulatta (C1

BL) and M. nemestrina (C1 MD)followed a similar pattern: males express greater FA but

the difference in FA between the sexes is not statistically significant (Figures 7g and 7h).

Plavcan and van Schaik (1992) have indicated that C. apella, L. albigena, and both

Macaca species are anthropoid species that show high-frequency and high-intensity intermale competition. Furthermore, females of these four sexually dimorphic primate species are reported to engage in coalitionary competition (Plavcan et al., 1995).

An additional possibility for why some comparisons were not observed to be statistically significantly different may relate to the length of the canine growth period.

Despite males of sexually dimorphic anthropoid species achieving canine dimorphism

through bimaturism (Schwartz and Dean, 2001; Guatelli-Steinberg et al., 2009),

differences in canine growth periods between the sexes may not be sufficiently large

enough to allow for an exceedingly larger number of developmental perturbations to act

upon male canines relative to female canines. For instance, canine crowns of P.

troglodytes males grow for a year longer than canine crowns of their female counterparts

(Schwartz and Dean, 2001). This one year difference in canine crown growth might be

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too short for P. troglodytes males to experience considerably more developmental

perturbations leading to a significantly greater expression of FA in males relative to

females. Moreover, overlap in the growth periods of males and females may influence

canine FA. Although enamel formation times differ between males and females of Cebus

(Guatelli-Steinberg et al., 2009)when the known periodicity for Cebus is applied to both males and females, the sexes express overlapping enamel formation times Thus, an overlap in growth duration between males and females may affect whether male canine

FA is significantly greater than female canine FA.

Finally, the lack of statistical significance in some comparisons, especially those of stage 2, may well be associated with low sample sizes (Smith et al., 1982; Palmer,

1994). Even though an F-test was used to test for differences in FA between males and females, sample size greatly influences the ability to detect a difference in FA between samples (Smith et al., 1982; Palmer, 1994). Sample sizes of eight primate species for stage 2 were below the minimum number of 30 recommended by Palmer (1994) (Table

22).

Conclusion

The results generally lend support the hypothesis that males of sexually dimorphic

primate species exhibit greater FA than their female counterparts and that males and

females of sexually monomorphic species express similar canine FA estimates. Although

the results obtained here support the argument that sexually selected structures express

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greater FA than non-sexually selected structures, a distinction between the potential

effects of ‘developmental destabilization’ and prolonged canine growth in males, both

brought about by sexual selection, cannot be made in this phase of testing. Nor can the

strength of sexual selection acting upon male and female canines or how much of a

difference in canine growth between males and females is needed to generate a

significant difference be determined by the results reported here. Yet, within sexually

dimorphic primate species, male canines do exhibit FA in the expected direction

predicted by H2 even if all comparisons were not statistically significant. Aside from C1

BL of H. hoolock, species with minimal or no canine sexual dimorphism express canine

FA that is not significantly different between males and females.

The next step in testing canine FA will specifically address whether growth duration can explain the association between FA and the sexually selected primate canine by independently examining ‘developmental destabilization’ and prolonged canine growth in male primates.

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CHAPTER 8: FLUCTUATING ASYMMETRY OF THE MALE PRIMATE CANINE

This chapter marks the final step in examining if and to what extent growth

duration is associated with developmental instability (DI). Specifically, this chapter uses

male primate canine fluctuating asymmetry (FA) to determine if growth duration better

explains the association between FA and sexually selected structures than does the sexual

selection–FA hypothesis proposed by other scholars (e.g. Moller, 1992; Moller and

Pomiankowski, 1993; Moller and Swaddle, 1997; Tomkins and Simmons, 2003; Watson

and Thornhill, 1998). The sexual selection-FA hypothesis, discussed here as the

‘developmental destabilization’ hypothesis, proposes that sexually selected structures are more sensitive to developmental perturbations resulting in these structures expressing greater FA relative to non-sexually selected structures (e.g. Moller, 1992; Moller and

Pomiankowski, 1993; Moller and Swaddle, 1997; Tomkins and Simmons, 2003; Watson and Thornhill, 1998).

In the previous chapter, males of sexually dimorphic species were shown to have canine FA which exceeded that of female canine FA; however, only four comparisons between males and females were found to differ significantly in canine FA. Several other comparisons (see Chapter 7) indicated results in the direction predicted by hypothesis 2

(H2) – males of sexually dimorphic species express canine FA that is greater than female

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canine FA – but these results were not found to be statistically significant (see Tables 7e

and 7g). The potential effects of ‘developmental destabilization’ and prolonged canine

growth in males are both brought about by sexual selection. Comparing male and female

canine FA to test H2 did not allow for the potential effects of ‘developmental

destabilization’ and prolonged canine growth to be teased apart.

As discussed in Chapter 7, there are potential reasons for why a statistically

significant difference was not found in several comparisons even though the results were

in the predicted direction. One explanation is that directional selection may also be

influencing female canines if females of sexually dimorphic species contribute to canine

dimorphism (e.g. Plavcan et al., 2005). Or, differences in the duration of canine growth

between the sexes of some sexually dimorphic species might not be long enough to

provide males with opportunities to experience a greater number of developmental

perturbations relative to females. Again, it was not possible to determine if one, both, or

other explanations are associated with the lack of statistical significance in testing H2.

One of the objectives of this dissertation is to investigate the potential effects of

‘developmental destabilization’ and growth duration, referred to as the ‘window of

vulnerability’ (WOV) (Vrijenhoek, 1985). In order to meet this objective it is necessary

to disentangle ‘developmental destabilization’ and growth duration and examine each

independently of the other. Disentangling these potential effects will be attempted

through testing hypothesis 3 (H3). In this chapter, H3 is tested through two approaches.

First, linear regressions (LRs) are used to evaluate the statistical significance of the effects of sexual selection and growth duration on canine FA. Several non-human primate

188 species are used in the LRs in an attempt to understand whether variables associated with sexual selection or estimates of growth duration more closely predict C1 FA. In the second approach, an attempt is made to account for the potential effects of

‘developmental destabilization’ and growth duration through controlled species comparisons. The controlled comparisons are conducted in pairs of species that have either similar growth duration or similar levels of sexual selection but not both.

Hypothesis 3 (H3)

Using male mandibular canines, H3 is tested in some platyrrhine and catarrhine species. Specifically, H3 uses a series of controlled comparisons designed to disentangle the potential effects of ‘developmental destabilization’ and WOV. Comparisons are based on C1 lateral EFTs (Schwartz and Dean, 2001; Guatelli-Steinberg et al., 2009; Schwartz, personal communication, 2012) and CLs (Kay et al., 1988; Plavcan and van Schaik,

1992).

Lateral Enamel Formation Times (EFTs)

With the exception of perikymata (pk) on great ape canines, data collected on pk by Guatelli-Steinberg were used to determine C1 lateral EFTs (Table 30). Species’ periodicities were applied to mean pk/striae counts for 80% crown height or 90% crown height of C1 lateral EFT for each species. Table 30 outlines the mean pk/striae counts for

80% crown height and 90% crown height, the number of specimens from which mean pk/striae counts for 80% crown height and 90% crown height were generated, range and

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* Mean Lateral Enamel Formation Times for 80% and 90% Crown Height of C1

Mean Periodicitiy Estimated Average Age Mean Periodicitiy Estimated Average Age N N 80% pk Range (Avg) Age Range (days; yrs) 90% pk Range (Avg) Age Range (days; yrs) Species Ateles 163.8 5 4 (4) 655.2 655.2; 1.80 182.3 3 4 (4) 729.2 729.2; 2.00 geoffroyi Cebus 172.5 4 5, 6 (5.5) 862.5‐1035 948.75; 2.60 ‐‐5, 6 (5.5) ‐‐ albifrons Cebus apella 164.8 5 4,5 (4.5) 659.2‐824 741.6; 2.03 169 3 4,5 (4.5) 676‐845 760.5; 2.08 Cercocebus 231.5 4 ‐‐‐252 1 ‐‐‐ atys Cercocebus 245 4 4 (4)+ 980 980; 2.68 270.3 3 4 (4) 1081.2 1081.2; 2.96 torquatus

Cercopithecus +

190 225.75 4 4 (4) 903 903; 2.47 251 2 4 (4) 1004 1004; 2.75 mitis

Hylobates ~ 275.75 10 4.33 1194 1194; 3.27 294.5 3 4.33 1275.19 1275.19; 3.49 Hylobates 274 8 ‐‐‐281 2 ‐‐‐ agilis Hylobates lar 4 (4) ‐‐‐‐4 (4) ‐‐ Symphalangus 277.5 2 4,5 (4.5) 1110‐1387.5 1248.75; 3.42 308 1 4,5 (4.5) 1386 1386; 3.80 syndactylus Macaca 222.3 3 4,5 (4.5) 889.2‐1111.5 1000.35; 2.74 243 1 4,5 (4.5) 972‐1215 1093.5; 3.00 nemestrina Papio anubis 176.2 5 5,7 (6) 881‐1233 1057.2; 2.90 202 3 5,7 (6) 1010‐1414 1212; 3.32

Table 30. Mean Lateral EFTs for 80% and 90% Crown Height - New World Monkeys, Old World Monkeys, and Lesser Apes *Information for this table was taken either from Guatelli-Steinberg and colleagues (2009) or from unpublished data collected by Dr. Guatelli-Steinberg. +Periodicity for C. torquatus and C. mitis were provided by Dr. Schwartz. ~Information for Hylobates was determined by combining Hylobates and Symphalangus data.

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average periodicities, estimated C1 lateral EFTs for 80% and 90% crown height, and

mean C1 lateral EFT for 80% and 90% crown height of all species, for which this

information is available. Table 30 does not include great ape data, which are located in

Table 31. Due to limitations associated with sample size or the lack of periodicity

information, some species listed in Table 30 are not used to test H3. For instance,

Cercocebus species were not used to test H3 but their C1 lateral EFTs are provided in

Table 30.

Lateral EFTs of C1 for Hylobates was derived from combining the following: 1) mean pk/striae counts for 80% crown height and 90% crown height of Hylobates agilis and Symphalangus syndactylus and 2) periodicities of Hylobates lar and Symphalangus syndactylus. To calculate C1 FA, H. lar, H. agilis and S. syndactylus male samples were combined. Merging the mean pk/striae counts for 80% crown height and 90% crown height, periodicities, and sample sizes of these lesser apes was done in order to increase the species sample.

Mandibular canine lateral EFTs of great apes were derived from data available in

Schwartz and Dean (2001) and confirmed through personal communication with

Schwartz. Average lateral EFTs for both mean pk/ striae counts of 80% crown height and

90% crown heights of C1 were determined for three great ape species. Table 31 provides

the lateral EFTs of these great ape species. Even though the sample size minimum requirement was relaxed to N=10 in this chapter, P. pygmaeus cannot be used to test H3 because the sample size of this great ape falls below 10.

191

In addition to the lateral EFT data on great apes, Schwartz provided periodicity

information for C. mitis, which is applied to the mean pk/striae counts of 80% and 90%

crown height of C. mitis’ C1 (Table 30). All other periodicity ranges were taken from data

presented in Guatelli-Steinberg and colleagues (2009).

Average Lateral Enamel Average Lateral Enamel Formation Times (days; yrs) Formation Times (days; Species at 80% Crown Height yrs) at 90% Crown Height Pan 1995; 5.47 2198; 6.02 troglodytes Gorilla gorilla 2453; 6.72 2755; 7.55 Table 31. Mean Lateral Formation Times for 80% and 90% Crown Height for Great Apes

Competition Levels (CLs)

CLs are considered to be an empirical measure of competition among primate

species based on intensity and frequency of intra-male competition (Plavcan, 1990;

Plavcan and van Schaik, 1992). Plavcan and colleagues (Kay et al., 1988; Plavcan and

van Schaik, 1992) present four CLs for classifying primate species. Competition level one (CL1) represents low frequency of inter-male competition and low intensity behavior. High frequency and low intensity describes competition level two (CL2) while low frequency and high intensity represents competition level three (CL3). Finally, high frequency inter-male competition and high intensity behavior represent competition level four (CL4). This study follows the classification scheme of Plavcan and van Schaik

(1992) in placing primate species into CLs.

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Regression Analysis

Linear regressions (LR) are used here to evaluate the relationship between C1 FA

and the following three independent variables: mandibular canine (C1) lateral enamel

formation times (EFTs), competition levels (CL), and canine dimorphism (CD) index.

LRs are conducted in three sets. Set 1 focuses mainly on the relationship between canine FA and lateral EFTs. Using nine primate species, the relationship between FA and lateral EFTs is determined. I also evaluate if the strength of the relationship increases when CL or CD is included in the model. In the second set (Set 2) of LRs, the sample size increases to 14 primate species because it is not limited to species with known lateral

EFTs. In this set, the relationship between canine FA and CL is examined. In the final set of LRs (Set 3), the relationship between canine FA and CD is examined in 14 primate species.

Both the linear regressions and the controlled comparisons of this chapter utilize

C1 lateral EFTs as the variable for developmental timing and CL as a variable

representing the strength of sexual selection. LRs also include the variable CD as another

variable representing the strength of sexual selection. Lateral EFTs were taken from the

literature (e.g. Schwartz and Dean, 2001; Guatelli-Steinberg et al., 2009) or determined

through raw data provided by Guatelli-Steinberg and Schwartz. Because lateral EFTs are

1 not available for C , LRs are only conducted on C1. The number of species for which

lateral EFTs are available is restricted by the data currently available in the literature or

obtained through personal communication. As such, the number of primate species

included in the LRs is limited by our present knowledge of C1 lateral EFTs.

193

Lateral EFTs of C1 for Hylobates for the LRs was derived from combining the following: 1) mean pk/striae count for 80% crown height of Hylobates agilis and

Symphalangus syndactylus and 2) periodicities of Hylobates lar and Symphalangus syndactylus. To calculate C1 FA, H. lar, H. agilis and S. syndactylus male samples were combined. Merging the mean pk/striae count for 80% crown height, periodicities, and sample sizes of these lesser apes was done in order to increase the species sample for the

LRs. Combing these three lesser apes is justified because of their phylogeny. Hylobates and Symphalangus have been found to be closely related (Israfil et al., 2011; Matsudaira and Ishida, 2010) while other scholars note the close affiliation between H. lar and H. agilis (e.g. Geissmann, 2002; Matsudaira and Ishida, 2010). In addition to phylogeny,

Hylobates and Symphalangus exhibit similar mean pk/striae counts for 80% crown height and/or periodicity ranges (Guatelli-Steinberg et al., 2009).

Canine dimorphism (CD) index and competition levels (CL) represent the strength of male intra-sexual selection. CD indices for C1 BL and C1 MD outlined in

Chapter 7 (see Figures 12 and 13) will be used here. CLs were developed by Plavcan and

colleagues (Kay et al., 1988; Plavcan, 1990; Plavcan and van Schaik, 1992) and represent

a classification scheme for the strength of male intra-sexual selection. A previous study

which tested the association between maxillary canine (C1) crown height FA and sexual

selection in non-human primates applied CD and CLs (Manning and Chamberlain, 1993).

Strong correlations were found between male C1 FA and CD and C1 FA and CL by

Manning and Chamberlain (1993), supporting the ‘developmental destabilization’

hypothesis, but not ruling out growth duration as a factor. Here, the relationship between

194

CD and FA and CL and FA are tested across several primate species using MD and BL

canine dimensions, rather than using canine crown height.

Aside from Hylobates, C1 FA estimates used for the LRs were obtained from the statistical analysis conducted in Chapter 7. Because FA represents small, random deviations from bilateral symmetry, C1 FA estimates are extremely small in comparison

to CD and canine growth data. FA estimates of C1 were multiplied by 10,000 prior to

conducting the regression analysis. LRs were performed on both BL and MD dimensions

of C1. Table 32 lists the primate species and the corresponding data used to generate the

LRs.

Linear Regression: Results and Discussion

Table 33 lists the results of the first set of LRs for which nine primate species

were included in the analysis (Table 32). The results of the LR conducted on 14 primate

species are available in Tables 34 (Set 2) and 8f (Set 3). Figures 21 through 26 represent a visual illustration of the relationships between FA and lateral EFTs, FA and CL, and

FA and CD.

Linear Regressions: Set 1

Set 1 was conducted to investigate the relationship between FA and growth duration, represented by C1 lateral EFTs (or LEFTS). The relationship of variables – C1

2 FA and C1 lateral EFTs of nine primate species – is statistically significant in the BL (R

2 = 84.96; p-value =0.0004) and MD (R = 81.59; p-value =0.0008) C1 dimensions (Table

195

33; Figures 21 and 22). This means that 84.96% of the observed variation in C1 BL FA of these nine primate species can be explained by C1 lateral EFTs while 81.59% of the

Data Used In Linear Regression: Set 1

C1 BL C1 MD Lateral EFTs for 80% Sample FA Sample FA Species CL CD CD Crown Size (x10,000) Size (x10,000) Height G. gorilla 6.72 3 83 1.40 2.980 83 1.37 4.040 P. troglodytes 5.47 2 34 1.25 1.860 34 1.19 4.932 Hylobates 3.27 1 81 1.07 0.297 82 1.07 0.744 P. anubis 2.90 4 58 1.61 0.744 57 1.53 0.466 M. nemestrina 2.74 4 11 1.71 0.286 11 1.53 0.661 C. mitis 2.47 3 48 1.36 0.937 46 1.23 0.945 C. apella 2.03 4 103 1.18 0.712 103 1.20 0.377 C. albifrons 2.60 3 28 1.14 0.483 26 1.23 0.349 A. geoffroyi 1.80 2 15 1.10 0.174 15 1.16 0.912

Data Used in Linear Regression: Sets 2 and 3

C1 BL C1 MD

Sample FA Sample FA Species CL CD CD Size (x10,000) Size (x10,000)

G. gorilla 3 83 1.40 2.980 83 1.37 4.040 P. troglodytes 2 34 1.25 1.860 34 1.19 4.930 Hylobates 1 81 1.07 0.297 82 1.07 0.774 H. hoolock 1 13 1.05 0.158 15 1.07 0.528 P. anubis 4 58 1.62 0.744 57 1.53 0.466 M. nemestrina 4 11 1.71 0.286 11 1.53 0.661 M. mulatta 4 15 1.50 0.258 15 1.44 0.399 L. albigena 4 14 1.34 0.196 11 1.26 2.130 C. guereza 3 13 1.20 0.063 13 1.14 0.120 C. mitis 3 48 1.36 0.937 46 1.23 0.945 C. apella 4 103 1.18 0.712 103 1.20 0.377 C. albifrons 3 28 1.14 0.483 28 1.23 0.349 A. geoffroyi 2 15 1.10 0.174 15 1.16 0.912 Table 32. Data Used for Linear Regressions (LRs)

196

observed variation in C1 MD FA can be explained by C1 lateral EFTs. It should be noted

that C1 lateral EFTs at 80% crown height were used in the LR analysis because they were available for a greater number of primate species than at C1 lateral EFTs at 90% crown

height.

To further explore what variables might be contributing to FA observed in the

primate C1, two additional variables were examined. In examining the relationships

between C1 FA and CL and C1 FA and CD, statistically significant relationships were not

found (Table 33; Figures 23 and 24). Furthermore, it does not appear that either CL or

CD contribute to the observed variation in C1 FA of these nine primate species (Table

31).

Set 1 also included LRs that examined if the combinations of C1 lateral EFTs and

CL and C1 lateral EFTs and CD could explain the variation in C1 FA better than the

2 variables on their own. The R reported for both combinations (e.g. C1 lateral EFTs and

2 CL and C1 lateral EFTs and CD) is only slightly larger than the R determined for the

relationship between C1 FA and C1 lateral EFTs (Table 33). Thus, the model does not

improve by much when C1 lateral EFTs and an additional variable representing sexual

selection are examined together.

Linear Regressions: Set 2

Adding additional catarrhine species to the analysis did not strengthen the

2 relationship between FA and CL in either the BL or MD dimensions of C1 (C1 BL: R =

2 0%; p-value =0.9817; C1 MD: R = 2.42%; p-value =0.5952) (Table 34; Figure 25).

197

G. gorilla

198 P. troglodytes

C.mitis

C. apella P.anubis

C. albifrons

Hylobates M. nemestrina A. geoffroyi

Figure 21. Graph of C1 BL FA (asy) and Lateral EFTs (LEFTS)

198

P. troglodytes

G. gorilla 199

A. geoffroyi C,mitis

Hylobates M. nemestrina C. apella P.anubis C. albifrons

Figure 22. Graph of C1 MD FA (asy) and Lateral EFTs (LEFTS)

199

C1 BL Dependent R2 of p‐value of Model Variable Model Co‐efficient Coefficient FA = constant + LEFT 0.8496 0.51104 0.0004 FA = constant + CL 0.0001 0.00624 0.9854 FA = constant + CD 0.0219 0.59302 0.704 FA = LEFT + CL 0.8883 LEFT = 0.53341 LEFT = 0.0005 CL = 0.17466 CL = 0.1998 FA = LEFT + CD 0.85058 LEFT = 0.50879 LEFT = 0.0012 CD = 0.11466 CD = 0.8610

C1 MD Dependent R2 of p‐value of Model Variable Model Co‐efficient Coefficient FA = constant + LEFT 0.8159 0.94087 0.0008 FA = constant + CL 0.0913 ‐0.49424 0.4293 FA = constant + CD 0.0062 ‐0.8406 0.8401 FA = LEFT + CL 0.8311 LEFT = 0.91455 LEFT = 0.0022 CL = ‐0.20547 CL = 0.4909 FA = LEFT + CD 0.8433 LEFT = 0.95730 LEFT = 0.0013 CD = ‐1.77051 CD = 0.3456 Table 33. Set 1, Linear Regression Results

Linear Regressions: Set 3

The relationship between FA and CD in both the BL and MD dimensions of C1 is

2 2 not significant (C1 BL: R = 3.45%; p-value =0.5252; C1 MD: R = 0.02%; p-value

=0.8701) (Table 35; Figure 26).

Discussion

The lack of statistical significance in some comparisons could possibility be related to the low number of species (e.g. N= 9 or N= 14) included in the LRs as well as

200 the low sample size of some primate species included in the analysis (e.g. N =11 individuals of M. nemestrina). Given the limitations of this study, the LRs conducted here are the most reliable statistical method that could be performed.

C1 BL Dependent R2 of p‐value of Model Variable Model Co‐efficient Coefficient FA = constant + CL 0.0000 ‐0.00513 0.9817

C1 MD Dependent R2 of p‐value of Model Variable Model Co‐efficient Coefficient FA = constant + CL 0.0242 ‐0.21251 0.5952 Table 34. Set 2, Linear Regression Results

C1 BL Dependent R2 of p‐value of Model Variable Model Co‐efficient Coefficient FA = constant + CD 0.0345 0.74172 0.5252

C1 MD Dependent R2 of p‐value of Model Variable Model Co‐efficient Coefficient FA = constant + CD 0.0023 0.40053 0.8701 Table 35. Set 3, Linear Regression Results

Despite the small species sample (N=9) used to test the relationship between FA and C1 lateral EFTs, the results were significant. The results of the LRs conducted here suggest that developmental timing better explains the variation observed in primate

201

A B

G. gorilla P. troglodytes

G. gorilla

P. troglodytes

C.mitis P.anubis

202 C. apella A. geoffroyi C.mitis C. albifrons Hylobates M. nemestrina Hylobates A. geoffroyi C. albifrons P.anubis M. nemestrina C. apella

Figure 23. Graphs for C1 FA (asy) and Competition Level (cl), Set 1: A. C1 BL FA and Competition Level, B. C1 BL FA and Competition Level

202

A B

G. gorilla P. troglodytes

G. gorilla

P. troglodytes

C. mitis P. anubis 203 C. apella C. mitis A. geoffroyi Hylobates C. albifrons M. nemestrina M. nemestrina Hylobates C. albifrons P. anubis A. geoffroyi C. apella

Figure 24. Graphs for C1 FA (asy) and Canine Dimorphism (cd), Set 1: A. C1 BL FA and Canine Dimorphism, B. C1 BL FA and Canine Dimorphism

203

A B

G. gorilla P. troglodytes

G. gorilla

P. troglodytes

L. albigena

C. mitis P. anubis C. apella C. mitis C. albifrons Hylobates A. geoffroyi 204 M. nemestraina Hylobates M. nemestraina A. geoffroyi C. albifrons P. anubis M. mulatta H. hooloc k C. guereza k M. mulatta H. hooloc C. apella L. albigena C. guereza

Figure 25. Graphs for C1 FA (asy) and Competition Level (cl), Set 2: A C1 BL FA and Competition Level, B C1 BL FA and Competition Level

204

A B

G. gorilla P. troglodytes

G. gorilla

P. troglodytes

L. albigena

C. mitis

C. apella P. anubis

205 A. geoffroyi C. mitis C. albifrons Hylobates M. nemestrina Hylobates M. nemestrina L. albigena H. hoolock C. albifrons A. geoffroyi C. apella P. anubis M. mulatta M. mulatta H. hoolock C. guereza C. guereza

Figure 26. Graphs for C1 FA (asy) and Canine Dimorphism (cd), Set 3: A C1 BL FA and Canine Dimorphism, B C1 BL FA and Canine Dimorphism

205

C1 FA (Tables 33). CL and CD do not contribute to the observed variation in primate C1

FA (Tables 33, 34, and 35; Figures 23 and 24).

Controlled Comparisons

H3 is further tested through two series of controlled comparisons. The first series of controlled comparisons includes primate species with different durations of canine

growth but assigned to the same CL. The second series of controlled comparisons are

between species exhibiting similar growth duration but are classified into different CLs.

Each series of controlled comparisons has predictions that relate to the WOV and

‘developmental destabilization’ hypotheses.

The controlled comparisons are limited by the data available in the literature. In

particular, the availability of both lateral EFTs and periodicity information limited the

number of primate species that could be used for testing of H3. Despite these limitations,

H3 is tested in both platyrrhine and catarrhine species. H3 is tested using both 80% crown

height (H3a) and 90% crown height (H3b).

Table 36 lists the sample sizes of each species used to test H3 as well as their

lateral EFTs, periodicities, CLs, and C1 FA estimates for both BL and MD canine dimensions. In testing H3, the sample size minimum of N=30 was relaxed to N=10 in

order to increase the species sample. Because the number of species that can be used to

test H3 is dependent on C1 lateral EFTs, the species sample was already limited (e.g.

N=13) prior to the beginning of data collection. Although great effort was made to collect

dental data on at least 30 males of each species for which C1 lateral EFTs were available,

206 museum collections limited the number of specimens for which dental measurements could be performed.

Mean 80% Mean 90% crown height: crown height: Average Average Sample Size Lateral EFTs Lateral EFTs

Species (C1 BL, C1 MD) CL (yrs) (yrs) C1 BL FA C1 MD FA

Ateles geoffroyi 15, 15 2 1.80 2.00 1.74x10‐5 9.12x10‐5

Cebus albifrons 28, 26 3 2.60 ‐ 4.83x10‐5 3.49x10‐5

Cebus apella 103, 103 4 2.03 2.08 7.12x10‐5 3.77x10‐5

Cercopithecus 48, 46 3 2.47 2.75 9.37x10‐5 9.45x10‐5 mitis Macaca 11, 11 4 2.74 3.00 2.86x10‐5 6.61x10‐5 nemestrina

Papio anubis 58, 57 4 2.90 3.32 7.44x10‐5 4.66x10‐5

Hylobates 81, 82 1 3.27 3.49 2.97x10‐5 7.74x10‐5

Pan 34, 34 2 5.47 6.02 1.86x10‐4 4.93x10‐4 troglodytes

Gorilla gorilla 83, 83 3 6.72 7.55 ‐4 ‐4 2.98x10 4.04x10 Table 36. Species Used for Controlled Comparisons

The first series of controlled comparisons for both H3a (using 80% crown height) and H3b (using 90% crown height) focuses on species with different C1 lateral EFTs, but assigned to the same CL (Table 37):

1. Under the WOV hypothesis, species with a longer duration of growth are

expected to exhibit significantly greater C1 FA than species with a shorter

duration of growth.

2. Under the ‘developmental destabilization’ hypothesis, species with the same

CL are expected to exhibit C1 FA that does not differ significantly. 207

First Series of Controlled Comparisons H3a: 80% Crown Height H3b: 90% Crown Height Pan troglodytes ‐ Ateles geoffroyi Pan troglodytes ‐ Ateles geoffroyi Gorilla gorilla ‐ Cebus albifrons Gorilla gorilla ‐ Cercopithecus mitis Gorilla gorilla ‐ Cercopithecus mitis Cebus apella ‐ Macaca nemestrina Cebus apella ‐ Macaca nemestrina Cebus apella ‐ Papio anubis Cebus apella ‐ Papio anubis Table 37. First Series of Controlled Comparisons

The second series of controlled comparisons for H3a and H3b focus on species with different CL but have similar C1 lateral EFTs (Table 38):

1. Under the WOV hypothesis, species with similar growth durations are

expected to exhibit C1 FA that is not significantly different.

2. Under the ‘developmental destabilization’ hypothesis, species assigned to a

higher CL are expected to exhibit significantly greater C1 FA than species

assigned to a lower CL.

Second Series of Controlled Comparisons H3a: 80% Crown Height H3b: 90% Crown Height Cebus albifrons ‐ M. nemestrina Cebus apella ‐ Ateles geoffroyi Cebus apella ‐ Ateles geoffroyi Hylobates ‐ Macaca nemestrina Cercopithecus mitis ‐ Macaca nemestrina Hylobates ‐ Papio anubis Cercopithecus mitis ‐ Papio anubis Cercopithecus mitis ‐ Macaca nemestrina Cebus albifrons ‐ P. anubis Cercopithecus mitis ‐ Papio anubis Table 38. Second Series of Controlled Comparisons

208

Figures 27 through 30 provide visual illustrations of the differences and

similarities in developmental timing between species used to test H3. Figures 27 and 28 are associated with comparisons where species are assigned to the same CL but exhibit differences in C1 lateral EFTs. Figures, 29 and 30 depict comparisons where species exhibit similar C1 lateral EFTs but are categorized into different CLs.

8.00

7.00

6.00

5.00 (years)

4.00 EFTs CL3 CL3 Lateral 3.00

CL2 CL4 CL4

2.00

1.00

0.00 A. geoffroyi P. C. albifrons G. gorilla C. mitis G. gorilla C. apella M. C. apella P. anubis troglodytes nesestrina Controlled Comparisons Figure 27. First Series of Controlled Comparisons for 80% Crown Height Each grouping of bars represents a single comparison. CLs are listed for each comparison.

Controlled Comparisons: Results

Tables 38 and 39 contain the results of F-tests for each controlled comparison.

Figures 31 through 38 display the results of the controlled comparisons. These tables and figures are spaced throughout the next several pages in order to correspond to the appropriate description of the controlled comparisons. Within each figure, white stars

209

Figure 28. First Series of Controlled Comparison for 90% Crown Height Each grouping of bars represents a single comparison. CLs are listed for each comparison.

3.50

3.00 CL4 CL4 CL4 CL4 CL3 CL3 CL3 CL3 2.50

CL4 2.00

(years) CL2

EFTs

1.50 Lateral

1.00

0.50

0.00 C. albifrons M. A. geofforyi C. apella C. mitis M. C. mitis P. anubis C. albifrons P.anubis nemestrina nemestrina Controlled Comparisons Figure 29. Second Series of Controlled Comparisons for 80% Crown Height Each grouping of bars represents a single comparison. CLs are listed for each comparison. 210

Figure 30. Visual Depiction of the Second Series of Controlled Comparisons – H3b, 90% Crown Height

indicate statistically significant differences between the species while black stars indicate results that are not quite statistically significant. The stars are placed on the bar of the species with the greater C1 FA. The absence of a star indicates a non-statistically

significant result.

First Series of Controlled Comparisons: Mean Lateral EFTs of 80% Crown Height

Pan troglodytes versus Ateles geoffroyi.

Both A. geoffroyi and P. troglodytes are assigned to CL 2. Because the lateral

EFT C1 of P. troglodytes’ C1 is greater than A. geoffroyi, under the WOV hypothesis P.

troglodytes was predicted to exhibit statistically significantly greater FA than A.geoffroyi

211

A. geoffroyi vs. A. P. C. G. C. C. M. P. P. troglodytes geoffroyi troglodytes albifrons gorilla mitis apella nemestrina anubis Tooth & df df df df df df df df F ‐ratio P Dimension

C1 BL 12 31 24 82 47 55 10 56 10.71 0.0001

C1 MD 13 33 25 77 46 83 10 54 5.41 0.0012

212

C. albifrons vs. C. mitis vs. G. C. apella vs. C. apella vs. P. C. albifrons vs. C. apella vs. A. G. gorilla gorilla M. nemestrina anubis M. nemestrina geoffroyi

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

6.18 0.0001 2.77 0.0001 2.49 0.0598 1.04 0.4425 1.69 0.1952 4.09 0.0053 11.57 0.0001 3.81 0.0001 1.75 0.0831 1.24 0.1867 1.89 0.0956 2.41 0.0083

Continued Table 39. F-tests for Controlled Comparisons Using Mean Lateral EFTs at 80% Crown Height

212

Table 39 continued

C. mitis vs. M. C. mitis vs. P. C. albifrons vs. nemestrina anubis P. anubis

F ‐ratio PF‐ratio PF‐ratio P

3.78 0.0155 1.45 0.0912 1.54 0.1233 1.60 0.2153 2.27 0.0020 1.33 0.2205

213

214

Figure 31. Results for the First Series of Controlled Comparisons - Mean Lateral EFTs at 80% Crown Height – C1 BL White stars indicate that comparisons were statistically significant. Black stars indicate that comparisons are approaching statistical significance (C. apella and M. nemestrina comparison p=0.0598).

214

215

Figure 32. Results for the First Series of Controlled Comparisons - Mean Lateral EFTs at 80% Crown Height – C1 MD White stars indicate that comparisons were statistically significant. Black stars indicate that comparisons are approaching statistical significance (C. apella and M. nemestrina comparison p=0.0831)

215

This comparison supported the WOV hypothesis (Figures 31 and 32): C1 FA of P.

troglodytes is significantly greater than C1 FA of A. geoffroyi (Table 36). These results

are not consistent with the ‘developmental destabilization’ hypothesis.

Gorilla gorilla versus Cebus albifrons

As predicted under the WOV hypothesis, G. gorilla exhibits significantly greater

C1 FA than C. albifrons (Figures 31 and 32). The results of this comparison are not

consistent with the ‘developmental destabilization’ hypothesis.

Gorilla gorilla versus Cercopithecus mitis

Lateral EFTs of G. gorilla and C. mitis differ by 4.25years (Table 36;

Figure 27). G. gorilla was found to express greater C1 FA relative to C. mitis (Figures 31 and 32). This comparison supports the WOV hypothesis, not the ‘developmental destabilization’ hypothesis.

Cebus apella versus Macaca nemestrina

Mandibular canine lateral EFTs of M. nemestrina at 80% crown height is approximately 0.75 years longer than that of C. apella (Table 36; Figure 27). Both species are assigned to the same CL (Table 34). Because the comparison between C. apella and M. nemestrina is not quite statistically significant (Table 39; Figures 31 and

32), the WOV hypothesis is not supported. Rather, this comparison lends support to the

‘developmental destabilization’ hypothesis.

216

Even though this comparison does not support the WOV hypothesis, the FA

difference is in the expected direction because FA of the C1 MD is greater in M.

nemestrina than C. apella (Figure 32). This pattern does not hold when FA of C1 BL is examined because C1BL FA estimates of C. apella are greater than M. nemestrina

(Figure 31).

Cebus apella versus Papio anubis

C. apella and P. anubis are assigned to the same CL level but P. anubis exhibits a

longer canine growth period relative to C. apella (Table 36). Under the WOV hypothesis,

it is predicted that P. anubis will exhibit significantly greater canine FA than C. apella. .

Canine FA of P. anubis is not statistically significantly greater than that of C. apella

(Figures 31 and 32). Thus, the results of this comparison do not support the WOV hypothesis. It is important to note, however, that C1 FA is the direction predicted by the

WOV hypothesis: P. anubis exhibits a greater C1 FA than C. apella (Figures 31 and 32).

Second Series of Controlled Comparisons: Mean Lateral EFTs of 80% Crown Height

Cebus ablifrons versus Macaca nemestrina

M. nemestrina is classified in one CL level higher than C. albifrons but these

species have similar growth durations (Table 36). Under the WOV hypothesis, these

species were predicted to exhibit C1 FA, which does not differ significantly because their

C1 lateral EFTs are similar. These results support the WOV hypothesis (Figures 33 and

34).

217

Cebus apella versus Ateles geoffroyi

These platyrrhines species exhibit similar lateral EFTs but C. apella is assigned to

CL4 while A. geoffoyi is in CL2 (Table 36). The controlled comparison between C.

apella and A. geoffroyi in the BL dimension supports the ‘developmental destabilization’

hypothesis because C. apella has statistically significantly higher C1 BL FA (Figures 33

and 34). In the MD dimension, A. geoffroyi expresses significantly greater C1 FA than C.

apella (Figure 34). The results of this comparison do not lend support to either hypothesis

considered in this chapter. The WOV hypothesis is not supported since a significant

difference in C1 MD FA was found (Figure 34). Moreover, the ‘developmental

destabilization’ hypothesis is also not supported because A. geoffroyi expresses greater C1

MD FA relative to C. apella, which is in the opposite direction predicted by the

‘developmental destabilization’ hypothesis.

Cercopithecus mitis versus Macaca nemestrina

Although assigned to different CLs, C. mitis and M. nemestrina exhibit similar C1 lateral EFTs. With respect to the MD dimension, the comparison between C1 FA

estimates of C. mitis and M. nemestrina supports the WOV hypothesis (Figure 34).

FA of C. mitis is significantly greater in the C1 BL dimension than C1 BL FA of

M. nemestrina (Table 39; Figure 33). This result not lend support to either the WOV or

218

0.00010000

0.00009000

0.00008000

0.00007000

0.00006000 FA 0.00005000 BL

C1 219

0.00004000

0.00003000

0.00002000

0.00001000

0.00000000 C. albifrons M. C. apella A. geoffroyi C. mitis M. C. mitis P. anubis C. albifrons P. anubis nemestrina nemestrina Controlled Comparisons

Figure 33. Results for the Second Series of Controlled Comparisons - Mean Lateral EFTs of 80% Crown Height – C1 BL White stars indicate that comparisons were statistically significant.

219

0.00010000

0.00009000

0.00008000

0.00007000

0.00006000 FA

0.00005000 MD 220 1 C

0.00004000

0.00003000

0.00002000

0.00001000

0.00000000 C. albifrons M. C. apella A. geoffroyi C. mitis M. C. mitis P. anubis C. albifrons P. anubis nemestrina nemestrina Controlled Comparisons

Figure 34. Results for the Second Series of Controlled Comparisons - Mean Lateral EFTs of 80% Crown Height – C1 MD White stars indicate that comparisons were statistically significant. Black stars indicate that comparisons are approaching statistical significance (C. abifrons and M. nemestrina comparison p=0.0956).

220

‘developmental destabilization’ hypotheses (Table 39 and Figure 33).

Cercopithecus mitis versus Papio anubis

FA of C1 BL for C. mitis and P. anubis supports the WOV hypothesis, suggesting

that similar duration of C1 lateral EFTs is associated with canine FA estimates (Figure

33). FA estimates of C1 MD are significantly different between C. mitis and P. anubis,

suggesting support for the ‘developmental destabilization’ hypothesis (Figure 34).

However, the ‘developmental destabilization’ hypothesis is not supported because C.

mitis, which is in a lower CL level than P. anubis, exhibits greater C1 MD FA than P.

anubis. Thus, FA of C1 MD of this comparison does not support the WOV or

‘developmental destabilization’ hypothesis.

Cebus albifrons versus Papio anubis

FA of C1 is not statistically different between C. albifrons and P. anubis (Table

39; Figures 33 and 34). This result supports the WOV hypothesis, suggesting that growth duration is associated with C1 FA estimates.

First Series of Controlled Comparisons at Mean Lateral EFTs at 90% Crown Height

Pan troglodytes versus Ateles geoffroyi

The results of this comparison are similar to the results found when mean lateral

EFTs at 80% crown height were compared between P. troglodytes and A. geoffroyi. The

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A. geoffroyi vs. A. P. G. C. C. M. P. P. troglodytes geoffroyi troglodytes gorilla Hylobates mitis apella nemestrina anubis Tooth & df df df df df df df df F ‐ratio P Dimension

C1 BL 12 31 82 77 47 55 10 56 10.71 0.0001

C1 MD 13 33 77 78 46 83 10 54 5.41 0.0012

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C. mitis vs. G. C. apella vs. C. apella vs. P. C. apella vs. A. Hylobates vs. Hylobates vs. P. gorilla M. nemestrina anubis geoffroyi M. nemestrina anubis

F ‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio PF‐ratio P

2.77 0.0001 2.49 0.0598 1.04 0.4425 4.09 0.0053 1.03 0.5245 2.51 0.0001 3.81 0.0001 1.75 0.0831 1.24 0.1867 2.41 0.0083 1.17 0.4216 1.66 0.0249

Continued Table 40. F-tests for Controlled Comparisons Using Mean Lateral EFTs at 90% Crown Height

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Table 40 continued

C. mitis vs. M. C. mitis vs. P. nemestrina anubis

F ‐ratio PF‐ratio P

3.78 0.0155 1.45 0.0912 1.60 0.2153 2.27 0.0020

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224

Figure 35. Results for the First Series of Controlled Comparisons - Mean Lateral EFTs of 90% Crown Height – C1 BL White stars indicate that comparisons were statistically significant. Black stars indicate that comparisons are approaching statistical significance (C. apella and M. nemestrina comparison p=0.0598)

224

225

Figure 36: Results for the First Series of Controlled Comparisons - Mean Lateral EFTs of 90% Crown Height – C1 MD White stars indicate that comparisons were statistically significant. Black stars indicate that comparisons are approaching statistical significance (C. apella and M. nemestrina comparison p=0.0831).

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WOV hypothesis is supported: P. troglodytes exhibits C1 FA that is statistically greater

than that of A. geoffroyi, (Figures 35 and 36). This result suggests that prolongation of

growth of the male canine is associated with elevated C1 FA.

Gorilla gorilla versus Cercopithecus mitis

Similar to the results found when mean lateral EFTs at 80% crown height were

compared, G. gorilla exhibits C1 FA that is significantly greater than C1 FA of C. mitis.

These results suggest that a longer duration of lateral EFTs is associated with elevated C1

FA in males of these two catarrhines (Figures 35 and 36).

Cebus apella versus Macaca nemestrina

The comparison between C1 FA of C. apella and M. nemestrina is not statistically significant, which lends support to ‘developmental destabilization’ hypothesis (Figures

35 and 36).

Similar to what was reported for C1 MD in the controlled comparison for mean lateral EFTs at 80% crown height, M. nemestrina exhibits greater FA in the MD dimension than C. apella. Unlike the results reported earlier, mean lateral EFTs for 90% crown height the C1 MD FA comparison between M. nemestrina and C. apella

approaching statistical significant (p=0.0831) (Table 40; Figure 36). However, since it is

not statistically significant, the result does not support the WOV hypothesis.

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Cebus apella versus Papio anubis

The results of this comparison are similar to the results found for mean lateral

EFTs at 80% crown height. The comparison between C. apella and P. anubis is not statistically significant, lending support to the ‘developmental destabilization’ hypothesis

(Figures 35 and 36). However, the C1 FA estimations of C. apella and P. anubis are in

the direction predicted by the WOV hypothesis.

Second Series of Controlled Comparisons: Mean Lateral EFTs of 90% Crown Height

Cebus apella versus Ateles geoffroyi

The controlled comparison between C. apella and A. geoffroyi for C1 BL FA

supports the ‘developmental destabilization’ hypothesis (Figures 37 and 38), which is the

same result found when these platyrrhines were compared at 80% crown height.

Additionally, similar results were found for C1 MD FA: neither the WOV nor

‘developmental destabilization’ hypotheses are supported because A. geoffroyi expresses

significantly greater C1 MD FA than C. apella (Table 40).

Hylobates versus Macaca nemestrina

Even though these two primate species are assigned to different CLs their growth

durations are similar (Table 36). FA of C1 for Hylobates and M. nemestrina do not differ

significantly from each other, leading support to the WOV hypothesis (Figure 38).

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Hylobates versus Papio anubis

P. anubis is several CLs above Hylobates; however, C1 laterals EFTs of these

species are similar (Table 36). The results of controlled comparison between P. anubis

and Hylobates produced mixed results. In the BL dimension, P. anubis exhibits

significantly greater C1 FA than Hylobates, leading support to the ‘developmental

destabilization’ hypothesis (Table 40 and Figure 38). Hylobates expresses significantly

greater C1 FA than P. anubis in the MD dimension (Table 40 and Figure 38). The result

of the comparison between Hylobates and P. anubis in the MD dimensions does not lend

support to the WOV hypothesis or the ‘developmental destabilization’ hypothesis.

Cercopithecus mitis versus Macaca nemestrina

The results of this comparison are the same as those reported for 80% crown height (Figure 38). In the MD dimension, the WOV hypothesis is supported. However, in the BL dimension, canine FA of C. mitis and M. nemestrina in the BL dimension does

not lend support to the WOV or the ‘developmental destabilization’ hypotheses (Figure

37).

Cercopithecus mitis versus Papio anubis

FA of C1 BL for C. mitis and P. anubis supports the WOV hypothesis, suggesting

that similar duration of C1 lateral EFTs is associated with canine FA estimates (Figure

37). FA of C1 MD does not support the WOV or ‘developmental destabilization’

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0.00010000

0.00009000

0.00008000

0.00007000

0.00006000 FA 0.00005000 BL 1 C 229

0.00004000

0.00003000

0.00002000

0.00001000

0.00000000 C. apella A. geoffroyi Hylobates M. Hylobates P.anubis C. mitis M. C. mitis P.anubis nemestrina nemestrina Controlled Comparisons

Figure 37. Results for the Second Series of Controlled Comparisons - Mean Lateral EFTs of 90% Crown Height – C1 BL White stars indicate that comparisons were statistically significant.

229

0.00010000

0.00009000

0.00008000

0.00007000

0.00006000 230 FA

0.00005000 MD 1 C

0.00004000

0.00003000

0.00002000

0.00001000

0.00000000 C. apella A. geoffroyi Hylobates M. Hylobates P.anubis C. mitis M. C. mitis P.anubis nemestrina nemestrina Controlled Comparisons

Figure 38. Results for the Second Series of Controlled Comparisons - Mean Lateral EFTs of 90% Crown Height – C1 MD White stars indicate that comparisons were statistically significant.

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hypothesis. FA estimates of C1 MD are significantly different between C. mitis and P. anubis, suggesting support for the ‘developmental destabilization’ hypothesis (Figure

38). However, the ‘developmental destabilization’ hypothesis is not supported because C. mitis, which is in a lower CL level than P. anubis, exhibits greater C1 MD FA than P.

anubis.

Discussion

This chapter represents the final step in investigating whether an association

between growth duration and FA exists. To evaluate if an association between prolonged

periods of growth and FA exists in the sexually selected male primate canine, an attempt

was made to disentangle the ‘developmental destabilization’ and WOV hypotheses.

Towards disentangling these effects, controlled comparisons were performed. In one

series of comparisons, primate species assigned to the same CL but exhibiting different

durations of canine growth were compared. In the second set of comparisons, species

assigned to different CL but which exhibited similar durations of canine growth were

compared. In addition to being limited by data on lateral EFTs, testing of H3 was also

limited due to the criteria for the controlled comparisons. Summaries of the results of

each comparison are provided in Tables 41 and 42. The results of testing H3 can be

summarized as follows:

1. The results of the LRs support a stronger relationship between lateral EFTs

and C1 FA than relationships between CL and C1 FA and CD and C1 FA.

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2. The great apes used to test H3 exhibited statistically significantly greater C1

FA relative to the primate species they were compared to in the first series of

controlled comparisons.

3. Results of comparisons between C. mitis and other catarrhines are consistent

with an association between growth duration and FA in at least one C1

dimension.

4. Comparisons between C. albifrons and catarrhines are consistent with an

association between growth duration and C1 FA.

5. In comparisons where C. apella was compared to a catarrhine species the

results were consistent with the ‘developmental destabilization’ hypothesis.

ˠ Comparison Support for WOV (statistically significant result) 80% CH: P. troglodytes * - A. geoffroyi √ 80% CH: G. gorilla * - C. albifrons √ 80% CH: G. gorilla * - C. mitis √ 80% CH: C. apella - M. nemestrina* 80% CH: C. apella - P. anubis* 90% CH: P. troglodytes * - A. geoffroyi √ 90% CH: G. gorilla * - C. mitis √ 90% CH: C. apella - M. nemestrina*

90% CH: C. apella - P. anubis* Table 41. Results of Comparisons: Same CLs, Different C1 Lateral EFTs *Primate species predicted to express significantly greater C1 FA in a single comparison ˠCheck marks indicate support of WOV in at least one canine dimension.

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Support for WOVˠ Comparison (not statistically significant result)

80% CH: C. albifrons - M. nemestrina √ 80% CH: C. apella - A. geoffroyi 80% CH: C. mitis - M. nemestrina √ 80% CH: C. mitis - P. anubis √ 80% CH: C. albifrons - P. anubis √ 90% CH: C. apella - A. geoffroyi 90% CH: Hylobates - M. nemestrina √ 90% CH: Hylobates - P. anubis 90% CH: C. mitis - M. nemestrina √ 90% CH: C. mitis - P. anubis √ Table 42. Results of Comparisons: Different CLs, Similar C1 Lateral EFTs ˠCheck marks indicate support of WOV in at least one canine dimension

Reprised: Vulnerability to Asymmetry

Great apes have the longest C1 lateral EFTs relative to other primate species in the

study. When compared to other catarrhines as well as platyrrhines, G. gorilla and P.

troglodytes exhibited significantly greater C1 FA. The results of these comparisons

support the WOV hypothesis suggesting that an association between canine FA and

growth duration does exist. The comparisons for which the great apes were included

suggest that species with longer C1 lateral EFTs exhibit significantly greater C1 FA

relative to species with shorter C1 lateral EFTs.

Due to the limitations of this study, only two great ape species were included in testing H3. Although other controlled comparisons, such as C. albifrons and M. nemestrina, are consistent with the WOV hypothesis, the strongest support for the WOV hypothesis is observed in the controlled comparisons that included G. gorilla and P. 233 troglodytes. Moreover, the results indicate that the African great apes are driving the significance of the linear regressions (Table 33; Figures 21 and 22). Thus, the results of controlled comparisons might be a consequence of other biological similarities between these closely related African apes despite the minimum difference in growth of 4 years between the great apes and the monkeys they were compared to (Table 36).

It is possible that the underlying developmental stability process is similar among closely related species. The ability of an organism to buffer developmental perturbations might be similar in closely related species because these species possess similar mechanisms for maintaining developmental stability. As described elsewhere, developmental stability is the result of mechanisms that were effective at buffering the effects of developmental perturbations (Graham et al., 1993; Klingenberg, 2003; Nijhout and Davidowitz, 2003; Zakharov, 1992). If such mechanisms are not successful at buffering perturbations encountered during development, the organism is unable to achieve its target phenotype (Nijhout and Davidowitz, 2003). As the organism experiences developmental perturbations that it cannot buffer, developmental noise accumulates.

Some have argued that selection favors mechanisms resulting in developmental stability in some traits over other traits (e.g. Balmford et al., 1993; Clarke, 1992; Moller and Hoglund, 1991; Fenster and Galloway, 1997). In other words, mechanisms that buffer developmental perturbations have been suggested as being heritable (Hamdoun and Epel, 2007; Klingenberg, 2003; Waddington, 1957; Willmore et al., 2007). If this is

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the case, both developmental stability and developmental instability are potentially

heritable and could easily be similar among closely related species.

With respect to these African great apes, mechanisms which effectively buffer

developmental perturbations might not be as effective as those possessed by monkeys.

Hence, it is possible that the observed significant differences in C1 FA estimates between these great apes and monkeys are associated with P. troglodytes and G. gorilla having similar mechanisms for buffering developmental perturbations that are more similar to each other than to monkeys and/or because these great apes species are experiencing similar developmental perturbations due to residing in similar environments. From the data collected for this dissertation is not possible to determine if G. gorilla and P. troglodytes have similar developmental processes. Nor it is possible to know the precise stressors that individuals of G. gorilla and P. troglodytes encountered during development relative to the monkeys. In order to know whether developmental processes are heritable, additional species of apes as well as additional data would need to be collected. Such an analysis is beyond the scope of the dissertation. What can be said is that G. gorilla and P. troglodytes express significantly greater C1 FA than the monkeys

they were compared to in the controlled comparisons.

Because G. gorilla and P. troglodytes express C1 FA that is significantly different

from monkeys they were compared to, the results of these controlled comparisons are in

direct opposition to the ‘developmental destabilization’ hypothesis. The results of these

comparisons indicate that species experiencing the same intensity of sexual selection (as indicated by CLs) do not express similar C1 FA estimates. For instance, P. troglodytes

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and A.geoffroyi are assigned CL 2; however, C1 FA of P. troglodytes greatly exceeds that

of A.geoffroyi (Table 36; Figures 31, 32, 33, and 34). Rather, the results of these

comparisons are consistent with the WOV hypothesis.

Relative to the other controlled comparisons, comparisons including great apes were especially useful for testing H3 because they examined species with C1 lateral EFTs

that differ by at least four years (Tables 34, 35, and 36). The C1 lateral EFs between the

great apes and the monkeys examined in these controlled comparison may have been

long enough to detect a difference in canine FA. Therefore, the results of these

comparisons – P. troglodytes – A. geoffroyi, G. gorilla – C. albifrons, and G. gorilla – C. mitis – suggest that prolonged growth periods represent an opportunity for growing body structures to experience developmental stress and sustain injury to developing systems.

Cebus apella: The Odd Species Out?

The results that consistently do not lend support to the WOV hypothesis are from the controlled comparisons, which include C. apella. The type of stressors or the intensity of stressors experienced by species samples included here may affect the comparisons.

Nevertheless, possible reasons for why these controlled comparisons do not provide support for the WOV hypothesis can be examined through four questions. These questions are: 1) Could the sample size of a species be an influential factor for whether or not results of a comparison are statistically significant? 2) How much of a difference in canine growth is needed for one species to express statistically greater canine FA relative to another species? 3) Could individuals of C. apella be experiencing more severe and/or

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frequent developmental perturbations relative to both M. nemestrina and P.anubis? 4)

Could M. nemestrina and P.anubis be better at buffering developmental perturbations than C. apella? The following discussion focuses on the controlled comparisons between

C. apella and M. nemestrina and between C. apella and P. anubis.

C. apella and M. nemestrina Controlled Comparisons

Based on the WOV hypothesis, M. nemestrina should have expressed greater FA

than C. apella. Under the ‘developmental destabilization’ hypothesis, M. nemestrina and

C. apella should not express significantly different C1 FA because they are assigned to

the same CL. All controlled comparisons (e.g. 80% and 90% crown heights) between C1

FA of M. nemestrina and C. apella were not significantly different. Thus, these results lend support to the ‘developmental destabilization’ hypothesis because a significant difference in C1 FA was not found between M. nemestrina and C. apella.

Aside from the possibility that these species express similar canine FA because they are assigned to the same CL, sample size variation between M. nemestrina and C.

apella could explain why this comparison did not uphold the WOV hypothesis is (Table

36). The small sample size of M. nemestrina (N=11) might have effected canine FA of

this species. As discussed elsewhere, sample sizes fewer than thirty individuals might

obscure the variance present in the morphological structures (Smith, 1989; Palmer, 1994).

Despite this limitation, sample sizes of less than thirty individuals were included in

testing H3 in order to increase the number of controlled comparisons. In the cases where

sample sizes of one, or both, species are lower than the recommended level, results

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should be viewed cautiously. The differences in sample size, particularly the low sample

size of M. nemestrina, might explain the lack of statistical significance in these

comparisons, but does not shed light on why C. apella expressed slightly greater C1 FA relative to M. nemestrina in one comparison.

A secondary possible explanation for the observed results for comparisons

between C. apella and M. nemestrina is that the difference in lateral EFTs is not long enough to result in one species expressing significantly greater canine FA relative to the other species. At 80% completion of crown height, there is an average difference of 0.74 years between the species. The results of this comparison are in the predicted direction

(e.g. M. nemestrina expresses greater canine FA relative to C. apella), but are not

statistically significant. At 90% completion of crown height, these two species differ in growth by almost a year (0.92 years) (Table 36). The comparison at 90% completion of crown height, however, indicates that C. apella expresses greater C1 FA than M.

nemestrina, although, once again, this comparison is not statistically significant.

Due to the inconsistencies in the results, more than likely C. apella is not

experiencing more stress than M. nemestrina nor is M. nemestrina better at buffering

development perturbations relative to C. apella. If the results of all controlled

comparisons between M. nemestrina and C. apella had indicated that one species

consistently expressed greater C1 FA than the other species, it would be more reasonable

to suggest that the amount of stress being experienced by one species or the success of a

species at buffering perturbations influenced the results. Since the species exhibiting

greater C1 FA is not consistent across the controlled comparisons of M. nemestrina and

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C. apella, the amount of stress experienced and/or buffering ability are not strong

explanations for the observed results between C. apella and M. nemestrina.

C. apella and P. anubis Controlled Comparisons

Under the WOV hypothesis, P. anubis, a species exhibiting a longer C1 lateral

EFTs than C. apella, was expected to express significantly greater C1 FA than C. apella despite these species being assigned to the same CL. A significant difference in C1 FA

estimates was not found in the comparisons between P. anubis and C. apella. These results lend support to the ‘developmental destabilization’ hypothesis because these species are in the same CL. In the BL dimension of C1, P. anubis expresses slightly

greater FA than C. apella, which is in the direction predicted by the WOV hypothesis

(Table 36). The FA estimates of C1 MD, however, are almost identical in these two species.

Sample size is not likely to be an influential factor in comparing C. apella and P. anubis because the sample for both species is above 50 individuals (Table 36). The degree of difference in C1 lateral EFTs is necessary to generate a statistically significant

difference in canine FA between two species does represent a possible factor, which

could be influencing the dental FA of these two species. Lateral EFTs ranges of C1 for C. apella and P. anubis do not overlap and differ, on average, by 0.84 - 1.24 years (Table

30). Even though P. anubis does express C1 FA that is greater than C. apella the lack of

statistical significance could imply that 0.84 – 1. 24 years is not a substantial enough

difference in growth duration for P. anubis to experience more developmental

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perturbations and deviate substantially from development precision to generate

significantly greater dental FA relative to C. apella.

A final possibility is that the amount of stress being experienced by one species, or the success of one species at buffering perturbations, is contributing to C1 FA

estimates in the BL dimension being similar between P. anubis and C.apella.

Size Matters

For testing all the hypotheses in this chapter, the sample size minimum of N=30

was relaxed in order to include additional species such as M. nemestrina, A. geoffroyi,

and C. albifrons. In some of the comparisons where the sample size of M. nemestrina

differs greatly from its counterpart the WOV hypothesis is not supported. Considering

how sensitive FA is as well as how significant size sample is for detecting FA unaffected

by other factors, differences in sample size of species could influence both statistical

power of a comparison as well as the detection of FA (e.g. Palmer, 1994, 1996; Lens et

al., 2002). For instance, when testing for differences in FA between two samples – in this

case, male canine FA of different primate species – the success of detecting a difference

in variance, even when applying an F-test, is highly dependent on sample size (Smith et

al., 1982; Palmer and Strobeck, 1986, 2003; Palmer, 1994). If only a small difference in

FA between the samples being compared exists, the ability to detect this difference in FA

requires both samples to be represented by large sample sizes (Smith et al., 1982; Palmer

and Strobeck, 1986; Palmer, 1994, Palmer and Strobeck, 2003). The small sample size of

M. nemestrina (N=11; Table 36) may be a contributing factor to the lack of support for

240 the WOV hypothesis. In comparisons between M. nemestrina and C. apella as well as M. nemestrina and C. mitis, the sample sizes between M. nemestrina and the other anthropoids differ greatly (Table 36). The sample size of M. nemestrina might be too low to detect an accurate ‘signal’ (i.e. FA) for this species as well as to be too small for a reliable comparison between M. nemestrina and other species. With respect to the latter possibility, comparisons between M. nemestrina and primate species for which a more accurate FA ‘signal’ was detected might be at disadvantage because the sample size between the species differs too much to statistically detect a difference in FA estimates between the species. In other words, the sample size of M. nemestrina predisposes some comparisons to a very low probability of detecting a difference in dental FA M. nemestrina and another species.

Comparisons between C. albifrons and M. nemestrina support the WOV hypothesis. Both C. albifrons and M. nemestrina fall below the minimum of N=30, but their sample sizes are similar (Table 36), which means that detecting a difference in dental FA between these two species might be more probable than between C. apella and

M. nemestrina. Additionally, the controlled comparison between Hylobates and M. nemestrina also support the WOV hypothesis. However, the sample size of Hylobates is larger than that of M. nemestrina (Table 36). Because of the criteria for the controlled comparisons, the WOV hypothesis was supported in this comparison since a significant difference in FA was not found. It is possible that a significance difference in canine FA was not found between M. nemestrina and Hylobates because of the association between

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developmental timing and canine FA or because the sample size of M. nemestrina was

too smallto detect an accurate ‘signal’ of FA.

The WOV hypothesis is supported when A. geoffroyi and P. troglodytes are

compared, but is not supported when A. geoffroyi is compared to C. apella. Although the

sample size of P. troglodytes is above N=30, it is still close to that of A. geoffroyi

suggesting that comparison between these two species is not influenced by the small

sample size of A. geoffroyi (Table 36). However, the difference in sample sizes between

A. geoffroyi and C. apella is large (Table 36). Such a large difference in sample size between these two platyrrhines might affect any comparison between them to a very low

probability of detecting a difference in dental FA.

Conclusion

This chapter addressed whether growth duration could explain the association

between FA and the sexually selected primate canine by independently examining

‘developmental destabilization’ and prolonged canine growth in male primates.

Controlled comparisons were conducted to disentangle the potential effects of

“developmental destabilization” brought about by sexual selection and the potential effect

of prolonged canine growth in males, also brought about by sexual selection.

Results reported for the three sets of linear regressions indicate that C1 lateral

EFTs are more likely to explain the variation observed in C1 FA than either CL or CD

(Table 31). Even when additional catarrhine species were added to the sample, CL and

CD did not show a significant relationship to C1 FA (Tables 32 and 33).

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Controlled comparisons which included a great ape species lend support the

WOV hypothesis. Comparisons between monkeys are not as clear-cut in their support of the WOV as those comparisons with G.gorilla and P. troglodytes. Some comparisons between the monkeys do support the WOV hypothesis. For instance, C. albifrons and M.

nemestrina were found to exhibit similar C1 FA. Additionally, C. mitis and P. anubis

exhibit similar C1 FA in the BL dimension.

Some comparisons between New World Monkeys and Old World Monkeys, such

as those comparisons that include C. apella and P. anubis, lend support to the

‘developmental destabilization’ hypothesis. In the comparison between C. apella and P.

anubis,a significant difference in C1 FA was not found.

Among species in which strong or extreme sexual selection is believed to be

acting upon the primate canine (e.g. species assigned to CL4; Table 36), canine FA

between males of differences primate species lends support to the ‘developmental

destabilization’ hypothesis, suggesting that the FA- sexual selection hypothesis might

account for canine FA in some but not all primate species. It is also possible that the

difference in the length of growth duration, or the window of opportunity, between

primate males is not long enough for one species to experience a greater number of

developmental perturbations and exhibit FA that is significantly different from another

species. If the latter point is accurate then it is not that an association does not exist

between growth duration and canine FA, but rather that a minimum difference in the

length of growth is needed for species assigned to CL4 to express significantly different

C1 FA estimates.

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Overall, it appears that lateral EFTs generally show a consistent association with

C1 FA, particularly among the great apes and in controlled comparisons between some

Old World monkey species. These findings lend support to the WOV hypothesis. Aside from the comparisons between C. apella and P.anubis, the ‘developmental destabilization’ hypothesis was a poor predictor of C1 FA estimates observed between

species assigned to the same CL. Moreover, in several comparisons between species

assigned to different CLs, C1 FA estimates did not support either WOV or

‘developmental destabilization’ hypotheses in at least one dimension. In the other canine

dimension of these comparisons, the WOV hypothesis was supported.

The controlled comparisons of this study were limited not only by sample size of

each species, but also by the canine growth data available in the literature. Until more is

known about canine growth, particularly lateral EFTs and crown formation times, the

investigation into whether growth duration is associated with canine FA in primates is

constrained. Additionally, a future objective is to determine how large a difference

between periods of growth is necessary for FA to be significantly different between

species. With respect to the results of this study, the WOV hypothesis is upheld when

species whose lateral EFTs differ by more than two years are compared.

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CHAPTER 9: DISCUSSION AND CONCLUSIONS

Summary of Objectives

This dissertation addressed the association between prolongation of growth and dental fluctuating asymmetry (FA). FA represents random deviations from perfect symmetry caused by the inability of an organism to resist and/or buffer against stress during growth and development (Van Valen, 1962; Harris and Nweeia, 1980; Kieser et al., 1986; Palmer and Strobeck, 1986). Because the magnitude of FA is assumed to be proportional to the magnitude of local development perturbations, FA is commonly used to infer information on developmental precision, individual quality, and stress experienced during development (e.g. Doyle and Johnston, 1979; Sciulli et al., 1979;

Kieser and Groeneveld, 1986; Moller, 1990, 1992; Markow and Martin, 1993; Carchini et al. 2000; Gray and Marlowe, 2002; Gray and Marlowe, 2002; Prentice et al. 2008;

Dongen et al. 2009). These studies, among others, have revealed a pattern: elevated dental FA estimates are expressed by populations assumed to be either subject to high levels of stress during development or that were unable to successfully buffer against developmental stress, or both.

Vrijenhoek (1985) suggested that relative to body structures that form over short periods of time, those that take longer to form have a greater “widow of vulnerability”

(WOV) to accumulate disruptions during development. Prolonged growth periods could 245 result in costs to an organism’s developmental stability (DS), such as an increase in developmental noise (DN) observed through elevated FA. Within mammals, hominoids tend to show elevated FA in osteometric traits in comparison to mammals with shorter periods of growth (Hallgrimsson 1995). An increase in DN could therefore be a cost of prolonged growth periods for some mammalian species. Thus, populations once thought to be experiencing high levels of stress or believed to be unable to successfully buffer development perturbations, or both, might actually be experiencing a longer duration of growth, predisposing them to a greater WOV relative to other populations.

Because FA estimates are commonly used to infer the intensity or level of stress experienced during development and/or developmental precision of one population relative to another, it is important to understand what underlying variables might affect the expression of FA in morphological structures. This study aimed to establish if developmental timing could explain the variation observed in both first molar and canine

FA of several non-human primate species. The overarching objective of this dissertation was to determine if an association between growth duration and variation in dental FA expression is present across primate species. A secondary objective of this project focused on whether prolonged periods of growth could explain the association between

FA and sexually selected structures. To accomplish these objectives, dental FA of non- sexually selected and sexually selected teeth were compared among primate species.

Comparing the first molar FA among primate species was done to establish if and to what extent growth duration and FA are associated in a non-sexually selected structure. By doing this, a baseline was set for whether growth duration contributed to dental FA in

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primates. Life history schedules of primates, in addition to weaning age, were used as proxies for developmental timing to further explore whether or not developmental timing could explain the variation observed in first molar (M1) FA among primates.

With the intention of expanding upon our knowledge of FA in sexually selected structures, the dissertation assessed the extent to which canine FA differed between males and females of a species. The inclusion of both platyrrhines and catarrhines is important, especially considering how infrequently platyrrhines are included in studies addressing canine FA as well as canine growth. Following the comparisons of male and female C1

FA, linear regressions (LRs) were used to investigate if growth duration and C1 FA are

associated. Next, an attempt to disentangle the potential effects of ‘developmental

destabilization’ and growth duration was performed through a series of controlled

comparisons. These controlled comparisons are unique to this study and represent the first time primate canine FA has been evaluated in reference to both sexual selection and prolongation of growth.

Summary of Hypotheses

To meet the primary objective of the dissertation, three hypotheses were

constructed. The dissertation hypotheses were tested in Chapters 5-8. The following

discussion summarizes the interpretation of results for the three hypotheses tested.

The first hypothesis (H1) addressed the influence of growth duration on M1 FA, a

non-sexually selected structure. H1 was tested in two different phases (i.e., H1a and

H1b). Both phases predicted that primate species with longer M1 growth periods would

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exhibit FA that was greater than species with shorter M1 growth periods because they

had more time to experience perturbations resulting in a decrease in developmental

stability (DS). In H1a, six of the ten predictions were upheld suggesting that, given the

same level of stress, primates exhibiting longer periods of growth are more likely to express elevated FA. The prediction that G. gorilla would exhibit the greatest M1 FA was

not upheld. Rather results indicated that P. troglodytes exhibited the greatest M1 FA.

Furthermore, M1 FA estimates of P. troglodytes and G. gorilla differed significantly

despite M1 crown formation times (CFTs) of P. troglodytes and G. gorilla varying only

by a few months (Schwartz et al., 2006; Smith et al., 2007). With respect to M1 FA of the

great apes, the results suggest that P. troglodytes is either not successfully buffering

developmental perturbations or experiencing more frequent or serve perturbations

relative to G. gorilla.

H1 was further tested in Chapter 6 using a continuum of life history (LH)

schedules of primate species as well as the specific ontogenetic event of weaning as

proxies for developmental timing. Incorporated into the testing of H1b was a linear

regression (LR) of M1 FA and age at weaning. The results of the LR were significant,

suggesting that a strong relationship between M1 FA and developmental timing. These

results of H1b lend support to a LH divergence between apes and Old World monkeys, as

argued by other scholars (e.g. Harvey and Clutton-Brock, 1985; Watts, 1990; Kelley,

1997) because great apes express significantly larger first molar FA estimates relative to

Old World monkeys. With respect to the proposed difference in M1 FA between

folivores and frugivores, M1 FA of C. guereza is generally in the predicted direction (e.g.

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less than the frugivores Old World monkeys). However, only a few comparisons

indicated that M1 FA was significantly different between C. guereza and other Old

World monkeys.

Overall, the results of testing H1a and H1b lend support to the hypothesis that the

length of developmental timing provides a WOV for which to experience perturbations

and deviate from bilateral symmetry. Those species with prolonged periods of growth

generally expressed greater FA relative to species with shorten periods of growth.

With Hypothesis 2 (H2), the focus of the dissertation turned to FA in the sexually selected primate canine. The relationship between canine dimorphism and elevated FA was examined by comparing canine FA estimates of male and female of monomorphic and dimorphic primate species. H2 was tested in two stages, which differed by the number of species included in the analysis. To increase the number of species included in testing H2, the minimum sample size requirement was relaxed to N=10 in stage 2 of H2.

Males of sexually dimorphic species were shown to have canine FA exceeding that of female canine FA. Across both stages of testing, males of six sexually dimorphic species

1 expressed greater C FA than females while males had greater C1 FA than females in 13 sexually dimorphic species. However, only four comparisons between male and female canine FA were found to be significantly different (see Tables 7e and 7g). Males and females of H. lar expressed similar (e.g. statistically insignificant) canine FA estimates in both stages of testing. However, canine FA of the other monomorphic species – H.

1 hoolock – supported the predictions of H2 in C1 but not C .

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The results of testing H2 support the notion that sexually selected structures express greater FA than non-sexually selected structures since the sexually selected male primate canine generally expressed greater canine FA than the non-sexually dimorphic female canine. A distinction between the potential effects of ‘developmental destabilization’ and prolonged canine growth in males could not be made from comparing canine FA estimates of males and females of a primate species. The potential effects of ‘developmental destabilization’ and prolonged canine growth in males could not be separated out in testing H2 because both are brought about by sexual selection.

Rather, testing H2 established that sexually selected structures are more likely to exhibit elevated FA relative to non-sexually selected structures.

Despite the finding that males of sexually dimorphic species exhibited elevated canine FA relative to females, many comparisons between the sexes were not statistically significant. It is possible that the small difference in the growth period of male and female canines in some species contributed to the lack of statistical significance.

Moreover, it is also possible that coalitionary competition among females contributes to canine dimorphism in sexually dimorphic anthropoid species (Plavcan et al., 1995).

Either of the above options could result in males either not having a growth period that differs enough from females to accumulate significantly more developmental perturbations or not being more prone to developmental perturbations relative to females because female canines are also under strong directional selection. These options might not be influencing canine FA at all, or could be specific to one primate species and not

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another. In stage 2 of H2, where sample sizes of some species were below N=30, a non-

statistically significant result could be due to low sample size.

Hypothesis 3 (H3) aimed to disentangle the potential effects of ‘developmental

destabilization’ and prolonged canine growth in male primates through two approaches.

In the first approach used in H3 an attempt to understand which variable, or variables,

more closely predicts FA C1 of was made through performing sets of LRs. Three

variables were used: C1 lateral enamel formation times (EFTs), competition levels (CL),

and canine dimorphism (CD). Mandibular lateral EFTs served as the variable for canine growth in both approaches used in H3. CD index and CL represent the strength of sexual selection and, therefore serve as variables representing sexual selection for the LRs. The results of the LRs support to a stronger relationship between C1 lateral EFTs and C1 FA than relationships between CL and C1 FA and CD and C1 FA.

In the second approach used to test H3, controlled comparisons were constructed

in an attempt to separate out the potential effects of ‘developmental destabilization’ and growth duration. Using C1 lateral EFTs for both 80% and 90% crown height as the

growth variable and CLs to represent the strength of sexual selection, two series of

controlled comparisons were performed. Each series of controlled comparisons applied different predictions to account for ‘developmental destabilization’ hypothesis or WOV hypothesis. Moreover, because of the criteria established for the controlled comparisons,

different species were compared for each prediction. For example, P. troglodytes’ C1 lateral EFT for both 80% and 90% crown height is compared to that of A. geoffroyi because males of these two primate species are assigned to the same CL but exhibit

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different durations of growth. Conversely, C1 lateral EFT for 90% crown height of

Hylobates and M. nemestrina are compared because these male catarrhines exhibit

similar growth but are classified to different CLs.

G. gorilla and P. troglodytes exhibited significantly greater C1 FA relative to the

primate species they were compared to (see Tables 8h and 8i). The results of these

comparisons are consistent with the WOV hypothesis. The controlled comparisons at C1

lateral EFT for 90% crown height, which included the lesser apes produced mixed

results. One comparison (Hylobates and M. nemestrina) was consistent with the WOV

hypothesis. However, the comparison between Hylobates and P. anubis did not lend

support to either the WOV or ‘developmental destabilization’ hypothesis. Even though a statistically significant difference in C1 FA estimates was found between Hylobates and

P. anubis, P. anubis did not consistently exhibit greater FA than Hylobates. If the

‘developmental destabilization’ hypothesis were to be supported, P. anubis, not

Hylobates, would exhibit greater C1 FA in both the BL and MD dimensions.

Among the controlled comparisons that compared C. apella to either another New

World monkey or two Old World monkeys (e.g. M. nemestrina and P. anubis), the results were not consistent with the WOV hypothesis. The trend observed across the controlled comparisons that contain C. apella suggest that that the ‘developmental destabilization’ hypothesis is a likely explanation for the observed results. However, it is also entirely possible that individuals of C. apella included in this study encountered stressors at more frequent intervals than the other species included in this study and/or experienced more

intense stressors, which caused a significant insult to the developmental system. The

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frequency or intensity of stressors could result in the presence of developmental noise especially if the mechanisms responsible for maintaining developmental stability failed to buffer developmental perturbations, possibly because the system was overloaded with perturbations, causing a significant insult to the system expressed through elevate FA.

Overall, lateral EFTs generally show a consistent association with C1 FA,

particularly among the great apes and in controlled comparisons between some monkey

species. These findings lend support to the WOV hypothesis. Aside from the comparison

between C. apella and P. anubis, the ‘developmental destabilization’ hypothesis proved

to be a poor indicator of canine FA among primate species assigned to the same CL. In

other comparisons between species of different CLs (e.g. M. nemestrina and C. mitis, C.

apella and A. geoffroyi, and Hylobates and P. anubis) the C1 FA estimates did not support either the WOV or ‘developmental destabilization’ hypotheses in at least one C1 dimension. In the other canine dimension of these comparisons, the WOV hypothesis was supported.

‘Window of Vulnerability’

So Little Time, Such Great Symmetry

First Molars

1 Relative to CFTs available for M1, the data on M CFT was limited to three species for testing H1. Of these three species, A. geoffroyi possessed the shortest M1 CFT

as well as the lowest M1 FA, supporting the WOV hypothesis. However, because this

platyrrhine was compared only to two great ape species – G. gorilla and P. troglodytes –

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it is not clear whether the great apes exhibited significantly greater FA than A. geoffroyi

for other reasons having to with their close biological relationship to each other or

because they grow their M1 for at least 0.75years longer than A. geoffroyi. Mechanisms to

buffer developmental perturbations might not be as effective in African great apes as the

mechanisms possessed by A. geoffroyi.

M. mulatta exhibited the shortest M1 CFT and expressed the lowest M1 FA. This

result supports the WOV hypothesis – the primate species with the shortest M1 CFT

expressed the lowest M1 FA. However, some species had similar M1 CFTs but did not

differ in first molar FA.

Canines

In testing H3, C1 FA was compared among primate species based on criteria established to disentangle ‘developmental destabilization’ and WOV hypotheses. For

each comparison, males of two species were compared. Thus, the ‘length’ of growth

duration is associated with the comparison being examined. For instance, in comparisons

that contained the great apes – P. troglodytes – A. geoffroyi, G. gorilla – C. albifrons, and

G. gorilla – C. mitis – the results suggest prolonged growth periods represent an opportunity for growing body structures to experience developmental stress and sustain injury to developing systems, especially when the window of opportunity, or length of growth duration, differs by more than two years (see Table 36 and Figures 31 through

38).

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Although a low sample size might have influenced the results of comparisons, it

does appear that when growth duration is similar between M. nemestrina and Hylobates, as well as M. nemestrina and C. albifrons, C1 FA estimates are also similar among these

primate species. Growth durations between M. nemestrina and the above named

catarrhines species differ at most by 0.50 years: by 0.49 years between M. nemestrina and

Hylobates for 90% crown height and by 0.14 years between M. nemestrina and C. albifrons for 80% crown height (Tables 30 and 36). These results are consistent with the

WOV hypothesis and, therefore, suggest that similarity in developmental timing is associated with similar C1 FA.

Sex Differences in Mandibular Canine FA

In testing H2 the predictions centered on whether males of sexually dimorphic species exhibited greater canine FA than females and if males and females of sexually monomorphic species exhibited similar canine FA. Because some comparisons between males and females of sexually dimorphic species were not found to be significant, this discussion section will explore the possibility that the length of growth duration might be associated with a lack of statistical significance among some results of testing H2.

Mandibular canine lateral EFTs used in this discussion were taken from the literature

(e.g. Schwartz and Dean, 2001; Guatelli-Steinberg et al., 2009) or determined through raw data provided by Guatelli-Steinberg and/or Schwartz. The male C1 lateral EFTs for

80% and 90% crown height are the same as those used in Chapter 8 to test H3. Because

females were not used in testing H3, this is the first time female C1 lateral EFTs for 80%

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and 90% crown height are appearing in the dissertation. Tables 43 and 44 provide C1

lateral EFTs for 80% and 90% crown height for both males and females of eight primate

species. Because the species sample is limited by both mean C1 lateral EFT for 80% and

90% crown height and sample size, the discussion here focuses on eight species and

particularly addresses those sexually dimorphic species for which a significant difference

in C1 FA was not found between males and females in Chapter 7 (see Tables 25 and 28).

Finally, because canine lateral EFTs for 80% and 90% crown height are only available

1 for the C1, C is not be included in the following discussion.

In stage 1 of testing H2 (e.g. Chapter 7), five sexually dimorphic species are

examined. All five sexually dimorphic species – G. gorilla, C. apella, C. mitis, P.

anubis, and P. troglodytes, exhibit C1 MD FA that is greater in males than in females, but

is not significantly different. In the BL dimensions of C1, FA of G. gorilla males

exhibited significantly greater C1 BL FA than females. Of the other four sexually

dimorphic species, three species exhibit C1 BL FA that was in the expected direction –

males expressing greater C1 BL FA than females. The difference in C1 BL FA between

males and females of these three species (e.g. C. mitis, C. apella, and P. anubis) were not

statistically significant. P. troglodytes females expressed C1 BL FA that was greater relative to males but not significantly different from males.

Males and females of C. apella differ by 0.35 years at C1 lateral EFTs for 80%

crown height (Tables 43 and 44). The small difference in C1 lateral EFTs for 80% crown

height between C. apella males and females could explain the lack of statistical

significance in this comparison in stage 1 of testing. However, in stage 2 of testing H2,

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* Mean C1 Lateral EFTs for 80% Crown Height Males Females Periodicitiy Average Periodicitiy Average Mean Estimated Mean Estimated N Range Age (days; N Range Age (days; 80% pk Age Range 80% pk Age Range Species (Avg) yrs) (Avg) yrs) Ateles 163.8 5 4 (4) 655.2 655.2; 1.80 135.3 6 4 (4) 541.2 541.2; 1.48 geoffroyi Cebus 948.75; 172.5 4 5, 6 (5.5) 862.5‐1035 117 1 5, 6 (5.5) 585‐702 643.5; 1.76 albifrons 2.60 613.35; Cebus apella 164.8 5 4,5 (4.5) 659.2‐824 741.6; 2.03 136.3 7 4,5 (4.5) 545.2‐681.5

257 1.68 Cercopithecus 225.75 4 4 (4)+ 903 903; 2.47 157 2 4 (4)+ 628 628; 1.72 mitis Macaca 1000.35; 543.15; 222.3 3 4,5 (4.5) 889.2‐1111.5 120.7 3 4,5 (4.5) 482.8‐603.5 nemestrina 2.74 1.49 1057.2; Papio anubis 176.2 5 5,7 (6) 881‐1233 118.3 15 5,7 (6) 591.5‐828.1 709.8; 1.94 2.90 Pan 1995; ‐‐ ‐ ‐ ‐‐ ‐ ‐ 1710; 4.68+ troglodytes 5.47+

2443; + ‐‐ ‐ ‐ + ‐‐ ‐ ‐ 1579; 4.33 Gorilla gorilla 6.72 Table 43: Mean Lateral EFTs for 80% Crown Height *Information for this table was taken either from Guatelli-Steinberg and colleagues (2009) or from unpublished data collected by Guatelli-Steinberg. +Periodicity for C. mitis was provided by Schwartz.

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* Mean C1 Lateral EFTs for 90% Crown Height Males Females Periodicitiy Average Periodicitiy Average Mean Estimated Mean Estimated N Range Age (days; N Range Age (days; 90% pk Age Range 90% pk Age Range Species (Avg) yrs) (Avg) yrs) Ateles 182.3 3 4 (4) 729.2 729.2; 2.00 151.4 5 4 (4) 605.6 605.6; 1.66 geoffroyi Cebus ‐‐5, 6 (5.5) ‐‐126 1 5, 6 (5.5) 630‐756 693; 1.90 albifrons

258 Cebus apella 169 3 4,5 (4.5) 676‐845 760.5; 2.08 ‐‐ ‐ ‐ ‐ Cercopithecus 251 2 4 (4) 1004 1004; 2.75 ‐‐ ‐ ‐ ‐ mitis Macaca 1093.5; 243 1 4,5 (4.5) 972‐1215 152 1 4,5 (4.5) 608‐760 684; 1.87 nemestrina 3.00 Papio anubis 202 3 5,7 (6) 1010‐1414 1212; 3.32 132.7 6 5,7 (6) 663.5‐928.9 796.2; 2.18 Pan 2198; ‐‐ ‐ ‐ ‐‐ ‐ ‐ 1928; 5.28+ troglodytes 6.02+

2755; + ‐‐ ‐ ‐ + ‐‐ ‐ ‐ 1768; 4.84 Gorilla gorilla 7.55 Table 44: Mean Lateral EFTs for 90% Crown Height *Information for this table was taken either from Guatelli-Steinberg and colleagues (2009) or from unpublished data collected by Guatelli-Steinberg. +Periodicity for C. mitis was provided by Schwartz.

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C1 BL FA was found to be significantly greater in C. apella males relative to females. C1

MD FA in stage 2 of H2 is greater in C. apella males than females but was not found to

differ significantly between the sexes. It is very possible that 0.35 years is too small of a

difference in developmental timing to allow for C. apella males to experience a greater

amount of developmental perturbations resulting in statistically significantly different C1

FA estimates relative to females. Furthermore, the estimated lateral EFTs for C. apella males and females overlap when the known periodicity of 4-6 day is applied to the both the mean 80% and 90% perkiymata counts (Tables 43 and 44).

On average, the C1 lateral EFTs for 80% crown height of C. mitis males and females differ by 0.75years (Tables 43 and 44). Across both stages of testing C. mitis males exhibit greater FA than females; however, the difference in C1 FA is not

significantly different between C. mitis males and females. A difference of 0.75 years

might also be too short a window of development to generate C1 FA estimates between C.

mitis males and females which are statistically significantly different.

P. troglodytes males and females differ by approximately the same time frame as

reported for C. mitis for C1 lateral EFTs for both 80% and 90% crown height (Tables 43

and 44). Because 0.75years might be too small of a difference in developmental timing to

generate significant differences in C1 FA, this could explain the results observed in the comparisons between P. troglodytes males and females. In both stages of H2, C1 BL FA of P. troglodytes females is greater than males while C1 MD FA is greater in males than

females. Since the comparisons between P. troglodytes males and females were not

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statistically significantly, C1 FA is presumed to be similar supporting the suggestion that

0.75years might be too small of a time difference.

Mandibular canine lateral EFTs for 80% and 90% crown height are over two

years longer in G. gorilla males than females. Furthermore, based on the research done

by Schwartz and Dean (2001) it is clear that there is no overlap in enamel formation

times between G. gorilla males and females. Schwartz and Dean (2001) report that male

gorillas consistently take longer to complete canine enamel formation than females. It is

quite surprising, therefore, that only C1 BL FA in stage 1 was found to differ significantly

between males and females of G. gorilla across both stages of testing H2. Even though

C1 MD FA of G. gorilla males and females was not found to differ significantly between the sexes, the results do approach statistical significant in stage 1 of H2 (stage 1 p-value =

0.0675). An increase in sample size, particularly in the female sample, might allow for a

stronger comparison. The lack of statistical significance in stage 2 could be an artifact of

which male specimens were selected for stage 2. The sample size of G. gorilla males was

reduced to match that of females. Those males expressing greater C1 FA might have been

randomly selected out of the sample of G. gorilla males for stage 2 of H2.

P. anubis males expressed greater C1 FA than females but this difference was not

found to be statistically significant. Growth duration between male and female of this species is 0.96years at 80% crown height and 1.14 years at 90% crown height. Such a difference in growth duration might not be long enough to result in statistically different

FA estimates between males and females.

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In stage 2 of H2, four other sexually dimorphic species were found to express C1

FA that is in the expected direction of H2 but was not statistically significant between the

sexes. Of these four species, lateral EFTs are only available for M. nemestrina and C.

albifrons. At mean pk/stirae for 80% crown height, M. nemestrina males and females

differ by 1.25 years while at mean pk/stirae for 90% crown height they differ by less than

a year. C. albifrons males and females lateral EFTs at mean pk/stirae for 80% crown heights are less than a year apart. As discussed above, a difference in growth of approximately a year might not be enough to generate a statistical difference in C1 FA estimates.

It is important to note that across both stages of testing almost all the sexually dimorphic species expressed C1 FA in the expected direction in at least one C1

dimension. The results of testing H2 across two stages suggest that there may be a certain

amount of time needed between males and females for males to express significantly

greater C1 FA. It is not surprising that when males and females differ in their lateral EFTs by less than a year the resulting C1 FA estimates are not statistically significant even

when males express greater C1 FA than females. Although the WOV and ‘developmental

destabilization’ hypotheses could not be separated out through testing H2, these results

are skewed towards the WOV hypothesis. This is particularly evident in species where

sexes differ little (e.g. less than a year) in canine growth but are considered to be highly

sexually dimorphic. Such species included the Old World monkeys P. anubis and M.

nemestrina as well as the platyrrhine C. apella.

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Growth Processes

Vrijenhoek’s (1985) WOV describes a mode of growth in which structures that

grow for a longer period of time are more likely to accumulate perturbations that disrupt

the developmental system because they have a longer time frame in which to experience

perturbations brought on by stress. Size can be achieved through sex differences in

growth rates or growth duration (bimaturism) or a combination of both. Bimaturism is

connected to Vrijenhoek’s (1985) WOV since it describes a mode of growth in which

males and females grow for a different amount of time permitting the opportunity for one

sex to accumulate more perturbations during development.

Hogg (2007) suggested that platyrrhines differ from catarrhines in that they

achieve canine sexual dimorphism through a sex difference in crown formation rate

rather than bimaturism. Guatelli-Steinberg and colleagues (2009), however, found evidence for platyrrhine males and females achieving canine sexual dimorphism through differences in enamel formation times, not rates. Moreover, Guatelli-Steinberg and

colleagues (2009) found some evidence that sex differences in crown formation rates

represent a minor component to the achievement of canine crown sexual dimorphism in

Papio and species of the C. mitis group.

The combination of different modes of dimorphic growth – bimaturism and

growth rate – for achieving canine sexual dimorphism might have contributed to

comparisons between males and females of P. anubis and C. mitis not indicating a

significant difference between male and female C1 FA. However, it is difficult to make an assertion concerning if and to what extent the combination of different modes of growth

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within a single morphological structure might affect dental FA. Within the FA literature a

clear distinction between growth rate and growth duration is rarely made. For instance, the phrases ‘growth period’ (Mateos et al., 2008, p.8) or ‘shifts in developmental timing’

(Kegley and Hemingway, 2007, 47) are commonly used to describe a structure’s growth.

Even when a distinction is made, as in some studies on cervid antlers (e.g. Ditchkoff et al., 2001) and bird feathers (Swaddle and Witter, 1994), only a single mode of dimorphic growth is examined. Moreover, a structure that achieves dimorphism through a combination of both modes of growth has yet to be researched in the FA literature.

Therefore it has yet to be established within the FA literature if one mode of dimorphic growth is associated with FA more often than the other mode, or if both modes have equivalent relationships with FA.

Additionally, more research on the achievement of canine sexual dimorphism in primate species is also needed. Even though Ateles and Cebus were found to not achieve canine sexual dimorphism through sex differences in growth rates (Guatelli-Steinberg et al., 2009) that does not mean that other platyrrhines follow the same pattern. Hogg’s

(2007) analysis on a small sample of platyrrhines suggesting that canine sexual dimorphism is achieved differently in platyrrhines and catarrhines could hold true for other platyrrhine species. However, until more data are collected on the achievement of canine sexual dimorphism in a wide range of primate species it will remain unclear if some platyrrhines differ from catarrhines and if other primate species achieve canine sexual dimorphism through a combination of dimorphic growth.

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Dental Indicators of Stress: Fluctuating Asymmetry and Linear Enamel Hypoplasia

General Overview of Patterns Observed Across Primate Species

Both linear enamel hypothesis (LEH) and FA are non-specific stress indicators.

LEH, a dental defect, results from the disruption of enamel development and appears as either a sharp line on the crown or a single groove/furrow/ridge on the crown surface

(Guatelli-Steinberg and Lukacs, 1999). Similar to dental FA, once LEH has formed it serves as permanent markers of the stress experienced during development. The presence of either of these dental indicators of stress implies that the organism experienced stress during development. These indicators of stress do not convey what stress (e.g. genetic, environmental) caused the disruption of enamel or the disruption of the developmental system.

The identification of LEH in human and non-human primates is considered a major component to assessing health in both archaeological and modern populations.

Although not as widely used as LEH, dental FA has been recorded for dental collections associated with archaeological (e.g. Bollini et al., 2008; Prowse, 2010) and paleoanthropology samples (Kegley and Hemingway, 2007; Barrett et al., 2012).

Both LEH and FA are believed to be influenced by the length of the growth

period. With respect to Pongo and Gorilla, males exhibit a greater number of LEH defects on their canine relative to females (Guatelli-Steinberg et al., 2012). Males of these great apes also grow their canines for a longer period of time relative to their female counterparts (Schwartz and Dean, 2001). While the frequency of LEH defects does not differ significant between males and females of Pan (Guatelli-Steinberg et al., 2012).

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Thus, researchers (e.g. Skinner and Guatelli-Steinberg, 1997; Guatelli-Steinberg, 1998;

Guatelli-Steinberg, 2000; Guatelli-Steinberg and Skinner, 2000; Hannibal and Guatelli-

Steinberg, 2005; Newell et al., 2006; Guatelli-Steinberg et al., 2012) have argued that the length of the growth period provides an opportunity for a greater accumulation of LEH defects on the tooth crown. Within the anthropological literature, a relationship between greater LEH prevalence and elevated dental FA has been investigated by a few scholars

(e.g. Hoover et al., 2005; Martin et al., 2011). Individuals with a high prevalence of LEH are hypothesized to also express elevated dental FA relative to individuals with a low prevalence of LEH (e.g. Hoover et al., 2005; Martin et al., 2011). Even though LEH was not recorded for specimens examined in this study, it is still possible to compare the pattern of LEH prevalence observed in past studies (e.g. Guatelli-Steinberg, 1998;

Guatelli-Steinberg and Lukacs, 1998; Guatelli-Steinberg, 2000; Guatelli-Steinberg et al.,

2012; Hannibal and Guatelli-Steinberg, 2005; Newell et al., 2006; Vitzthum and

Wikander, 1988) to the pattern of dental FA estimates reported in this study.

First molar FA of the primate species examined in this study generally follow the great ape – monkey dichotomy proposed for LEH defects in non-human primates

(Skinner and Guatelli-Steinberg, 1997; Guatelli-Steinberg, 1998; Guatelli-Steinberg,

2000; Guatelli-Steinberg and Skinner, 2000). Guatelli-Steinberg (2000) found that LEH frequencies of gibbons were intermediate between monkeys and great apes and that LEH

prevalence for gibbons differed significantly from monkeys but not from the great apes.

First molar FA variation reported in Chapter 5 (see Figure 6) increases from monkeys to great apes; however, the primate species examined in Chapter 6 (see Figures 8 and 9) do

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not show a progressive of M1 FA from monkeys to great apes. Rather, M1 FA of the

gibbons, H. lar and H. hoolock, is not immediate between monkeys and great apes but

falls within the range of M1 FA observed in Old World monkey species. Maxillary first

molar FA of H. lar, not H. hoolock, does fall between the great apes and monkeys (see

Table 18), which follows the great ape – monkey dichotomy of LEH defects in primate species (Skinner and Guatelli-Steinberg, 1997; Guatelli-Steinberg, 1998; Guatelli-

Steinberg, 2000; Guatelli-Steinberg and Skinner, 2000). Canines represent a common tooth for examining LEH prevalence in primates because of their long CFTs. Within New

World monkeys, Newell and colleagues (Newell, 1998; Guatelli-Steinberg, 1998; Newell et al., 2006) found that Cebus had significantly higher LEH frequencies than other ceboid genera. Within Cebus, C. apella and C. albifrons were found to have higher frequencies of LEH relative to other Cebus species (Newell et al., 2006). Furthermore, C. apella and

C. albifrons also had similar frequencies of LEH (Newell et al., 2006).

Because C. apella and C. albifrons are assigned to different competition levels and expressed similar growth (Table 43), these species did not fit the criteria for the controlled comparisons used to test H3 and were not compared. However, their FA estimates do not differ significantly from each other (Table 45) suggesting that similar to their LEH frequencies (Newell et al., 2006). C. apella and C. albifrons express similar C1

FA estimates. This is only a tentative connection between LEH and C1 FA since it is not

clear if the Cebus specimens examined for LEH by Newell and colleagues (2006) are

included in the Cebus samples for which C1 FA were determined. To make a stronger

case for a connection between LEH and FA in Cebus, a future study should examine

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C. apella Males vs. C. apella Males C. albifrons Males C. albifrons Males Tooth & FA df FA df F‐ ratio P Dimension ‐5 ‐5 C1 BL 6.70 x10 56 4.83x10 56 1.39 0.294 C MD ‐5 57 ‐5 56 1.14 0.3151 1 3.98 x10 3.49 x10 Table 45: F-tests for C. apella and C. albifrons C1 FA

these dental indicators of stress in the same individuals.

Whether or not dental FA parallels the pattern observed in LEH prevalence

among primate species is an important question when investigating the relationship between LEH and FA. A study by Martin and colleagues (2011) is the first to test the

hypothesis that individuals with a greater prevalence of LEH also express greater dental

FA non-human primate species. Among individuals of H. lar, individuals displaying

canine LEH exhibited greater FA magnitude than those individuals for which LEH was

absent (Martin et al., 2011). Among H. lar individuals with LEH defects, those

individuals with a greater prevalence of LEH also expressed greater canine FA relative to

those individuals with a lower prevalence of LEH. The results, however, were not

statistically significant possibly due to the small sample size of H. lar (N=54 total

individuals; N = 24 without LEH; N= 29 with LEH).

Additional research is needed to determine if the tentative relationship between

LEH and FA found by Martin and colleagues (2011) is also observed between males and

females of sexually dimorphic species and between different primate species.

267

A Second Look: Dental FA in Great Apes

P. pygmaeus was not included in testing H1 due to low sample size (N < 30), this great ape is included in this discussion to further expand on the variation observed in M1

FA of the great apes. Table 46 lists the sample sizes, M1 CFTs, and M1 FA estimates for

G. gorilla, P. troglodytes, and P. pygmaeus. Table 47 contains the results of the F-tests from comparing M1 FA estimates between the three great ape species.

Results of this study do not support P. pygmaeus exhibiting a significantly greater

M1 FA than G. gorilla and P. troglodytes (Tables 46 and 47). Rather, both G. gorilla and

P. troglodytes exhibit M1 FA that significantly differs from P. pygmaeus (Table 47). The significantly lower FA estimates for M1 of P. pygmaeus relative to the other great apes in all but one dimension (M1 MD) poses an interesting question: Why are Bornean orangutans exhibiting low M1 FA estimates despite having a long duration of M1 crown formation and being under nutritional stress (Vogel et al., 2012)?

Nutritional Stress

Conklin-Brittain and colleagues (2001) suggest that P. pygmaeus might not fit the fallback food paradigm of other apes. Rather, P. pygmaeus has learned to cope with food shortages through other means (Knott, 1999; Conklin-Brittian et al., 2001), such as relying on its own body fat (Knott, 1999) and moving between habitats (Tilson et al.,

1993). Even though P. pygmaeus is experiencing great nutritional stress (e.g. Vogel et al.,

2012), it appears that this form of stress has not impacted first molar FA. The movement around habitats might be an adequate way to reduce nutritional stress during most food

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Crown Sample SizesFormation Maxillary Mandibular Time (yr)*

1 1 1 1 Species M BL M MD M CA M1 BL M1 MD M1 CA M M1 BL MD CA BL MD CA

Pan 72 74 69 69 72 68 2.31 2.40 3.45x10‐4 2.27x10‐4 5.78x10‐4 4.68x10‐4 6.50x10‐4 9.94x10‐4 troglodytes Gorilla gorilla 143 145 143 144 142 142 2.59 2.81 1.68x10‐4 1.85x10‐4 2.59x10‐4 1.35x10‐4 2.38x10‐4 6.81x10‐4 Pongo 20 20 17 20 20 20 2.96 3.16 1.02x10‐5 2.02x10‐5 1.92x10‐5 5.62x10‐5 6.13x10‐4 5.31x10‐5 pygmaeus

269 Table 46: First Molar Crown Formation Times, Sample Sizes, and FA Estimates *Information for first molar crown formation times were taken from the following sources: Smith and colleagues (2007) and Kelley and Schwartz (2010)

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P. G. gorilla vs. P. G. gorilla vs. P. P. troglodytes P. pygmaeus G. gorilla troglodytes troglodytes pygmaues vs. P. pgymaeus Tooth & df df df F ‐ratio PF‐ratio PF‐ratio P Dimension M1 BL 142 71 18 2.05 0.0002 16.47 0.0001 33.82 0.0001 M1 MD 142 73 19 1.23 0.1447 9.16 0.0001 11.24 0.0001 M1 Crown Area 142 71 15 2.23 0.0001 13.49 0.0001 30.10 0.0001

M1 BL 142 67 19 3.46 0.0001 2.40 0.0150 8.33 0.0001

270 M1 MD 138 68 16 2.73 0.0001 2.58 0.0164 1.06 0.4742 M Crown Area 103 67 19 1.46 0.0415 12.82 0.0001 18.72 0.0001 1 Table 47. F-test for First Molar FA of Great Apes

251

shortages while also relying on their own body fat during periods of extreme low fruit

availability (Tilson et al., 1993; Knott, 1999). Such measures might offset developmental

instability permitting the developmental system to recover from a developmental

disruption prior to developmental noise becoming present in the system (see Figure 2a).

Even though it is possible that P. pygmaeus has an effective way to navigate food

shortages in comparison to the other great apes, the first molar sample size of P.

pygmaeus used in this dissertation is below the minimum requirement of N=30 (Table

9d). Such a small sample size, the resulting dental FA may not be representative of the

species. Until a greater sample size is obtained for P. pygmaeus this discussion must be viewed as tentative.

Parasites and FA

Parasites have been identified as a factor that has either a direct or indirect relationship with FA. Research on the relationship between parasites and elevated FA estimates lends support to both relationships (e.g. Polak, 1993; Bonn et al., 1996; Folstad et al., 1996; Moller, 1996; Thomas et al., 1998; Alibert et al., 2002). A greater body of

research, however, lends support to parasites representing a form of stress that directly

results in the presence of developmental instability and ultimately an increase in

developmental noise (e.g. Polak, 1993; Bonn et al., 1996; Folstad et al., 1996). If this is

the case, developmental instability of the host is directly related to parasite load and/or

parasite virulence (Polak, 1993; Agnew and Koella, 1997; Thomas et al., 1998). In

addition to the explanation provided above regarding nutritional stress in great apes,

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parasite load represents a second explanation for the unpredicted results of M1 FA observed among the great apes (Table 9d).

Nunn and colleagues (2003) identified host population density as a key

determinant of parasite spread within a species. Furthermore, body mass, diet, and social

contact were all found to be factors related to parasite prevalence (Nunn et al., 2003).

Unlike P. troglodytes and G. gorilla, P. pygmaeus exhibits a solitary and arboreal

lifestyle, which greatly decreases the amount of social contact between individuals

(MacKinnon, 1974; Clutton-Brock and Harvey, 1977). Due to this lifestyle, the risk of

parasite infection decreases relative to chimpanzees and gorillas because P. pygmaeus is

less likely to encounter parasites through ground contact (e.g. vegetation) and/or social

contact. Freeman and colleagues (2004) discuss how increased population densities of G.

gorilla aids in the transmission of parasites because there is a greater chance of

encountering another individual. Even though G. gorilla exhibits a low parasite level

(Freeman et al., 2004), it still appears that their social contact is continuing to facilitate

transmission in a way that is not observed in P. pygmaeus. Similar circumstances are

present for P. troglodytes. Studies on parasites in P. troglodytes populations have

indicated a large number of different parasite species using P. troglodytes as a host (e.g.

Goodall, 1968; McGrew et al., 1989; Huffman et al., 1997; Ashford et al., 2000).

Parasite infection can cause a variety of disease and health problems in a host

resulting in stress upon the host’s developmental system. If parasitism represents a

stressor capable of destabilizing the development of its host, it is possible that stress

brought on by disease through parasites explains the results of M1 FA among these three

272

great ape species. The low M1 FA estimates observed in P. pygmaeus therefore may

imply that this species did not experience as much disease stress initiated by parasites

during development relative to G. gorilla and P. troglodytes. First molar FA estimates indicate that P. troglodytes experienced greater stress during development. Such high M1

FA estimates in P. troglodytes might have been directly brought on by parasitic infections. Alternatively, the developmental system of P. troglodytes may have been compromised due to disease stress, predisposing this species to being more sensitive to developmental perturbations relative to G. gorilla and P. pygmaeus. The results reported here for P. pygmaeus are similar to those of Frederick and Gallup (2007). These authors found that P. pygmaeus exhibited the lowest dental FA among the great apes. Low pathogen virulence is suggested as a possible reason for why dental FA of P. pygmaeus is low compared to other great ape species. One drawback to the study by Frederick and

Gallup (2007) is that it is unclear which tooth types were used to calculate dental FA.

Therefore it is unclear if Frederick and Gallup (2007) included primate first molars in their determination of dental FA. Nevertheless, the similar finding regarding P. pygmaeus dental FA suggests that the results obtained here accurately reflect FA in this species.

Limitations of Comparisons

Limitations in the analysis are associated with the growth data available for non-

human primate species. For H1, M1 CFTs are only available for a few non-human

primate species. H2 and H3 were mainly limited by the data available on C1 lateral EFTs.

Testing of each hypothesis was further constrained by sample size, which ultimately was

273 influenced by the number of specimens available in museum collections and further compounded by wear, breakage, or other forms of damage to the dentition that excluded one tooth dimension, a single tooth, or an entire specimen from the analysis.

To overcome these limitations, and to further expand our knowledge on the extent to which growth duration influences FA expression, a greater sampling of CFTs and lateral EFTs on primates is needed. For instance, C1 lateral EFTs are only available for a limited number of platyrrhines while first molar CFTs was available only for a single platyrrhine species, A. geoffroyi. Expanding our knowledge of dental growth will permit more comparisons to be conducted among and between primate species.

Conclusion

This dissertation came to the following conclusions about the association between growth duration and FA:

1. Of the 10 predictions tested across two stages of H1a, six predictions were upheld

lending support to WOV hypothesis. Of the four predications not upheld, two are

associated with P. troglodytes (see point 3 below). The other two predictions

focused on the placement of P. anubis. Originally, P. anubis’ M1 FA was

predicted to fall between M1 FA of H. lar and the great apes (e.g. P. troglodytes

and G. gorilla). This finding was not consistent among M1 dimensions. It is

possible that the similarity in M1 CFTs among P. anubis and H. lar influenced

their FA estimates.

274

2. In both H1a and H1b, M1 of P. troglodytes is consistently and significantly higher

than M1 FA of other primate species. The results of M1 FA for P. troglodytes are

much higher than expected under the WOV hypothesis. In other words, FA

differences between P. troglodytes and monkeys are not proportional to their M1

CFTs or LH schedules.

3. M1 FA results from H1b argue against a broad phylogenetic effect because first

molar FA of Hylobates is more similar to M1 FA of Old World monkeys than to

great apes.

4. For M1 80.89% of the observed variation in M1 FA can be explained by age at

weaning while 82.94% of the observed variation in M1 FA can be explain by age

at weaning. The results of these linear regressions suggest that developmental

timing and M1 FA are associated.

5. Males of sexually dimorphic primate species expressed greater C1 FA than

females; however, many of these differences were not found to be significantly

different. Yet, the results are in the direction predicted by H2. The lack of

statistical significance among these comparisons might be due to the length of

developmental timing between the sexes or the potential of selection acting on

female canines.

6. Generally, males and females of the sexually monomorphic gibbons express

similar C1 FA. These results support H2.

7. Linear regressions indicate that C1 FA is strongly associated with C1 lateral EFTs

but not with competition levels or canine dimorphism.

275

8. Great apes express significantly greater C1 FA than the monkeys there were

compared to. The difference in growth between the great apes and the monkeys

they are compared to is at least 4 years. The results of these controlled

comparisons, however, might be a consequence of other biological similarities

between G. gorilla and P. troglodytes, which are closely biologically related

African apes. The mechanisms to effectively buffer developmental perturbations

might not be as effective in great apes as those possessed by monkeys. However,

the results of the controlled comparison including G. gorilla and P. troglodytes

are in direct opposition to ‘developmental destabilization’ hypothesis.

9. With respect to C1, a difference in developmental timing of at least two-years

appears to be the threshold in which significantly different FA estimates were

found. In species with growth durations that differed by less than two years, a

significant difference in C1 FA was not generally found.

10. Besides one comparison (e.g. C. apella and P. anubis), ‘developmental

destabilization’ was found to be a poor predictor of C1 FA.

11. Differences in growth duration between species might be offset by other factors,

which either increase or decrease sensitivity to developmental perturbations.

Contribution of this Dissertation to Understanding Dental FA Patterns

276

evaluated for FA, including structures that are and are not sexually selected. Information on stress experienced during development has been inferred from FA estimates on dental, cranial and post-cranial material. Because of the frequency at which FA estimates are used to infer information about quality, fitness, and stress experienced during development, it is important to understand what underlying variables might affect the expression of FA in a morphological structure This disseration contributes to our current understanding of FA in both a non-sexually selected and a sexually-selected structure.

This dissertation further contributes to our understanding because it represents the first study to attempt to:

1. Include platyrrhine species in dental FA analyses.

2. Examine dental dimensions not influenced by use-related wear.

3. Characterize the variation of M1 FA observed across several primate taxa.

4. Explore the contribution of M1 CFTs to variation in FA between primate species.

5. Explore the contribution of C1 lateral EFTs to variation observed in FA among

males and females of a species as well as among primate species.

6. Test specific hypotheses regarding the association between FA and sexual

selection and FA and developmental timing.

The frequency at which FA estimates are used to infer differnces in quality,

fitness, and stress experienced during development among species and populations across

different disciplines calls for a better understanding of the underlying variables that

contribute to FA expression. The use of FA as an indicator of stress is complicated by the

277

evidence suggesting that longer periods of developmental timing allow for a greater

accumulation of developemntal pertubations. Thus, evelated FA might not be a result of

greater stress, less quality, or lowered fitness, but rather a consequence of a longer

developmental period. To fully explore the extent to which growth duration is associated

with FA a greater understanding of dental growth in non-human primates is needed. Once more information on both CFTs and lateral EFTs are known, greater species sample sizes

can be applied to the hypotheses addressed here. Until then, dental metric measuremetns

that can be used to calcuate dental FA should collected from non-human primate

specimens. In addition to museum samples, reserachers should collect dental dimensions

from living primates in order to investigate if other factors such as nutrition and parasite

load are contributing to dental FA within and among species.

The testing of this dissertation’s hypotheses not only provided a greater

understanding of the effects of growth duration on developmental instability, but also

produced a more detailed picture of dental FA variation in primate species.

278

REFERENCES

Agnew P, Koella JC. 1997. Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proc R Soc Lond B 264: 9-15.

Aitken M, Anderson D, Francis B, Hinde J. 1989. Statistical Modelling in GLIM. Oxford: Oxford University Press.

Alfaro JWL, Silva J, Rylands AB. 2012. How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. Amer J Primat 74: 273-286.

Alibert P, Bollache L, Corberant D, Guesdon V, Cezilly F. 2002. Parasitic infection and developmental stability: Fluctuating asymmetry in Gammarus pulex infected with two acanthocephalan species. Journal of Parasitology 88: 47-54.

Ames LJ, Felley JD, Smith MH. 1979. Amounts of asymmetry in centrarchid fish inhabiting heated and nonheated reservoirs. Transactions of the American Fisheries Society 108: 489-495.

Angelopoulou MV, Vlachou V, Halazonetis DJ. 2009. Fluctuating molar asymmetry in relation to environmental radioactivity. Archives of Oral Biology 54: 666-670.

Arendt JD. 1997. Adaptive intrinsic growth rates: an integration across taxa. The Quarterly Review of Biology 72(2): 149-177.

Arendt JD. 2003. Reduced burst speed is a cost of rapid growth in anuran tadpoles: problems of autocorrelation and inferences about growth rates. Funct Ecol 17: 328-334.

Ashford RW, Reid GDF, Wrangham RW. 2000. Intestinal parasites of the chimpanzee Pan troglodytes, in Kibale Forest, Uganda. Ann. Trop. Med. Parasit. 94: 173–179.

Auffray JC, Debat V, Alibert P. 1999. Shape asymmetry and developmental stability. In: Chaplain MAJ, Singh GD, McLachlan JC, editors. On Growth and Form: Spatio- temporal Pattern Formation in Biology. New York: John Wiley & Sons. p 309-324.

Balmford A, Jones IL, Thomas ALR. 1993. On Avian Asymmetry: Evidence of Natural Selection for Symmetrical Tails and Wings on Birds. Proceedings: Biological Sciences 252: 245-251.

279

Barrett CK, Guatelli-Steinberg D, Sciulli PW. 2012. Revisiting dental fluctuating asymmetry in neandertals and modern humans. Am J Phys Anthrol 149: 193-204.

Bartos L, Bahbouh R, Vach M. 2007. Repeatability of size and fluctuating asymmetry of antler characteristics in red deer (Cervus elaphus) during ontogeny. Bio J Linn Soc 91: 215-226.

Basabose AK. 2002. Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology 58: 1-21.

Bateman PW. 2000. The influence of weapon asymmetry on male-male competition success in a sexually dimorphic insect, the African King cricket Libanasisdus vittatus (Orthoptera: Anostostomatidae). J Insect Behav 13: 157-163.

Beardmore JA. 1960. Developmental stability in constant and fluctuating temperatures. Heredity 14: 411-422.

Ben-David Y, Hershkovitz I, Rubin D, Moscona D, Ring B. 1992. Inbreeding effects on tooth size, eruption age, and dental directional and fluctuating asymmetry among South Sinai Bedouins. In: Smith P, Tchernov E, editors. Structure, function and evolution of teeth. London: Freund Publishing House, Ltd. P 361-389.

Beynon AD, Dean MC, Reid SJ. 1991. Histological study on the chronology of the developing dentition in gorilla and orangutan. Am J Phys Anthrol 86: 189-203.

Bjorksten T, Fowler K, Pomiankowski A. 2000. What does sexual trait FA tell us about stress? TREE 15(4): 163-166.

Bjorklund M, Merila J. 1997. Why some measures of fluctuating asymmetry are so sensitive to measurement error. Ann Zool Fenn 34:133-137.

Blomquist GE, Kowalewski MM, Leigh SR (2009) Demographic and morphological perspectives on life history evolution and conservation of new world monkeys. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB, editors. South American primates: comparative perspectives in the study of behavior, ecology, and conservation. New York: Springer. p 117–138

Bogin B. 1997. Evolutionary hypotheses for human childhood. Yearb. Phys. Anthropol. 40:63-89.

Bogin B. 2001. The growth of humanity. New York: Wiley-Liss.

280

Bollini GA, Rodriquez-Florez CD, Colantonio SE. 2009. Bilateral asymmetry in permanent dentition of 13 pre-conquest samples from Argentina (South America). HOMO – Journal of Comparative Human Biology 60: 127-137.

Bonn A, Gasse M, Rolff J, Martens A. 1996. Increased fluctuating asymmetry in the damselfly Coenagrion puella is correlated with ectoparasitic water mites: implications for fluctuating asymmetry theory. Oecologia 108: 596-598.

Bowyer RT, Stewart KM, Kie JG, Casaway WC. 2001. Fluctuating Asymmetry in Antlers of Alaskan Moose: Size Matters. Journal of Mammalogy 82(3): 814-824.

Brana F, Xiang J. 2000. Influence of Incubation Temperature on Morphology, Locomotor Performance, and Early Growth of Hatching Wall Lizards (Podarcis muralis). Journal of Experimental Zoology 286: 422-433.

Brandon-Jones D, Eudey A, Geissmann T, Groves CP, Melnick DJ, Morales JC, Shekelle M, Steart CB. 2004. Asian primate classification. Int J Primatol 25: 97-164.

Bubenik GA, Bubenik AB. 1990. Horns, pronghorns, and antlers: evolution, morphology, physiology, and social significance. New York: Springer.

Carbonell R, Telleria JL. 1998. Female choice for parasite-free male satin bowerbirds and the evolution of bright male plumage. Behavioral Ecology and Sociobiology 25: 445-454.

Carchini G, Chiarotti F, DiDomenico M, Paganotti G. 2000. Fluctuating asymmetry, size and mating success in males of Ischnura elegans (Vander Linden) (Odonata: Coenagrionidae). Animal Behavior 59: 177-182.

Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, McDowell LR. 2004. Predicting folivorous primate abundance: Validation of a nutritional model. Am. J. Primatol. 62: 55–69.

Chapman JW, Goulson D. 2000. Environmental versus genetic influences on fluctuating asymmetry in the house fly, Musca domestica. Biol J Linn Soc 70: 403-413.

Charnov EL. 1991. Evolution of life history variation among female mammals. Proc Natl Acad Sci 88: 1134-1137.

Charnov EL, Berrigan D. 1993. Why do female primates have such long lifespands and so few babies? or Life in the slow lane. Evol Anthro 1: 191-194.

281

Clarke GM. 1992. Fluctuating asymmetry: a technique for measuring developmental stress of genetic and environmental origin. Acta Zoologica Fennica 191: 31-35.

Clarke GM. 1993. The genetic basis for developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica 89: 15-23.

Clarke GM. 1995. Relationships between developmental stability and fitess: Application for Conservation Biology. Conservation Biology 9(1): 18-24.

Clarke GM. 1998. Developmental Stability and Fitness: The Evidence Is Not Quite So Clear. The American Naturalist 152(5): 762-766.

Clarke GM. 2003. Developmental Stability-Fitness Relationships in Animals: Some Theoretical Considerations. In: Polak M, editor. Developmental Instability: Causes and Consequences. New York: Oxford University Press. p 213-230.

Clarke GM, Barnd GW, Whitten MJ. 1986. Fluctuating asymmetry: A technique for measuring developmental stress caused by inbreeding. J Aust Biol Sci 39: 145-153.

Clarke GM, McKenzie LJ. 1992. Fluctuating asymmetry as a quality control indicator for insect mass rearing process. Journal of Economical Entomology 85: 2045-2050.

Clutton-Brock TH, Harvey PH. 1977. Primate ecology and social organization. J Zool 183: 1–39.

Conklin-Brittain NL, Knott CD, Wrangham RW. 2001. The feeding ecology of apes. In Conference Proceedings. The Apes: Challenges for the 21st Century. Brookfield: Brookfield Zoo. p 167–174

Cordell HJ. 2002. Epistasis: What it means, what it doesn’t mean, and statistical methods to detect it in humans. Human Molecular Genetics 11: 2463-2468.

Corruccini RS, Handler JS, Mutaw RJ, Lange FW. 1982. Osteology of a Slave Burial Population From Barbados, West Indies. Am J Phys Anthrol 59: 443-459.

Cuthill IC, Swaddle JP, Witter MS. 1993. Fluctuating asymmetry. Nature, Lond 363: 217-218.

David P, Hingle A, Fowler K, Pomiankowski A. 1999. Measurement bias and fluctuating asymmetry estimates. Anim Behav 57: 251-253.

David P, Hingle A, Greig D, Rutherford A, Pomiankowski A, Fowler K. 1998. Male sexual ornament size but not asymmetry reflects condition in stalk-eyed flies. Proc R Soc Lond B Biol Sci 265: 2211-2216.

282

Dean MC. 2006. Tooth microstructure tracks the pace of human life-history evolution. Proc R Soc B 273: 2799-2808.

Dean MC, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414: 628-631.

DeLeon VB. 2007. Fluctuating asymmetry and Stress in a Medieval Nubian Population. Am J Phys Anthrol 132: 520-534.

Dirks W. 1998. Histological reconstruction of dental development and age at death in a juvenile gibbon (Hylobates lar). J Hum Evol 35:411–425.

Dirks W. 2003. Effect of diet on dental development in four species of catarrhine primates. Am J Primatol 61: 29-40.

Dirks W, Bowman. 2007. Life history theory and dental development in four species of catarrhines primates. J Hum Evol 53:309-320.

Dirks W, Reid DJ, Jolly CJ, Phillips-Conroy JE, Brett FL. 2002. Out of the mouth of baboons: stress, life history, and dental development in the Awash National Park hybrid zone, Ethiopia. Am J Phys Anthrol 118: 239-252.

Ditchkoff SS, defreeze RL. 2010. Assessing fluctuating asymmetry of white-tailed deer antlers in a three-dimensional context. Journal of Mammalogy 9(1): 27-27.

Ditchkoff SS, Lochmiller RL, Masters RE, Starry WR, Leslie DM. 2001. Does fluctuating asymmetry of antlers in white-tailed deer (Odocoileus viginianus) follow patterns predicted for sexually selected traits? Proceedings of the Royal Society of London, B. Biological Sciences 268: 891-898.

Dongen SV. 2006. Fluctuating asymmetry and developmental instability in evolutionary biology: past, present, and future. Journal Compilation 19:1727-1743.

Dongen SV, Cornille R, Lens L. 2009. Sex and asymmetry in humans: what is the role of developmental instability? Journal of Evolutionary Biology 22: 612-622.

Doran DM, McNeilage A, Greer D, Bocian C, Mehlman P, Shah N. 2002. Western lowland gorilla diet and resource availability: new evidence, cross-site comparisons, and reflections on indirect sampling methods. Am J Primatol 58: 91–116.

Doyle WJ, Johnson O. 1977. On the meaning of increased fluctuating dental asymmetry: a cross population study. Am J Phys Anthrol 46: 123-127.

283

Emlen JM, Freeman DC, Graham JH. 1993. Nonlinear growth dynamics and the origin of fluctuating asymmetry. Genetica 89:77-96.

Evans MR. 1993. Fluctuating asymmetry and long tails: The mechanical effects of asymmetry may Act to enforce honest advertisement. Proceedings: Biological Sciences 253: 205-209.

Evans MR, Hatchwell BJ. 1993. New slants on ornament asymmetry. Proc R Soc Lond B Biol Sci 251: 171-177.

Evans MR, Marshall M. 1996. Developmental instability in Brassica campestris (Cruciferae): Fluctuating asymmetry of foliar and floral traits. J Evol Biol 9:717-736.

Evans MR, Martins TLF, Haley MP. 1995. Inter and intra-sexual patterns of fluctuating asymmetry in the red-billed streamertail: should symmetry always increase with ornament size? Behav Ecol 37: 15-27.

Falk D, Hidebolt C, Cheverud J, Vannier M, Helmkamp RC, Konigsberg L. 1990. Cortical asymmetries in frontal lobes of Rhesus monkeys (Macaca mulatta). Brain Research 512: 40-45.

Falk D, Pyne L, Helmkamp RC, DeRousseau CJ. 1988. Directional asymmetry in the forelimb of Macaca mulatta. Am J Phys Anthrol 77: 1-6.

Fashing PJ. 2001. Feeding ecology of guerezas in the Kakamega Forest, Kenya: The importance of Moraceae fruit in their diet. Int J Primatol 22: 579–609.

Fashing P J. 2006. African colobine monkeys: Patterns of between-group interaction. In Campbell, C., Fuentes A, MacKinnon K, Panger M, and Bearder S, editors. Primates in Perspective. Oxford: Oxford University Press. p 201–224.

Fashing PJ, Mulindahabi F, Gakima J-B, Masozera M, Mununura I, Plumptre AJ, Nguyen N. 2007. Activity and Ranging Patterns of Colobus angolensis ruwenzorii in Nyungwe Forest, Rwanda: Possible Costs of Large Group Size. Int J Primatol 28: 529- 550.

Felley J. 1980. Analysis of morphology and asymmetry in bluegill sunfish (Lepomis macrochirus) in the Southeastern United States. Copeia 1980:18-29.

Fenster CB, Galloway LF. 1997. Developmental homeostasis and floral form: evolutionary consequences and genetic basis. Int J Plant Sci 158 (Suppl) S212-S130.

284

Fields SJ, Spiers M, Hershokovitz I, Livshits G. 1995. Reliability of reliability coefficients in the estimation of asymmetry. Am J Phys Anthrol 96: 83-87.

Fiske P, Kalas JA, Saether SA. 1994. Correlates of male mating success in the lekking great snipe (Gallingo media): results from a four year study. Behav Ecol 5: 210-218.

Fox EA, van Schaik CP, Sitompul A, Wright DN. 2004. Intra- and Interpopulational Differences in Orangutan (Pongo pygmaeus) Activity and Diet: Implications for the Invention of Tool Use. Am J Phys Anthrol 125: 162-174.

Fox W, Gordon C, Fox M. 1961. Morphological effects of low temperatures during embryonic development of the garter snake, Thamnophis elegans. Zoologica 46: 57-71.

Fragaszy DM, Visalberghi E, Fedigan LM. 2004. The Complete Capuchin: The Biology of the Genus Cebus. United Kingdom: Cambridge University Press.

Frederick MJ, Gallup GG. 2007. Fluctuating Denatl Asymmetry in Great Apes, Fossil Hominins, and Modern Humans: Implications for Changing Stressors during Human Evolution. Acta Psychologica Sinica 39(3): 489-494.

Freeman DC, Brown ML, Duda JJ, Emlen JM, Graham JH, Krzysik A, Balbach H, Kovacic DA, Zak JC. 2004. Developmental instability in Rhus copallinum L.: multiple stressors, years, and responses. Int J Plant Sci 165: 53–63.

Folstad I, Arneberg P, Karter AJ. 1996. Antlers and parasites. Oecologia 105: 556-558.

Garn SM, Lewis AB, Swindler DR, Kerewsky RS. 1967. Genetic Control of Sexual Dimorphism in Tooth Size. J Dent Res 963-973.

Geissmann T. 2002. Taxonomy and evolution of gibbons. In Soligo C, Anzenberger G, Martin RD, editors. Anthropology and Primatology into the Third Millennium: The Centenary Congress of the Z¨urich Anthropological Institute (Evolutionary Anthropology Vol. 11, Suppl. 1). New York: Wiley-Liss, New York. p 28–31.

Gibson G, Wagner G. 2000. Canalization in evolutionary genetics: a stabilizing theory? BioEssays 22: 372-380.

Gippoliti S. 2001. Notes on the Taxonomy of Macaca nemestrain leonine Blyth, 1983 (Primates: Cercopithecidae). Hystrix It J Mamm 12: 51-54.

Goddard KW, Lawes MJ. 2000. Ornament size and symmetry: is the tail a reliable signal of male quality in the red-colored widowbird? The Auk 117(2):366-372.

285

Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. 2001. Teeth, Brains, and Primate Life Histories. Complete Capuchin 114: 192-214.

Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. 2003. Dental development and primate life histories. In: Kappeler PM, Pereira ME, editors. Primate Life Histories and Socioecology. Chicago: University of Chicago Press. p 177-203.

Gonzalez-Guzman LI, Mehlman DW. 2000. Developmental stability across the breeding distribution of the scissor-tailed flycatcher (Tyrannus forficatus). Ecology Letters 4: 444- 452.

Goodman AH, Armelagos GJ. 1989. Infant and Childhood Morbidity and Mortality Risks in Archaeological Populations. World Archaeology 1(2):225-243.

Goodman AH, Rose JC. 1990. Assessment of Systemic Physiological Perturbations From Dental Enamel Hypoplasia and Associated Histological Structures. Yearbook of Physical Anthropology 33:59-110.

Goodall J. 1986. The chimpanzees of Gombe. Cambridge, MA: Belknap Press.

Goulson D, Bristow L, Elderfield E, Brinklow K, Perry-Jones B, Chapman JW. 1999. Size, symmetry, and sexual selection in the house fly, Musca domestica. Evolution 53: 527-534.

Graham JH, Freeman DC, Emlen JM. 1993. Antisymmetry, directional selection, and dynamic morphogenesis. Genetica 89 121-137.

Graham JB, Emel JM, Freeman DC, Leamy LJ, Kieser JA. 1998. Directional asymmetry and the measurement of developmental instability. Biol J Linn Soc 64: 1-16.

Gray PB, Marlowe F. 2002. Fluctuating asymmetry of a foraging population: the Hadza of Tanzania. Annuals of Human Biology 29: 495-501.

Greene DL. 1984. Fluctuating dental asymmetry and measurement error. Am J Phys Anthrol 65:283-289.

Greenfield LO. 1992. Origin of the human canine: a new solution to an old enigma. Yearbook of Physical Anthropology 84:17-34.

Greenfield LO, Washburn A. 1991. Polymorphic aspects of male anthropoid canines. Am J Phys Anthrol 84: 17-34.

Groves CP. 2001. Primate Taxonomy. Washington and London: Smithsonian Institution Press.

286

Groves CP. 2005. Order Primates. In: Wilson DE, Reeder DM, editors. Mammal Species of the World. A Taxonomic and Geographic Reference, Third Edition. Baltimore, Maryland: Johns Hopkins University Press. p 111-184.

Groves CP. 2007. The endemic Uganda Mangabey, Lophocebus ugandae, and othermembers of the albigena-group (Lophocebus). Primate Conserv 22:69-74.

Grubb P. 2006. Geospecies and Superspecies in the African Primate Fauna. Primate Conservation 20: 75-78.

Grubb P, Butynski TM, Oates JF, Bearder SK, Disotell TR, Groves CP, Struhsaker T. 2003. Assessment of the Diversity of African Primates. International Journal of Primatology 24: 1301-1357.

Guatelli-Steinberg D. 1998. Prevalence and etiology of linear enamel hypoplasia in non- human primates. Ph.D. dissertation, University of Oregon, Eugene, OR.

Guatelli-Steinberg D. 2000. Linear enamel hypoplasia in gibbons (Hylobates lar carpenteri). Am J Phys Anthrol 112: 395–410.

Guatelli-Steinberg D. 2001. What can developmental defects of enamel reveal about physiological stress in nonhuman primates? Evol Anthro 10: 138-151.

Guatelli-Steinberg D. 2007. ‘Growing Pains’: Incremental Growth Layers in the Dental Enamel of Human Ancestors. In: Larsen CS, editor. A Companion to Biological Anthropology. United Kingdom: Wiley-Blackwell. p 485-500.

Guatelli-Steinberg D, Ferrell R, Spence J, Talabere T, Hubbard H, Schmidt S. 2009. Sex differences in lateral enamel formation in anthropoid mandibular canines. Am J Phys Anthrol 140:216-233.

Guatelli-Steinberg D, Ferrell RJ, Spence J. 2012. Linear enamel hypoplasia as an indicator of physiological stress in great apes: Reviewing the evidence in light of enamel growth variation. Am J Phys Anthrol 148: 191-204.

Guatelli-Steinberg D, Lukacs JR. 1998. Preferential expression of linear enamel hypoplasia on the sectorial premolars of rhesus monkeys (Macaca mulatta). Am J Phys Anthrol 107:179–186.

Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Natl Acad Sci 102: 14197-14202.

287

Guatelli-Steinberg D, Reid DJ. 2008. What molars contribute to an emerging understanding of lateral enamel formation in Neandertals vs. modern humans. Journal of Human Evolution 54: 236-250.

Guatelli-Steinberg D, Sciulli P, Edgar H. 2006. Dental fluctuating asymmetry in the Gullah: Tests of hypotheses regarding developmental stability in deciduous vs. permanent and male vs. female teeth. Am J Phys Anthrol 129: 427-434.

Guatelli-Steinberg D, Skinner M. 2000. Prevalence and Etiology of Linear Enamel Hypoplasia in Monkeys and Apes from Asia and Africa. Folia Primatologica 71: 115- 132.

Hallgrimsson B. 1993. Fluctuating asymmetry in Macaca fascicularis: A study of etiology of developmental noise. International Journal of Primatology 14(3):421-443.

Hallgrimsson B. 1995. Fluctuating Asymmetry and Maturational Spain in Mammals: Implications for the Evolution of Prolonged Development in Primates, Ph.D. thesis, University of Chicago.

Hallgrimsson B. 1999. Ontogenetic patterning of fluctuating asymmetry in Rhesus Macaques and Humans: Evolutionary and Developmental Implications. International Journal of Primatology 20(1):121-151.

Hallgrímsson B, Willmore K, Hall BK. 2002. Canalization, developmental stability, and morphological integration in primate limbs. Am J Phys Anthrol (Yearbook) 119(S35):131–158.

Hamdoun A, Epel D. 2007. Embryo stability and vulnerability in an always changing world. Proceedings of the National Academy of Sciences of the United States of America, 104, 1745–1750.

Hamilton WD, Zuk M. 1982. Heritable True Fitness and Bright Birds: A Role for Parasites? Science 218(4570): 384-387.

Hannibal DL, Guatelli-Steinberg D. 2005. Linear enamel hypoplasia in the great apes: analysis by genus and locality. Am J Phys Anthrol 127: 13–25.

Harris EF, Nweeia MT. 1980. Dental Asymmetry as a Measure of Environmental Stress in the Ticuna Indians of Colombia. Am J Phys Anthrol 53: 133-142.

Harris TR. 2005. Roaring, Intergroup Aggression, and Feeding Competition in Black and White Colobus Monkeys (Colobus guereza) at Kanyawara, Kibale National Park, Uganda. Ph.D. thesis, Yale University, New Haven.

288

Harrison ME. 2009. Orang-utan feeding behaviour in Sabangau, Central Kalimantan. PhD thesis. Cambridge: University of Cambridge.

Harrison ME, Marshall AJ. 2011. Strategies for the Use of Fallback Foods in Apes. Int J Primatol 32: 531-565.

Harvey PH, Clutton-Brock TH. 1985. Life History Variation in Primates. Evolution 39: 559-581.

Harvey PH, Kavanagh M. 1978. Sexual dimorphism in primate teeth. J Zool Lond 186:475-485.

Hauser MD, Akre K. 2001. Aymmetries in the timing of facial and vocal expressions by rhesus monkeys: implications for hemispheric specialization. Animal Behavior 61; 391- 400.

Hayes VJ, Freedman L, Oxnard CE. 1990. The taxonomy of savannah baboons: An odontomorphometric analysis. American Journal of Primatology 22: 171-190.

Hershkovitz P. 1949. Mammals Of northern Colombia. Preliminary report no. 4: Monkeys (Primates), with taxonomic revisions of some forms. Proc. U.S. Natn. Mus. 98: 323–427.

Hershkovtiz I, Livshits G, Moskona D, Arensburg B, Kobyliansky E. 1993. Variables Affecting Dental Fluctuating Asymmetry in Human Isolates. Am J Phys Anthrol 91:349- 365.

Hillson S. 1996. Dental Anthropology. Cambridge: Cambridge University Press.

Hillon S, Bond S. 1997. Relationship of Enamel Hypoplasia to the Pattern of Tooth Crown Growth: A Discussion. Am J Phys Anthrol 104: 89-103.

Hogg RT. 2007. Canine dimorphism, dental growth, and the evolution of anthropoid mating systems: the platyrrhine angle. Am J Phys Anthrol 132(Suppl 44): 130.

Hogg RT. 2008. Patterns underlying Retzius period variation in primates and mammals. Am J Phys Anthrol Suppl 135 (Suppl 46):119.

Hogg RT, Walker RS. 2011. Life-History Correlates of Enamel Microstructure in Cedidae (Platyrrhine, Primates). Anatomical Record 294: 2193-2206.

Hoover KC, Corruccini RS, Bondioli L, Macchiarelli R. 2005. Exploring the relationship between hypoplasia and odontometric asymmetry in Isola Sacra, an imperial roman necropolis. Am J Phys Anthrol 17: 752-764.

289

Hopkins W D, Washburn DA, Berke L, Williams M. (1992). Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta ): A dissociation between hand preference and performance. Journal of Comparative Psychology, 106, 392–397.

Hosken DJ. 2001. Size and fluctuating asymmetry in sexually selected traits. Animal Behavior 62: 603-605.

Hosken DJ, Blanckenhorn WU, Ward PI. 2000. Developmental stability in yellow dung flies (Scathophaga stercoraria): fluctuating asymmetry, heterozygosity and environmental stress. J Evolution Biol 13: 919-926.

Huffman MA, Gotoh S, Turner LA, Hamai M, Yoshida K. 1997. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38:111–125.

Humphrey LT. 2008. Enamel traces of early lifetime events. In: Schultkowski H, editor. Between biology and culture. Cambridge: Cambridge University Press. p 186–206.

Hunt J, Simmons LW. 1997. Patterns of fluctuating asymmetry in beetle horns: an experimental examination of the honest signaling hypothesis. Behav Ecol Sociobiol 41: 109-114.

Hutchinson DW, JM Cheverud. 1995. Fluctuating Asymmetry in Tamarin (Saguinus) Cranial Morphology: Intra-and Interspecific Comparisons between Taxa with Varying Levels of Genetic Heterozygosity. Journal of Heredity 86:280-288.

Imasheva AG, Bosenko DV, Bubli OA. 1999. Variation in morphological traits of Drosophila melanogaster (fruit fly) under nutritional stress. Heredity 82: 187-192.

Imasheva AG, Loeschcke V, Zhivotovsky LA, Lazebny OE. 1997. Effects of extreme temperatures on phenotypic variation and developmental stability in Drosophila melanogaster and Drosophila buzzatii. Biol J Linn Soc 61: 117-126.

Israfil H, Zehr SM, Mootnick AR, Ruvolo M, Steiper ME. 2011. Unresolved molecular phylogenies of gibbons and siamangs (Family: Hylobatidae) based on mitochondrial, Y- linked, and X-linked loci indicate a rapid Miocene radiation or sudden vicariance event. Mol Phylogenetic Evol 58: 447-455.

Iwasa Y. 2000. Dynamic optimization of plant growth. Ecol Ecol Res 2: 437-455.

Jagoe CH, Haines TA. 1985. Fluctuating asymmetry in fishes inhabiting acidifeied an unacidified lakes. Can J Zool 63: 130-138.

290

Janson CH, van Schaik CP. (1993). Ecological risk aversion in juvenile primates: Slow and steady wins the race. In Pereira ME, Fairbanks L A, editors. Juvenile Primates: Life History, Development, and Behavior. New York: Oxford University Press. p 57–74.

Jennions MD. 1996. The allometry of fluctuating asymmetry in southern African plants: flowers and leaves. Biol J Linn Soc 59: 127-142.

Kappeler PM, Pereira M, van Schaik CP. 2003. Primate life histories and socioecology. In: Kappeler PM, Pereira ME, editors. Primate life histories and socioecology. Chicago: University of Chicago Press. p 1–23.

Kark S, Lens L, Van Dongen S, Schmidt E. 2004. Asymmetry patterns across the distribution range: does the species matter? Biol J Linn Soc 81: 313-324.

Kay RF, Plavcan JM, Glander KE, Wright PC. 1988. Sexual selection and canine dimorphism in New World monkeys. Am J Phys Anthrol 77:385-397.

Kegley ADT, Hemingway J. 2007. Assessing fluctuating odontometric asymmetry among fossil hominin taxa through alternative measures of central tendency: Effect of outliers and directional components on reported results. HOMO – Journal of Comparative Human Biology 58:33-52.

Kelley J. 1997. Paleobiological and phylogenetic significance of life history in Miocene hominoids. In: Begun DR, Ward CV, Rose MD, editors. Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations. New York: Plenum Press. p 173– 208.

Kelley J. 2004. Life history and cognitive evolution. In: Russon A, Begun DR, editors. The evolution of thought: Evolutionary origins of great ape intelligence. Cambridge, UK: Cambridge University Press. p 280-297.

Kelley J, Schwartz, GT. 2010. Dental development and life history in living African and Asian apes. PNAS 107(3) 1035-1040.

Kelley J, Smith TM. 2003. Age at first molar emergence in early Miocene Afropithecus turkanensis and life-history evolution in the Hominoidea. J. Hum. Evol 44: 307-329.

Kellner JR, Alford RA. 2003. The Ontogeny of Fluctuating Asymmetry. American Naturalist. 161(6): 931-947.

Kieser JA. 1990. Human adult odontometrics: the study of variation in adult tooth size. Cambridge: Cambridge University Press.

291

Kieser JA, Groeneveld HT. 1986. Fluctuating odontometric asymmetry in a South African causcasoid population. J Dent Assoc S Afr 41: 185-189.

Kieser JA, Groeneveld HT, Preston CB. 1986. Fluctuating Dental Asymmetry as a Measure of Odontogenic Canalization in Man. Am J Phys Anthrol 71: 437-444.

Kirkpatrick RC. 1998. Ecology and behavior of snub-nosed and douc langurs. In: Jablonski NG, editor. The Natural History of the Doucs and Snub-Nosed Monkeys. Singapore:World Scientific Press. p 155–190.

Kirkpatrick RC. 2006. The Asian colobines: Diversity among leaf-eating monkeys. In: Campbell CJ, Fuentes A, MacKinnon K, Panger M, Bearder SK, editors. Primates in Perspective. Oxford: Oxford University Press. p 186–200.

Klingenberg CP. 2003. A developmental perspective on developmental instability. In: Polak M, editor. Developmental Instability: Causes and Consequences. New York: Oxford University Press. p14-34.

Klingenberg CP, Badyaev AV, Sowry SM, Beckwith NJ. 2001. Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. Am Nat 157: 11-23.

Klingenberg CP , McIntyre GS. 1998. Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52: 1363-1375.

Klingenberg CP , McIntyre GS, Zaklan SD. 1998. Left-right asymmetry of fly wings and the evolution of body axes. Pro R Soc Lond B Biol Sci 265: 1255-1259.

Klingenberg CP, Nijhout HF. 1999. Genetics of Fluctuating Asymmetry: A Developmental Model for Developmental Instability. Evolution 53(2): 358-375.

Knierim U, VanDongen S, Forkman, B, Tuyttens FAM, Spinka M, Campo JL, Weissengruber GS. 2007. Fluctuating asymmetry as an animal welfare indicator – A review of methodology and validity. Physiology and Behavior 92:398-421.

Knott CD. 1998. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating food availability. International Journal of Primatology 19: 1061– 1079.

Knott CD. 1999. Reproductive, Physiological and Behavioral Responses of Orangutans in Borneo to Fluctuations in Food Availability. Ph.D. Thesis, Harvard University, Cambridge, MA.

292

Knott CD. 2005. Energetic responses of food availability in the great apes; implications for hominin evolution. In: Brockman DK, van Schaik CP, editors. Seasonality in primates: Studies of living and extinct human and non-human primates. Cambridge, U.K.: Cambridge University Press, pp. 351–378.

Koshio C, Muraji M, Tatsuta H, Kudo S. 2007. Sexual selection in a moth: effect of symmetry on male mating success in the wild. Behavioral Ecology 18: 571-578.

Kozlov MV. 2003. Are fast growing birch leaves more asymmetrical? Oikos 101: 654– 658.

Kruuk LEB, Slate J, Pemberton JM, Clutton-Brock TH. 2003. Fluctuating asymmetry in a secondary sexual trait: no association with individual fitness, environmental stress or inbreeding, and no heritability. J Evol Bio 16: 101-113.

Kuswandari S, Nishino M. 2004. The mesiodistal crown diameters of primary dentition in Indonesian Javanese children. Archives of Oral Biology 49: 217-222.

Leamy LJ. 1999. Heritability of directional and fluctuating asymmetry for mandibular characters in random-bred mic. Journal of Evolutionary Biology 12: 146-155.

Leamy LJ, Klingenberg CP. 2005. The Genetics and Evolution of Fluctuating Asymmetry. Annu Rev Ecol Evol Syst 36:1-21.

Leamy LJ, Routman EF, Cheverud JM. 1997. A search for quantitative trait loci affecting asymmetry of mandibular characters in mice. Evolution 51: 957-969.

Leamy LJ, Routman EF, Cheverud JM . 2002. An epistatic genetic basis for fluctuating asymmetry of mandibular size in mice. Evolution 56: 642-653.

Leary RL, Allendorf FW, Knudsen KL. 1984. Superior developmental stability of heterozygosity in enzyme loci in salmonid fishes. American Naturalist 124: 540-551.

Leary RL, Allendorf FW. 1989. Fluctuating asymmetry as an indicator of stress: Implications for conservation biology. Trends in Ecology and Evolution 4(7): 214-217.

Leary RL, Allendorf FW, Knudsen RL. 1992. Genetic, environmental, and developmental causes of merisitic variation in rainbow trout. Acta Zool Fennica 191: 79- 95.

Leigh SR. 1992. Patterns of variation in the ontogeny of primate body size dimorphism. J Hum Evol 23:27-50.

293

Leigh SR. 2001. The Evolution of Human Growth. Evolutionary Anthropology 10:223– 236.

Leigh SR, Blomquist G. 2007. Life history. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Beader SK, editors. Primates in Perspective. Oxford, UK: Oxford University Press. p 396–407.

Leigh SR, Setchell JM, Buchanan LS. 2005. Ontogenetic Bases of Canine Dimorphism in Anthropoid Primates. Am J Phys Anthrol 127: 296-311.

Leigh SR, Setchell JM, Charpentier M, Knapp LA, Wickings J. 2008. Canine tooth size and fitness in male mandrills (Mandrillus sphinx). J Hum Evol 75-85.

Leigh SR, Shea BT. 1995. Ontogeny and the evolution of adult body size dimorphism in apes. Am J Phys Anthrol 36:37-60.

Lempa K, Martel J, Koricheva J, Haukioja E, Ossipov V, Ossipova S, Pihlaja K. 2000. Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion. Oecologia 122: 354-360.

Lens L, Van Dongen S. 2000. Fluctuating and directional asymmetry in natural bird populations exposed to different levels of habitat disturbance, as revealed by mixture analysis. Ecology Letters 3: 516-522.

Lens L, Van Dongen S, Kark S, Matthysen E. 2002. Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev 77: 27-38.

Lerner I. 1954. Genetic Homeostasis. New York: Wiley.

Leung B. 1998. Controlling for allometry in studies of fluctuating asymmetry and quality within samples. Proc R Soc Lond Ser B 265: 1623-1629.

Leung B, Forbes MR. 1996. Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience 3: 400-413.

Leung B, Forbes MR. 1997. Modeling fluctuating asymmetry in relation to stress and fitness. OIKOS 78(2):397-405.

Leung B, Forbes MR, Houle D. 2000. Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analysis involving multiple traits. American Naturalist 155: 101- 115.

294

Leutenegger W, Kelly JT. 1977. Relationship of sexual dimorphism in canine size and body size to social, behavioral and ecological correlates in anthropoid primates. Primates 18:117-136.

Ligon JD, Kimball R, Merola-Zwartjes, M. 1998. Mate choice by female red junglefowl: the issues of multiple ornaments and fluctuating asymmetry. Anim Behav 55: 41-50.

Livshits G, Kobyliansky E. 1991. Fluctutaing asymmetry as a possible measure of developmental homeostasis in humans. Hum Biol 63: 441-446.

Ludwig W. 1932. Das Recht-Links Proble im Teirreich und beim Menscen. Berlin: Springer.

Lundstrom A. 1960. Asymmetries in the number and size of the teeth and their aetiological significance. Transctions of the European Orthodontic Society 36: 167-185.

Macho GA. 2001. Primate molar crown formation times and life history evolution revisited. American Journal of Primatology 55:189-201.

MacKinnon J. 1974. The behavior and ecology of wild orang-utans (Pongo pygmaeus). Animal Behavior 22: 3-74.

Mal TK, Uveges JL, Turk KW. 2002. Fluctuating asymmetry as an ecological indicator of heavy metal stress in Lythrum salicaria. Ecological Indicators 1:189-195.

Mallard ST, Barnard CJ. 2004. Food stress, fluctuating asymmetry and reproductive performance in the Gryllid Crickets Gryllus bimaculatus and Gryllodes sigillatus. Behaviour 141: 219-232.

Manning JT, Chamberlain AT. 1993. Fluctuating asymmetry, sexual selection, and canine teeth in primates. Proc R Soc Lond B 251:83-87

Manning JT, Chamberlain AT. 1994. Fluctuating asymmetry, sexual selection, and canine teeth in primates. Proc R Soc Lond B 251:83-87.

Manning JT, Hartley MA. 1991. Symmetry and ornamentation are correlated in the peacock’s train. Animal Behavior 42: 1020-1021.

Markow TA. 1995. Evolutionary Ecology and Developmental Instability. Annu Rev Entomol 40: 105-120.

Markow TA, Martin JF. 1993. Inbreeding and developmental stability in a small human population. Annuals of Human Biology 20: 389-394.

295

Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M. 2009. Defining fallback foods and assessing their importance in primate ecology and evolution. AJPA 140: 603- 614.

Martin RD, MacLarnon AM. 1985. Gestation period, neonatal size and maternal investment in placental mammals. Nature 313: 220-223.

Martin, SA, Guatelli-Steinberg, D, Sciulli PW, Walker, PL. 2008. Brief Communication: Comparison of Methods for Estimating Chronological Age at Linear Enamel Formation on Anterior Dentition. Am J Phys Anthrol 135(3): 362-365.

Martin SA, Guatelli-Steinberg D, Sciulli PW. 2009. Sex differences in canine crown fluctuating asymmetry of Gorilla gorilla: A result of ontogenetic mechanisms underlying adult canine size sexual dimorphism? Presented at the 78th Annual Meeting of the American Association of Physical Anthropologists, Chicago, IL. Am J Phys Anthrol 138(S48): 185.

Martin SA, Guatelli-Steinberg D Sciulli PW. 2011. Relationships among crown formation time, fluctuating asymmetry, and linear enamel hypoplasia in gibbons and gorillas. Presented at the 79th Annual Meeting of the American Association of Physical Anthropologists, Minneapolis, Minnesota. Am J Phys Anthrol 144 (S52): 207.

Martel J, Lempa K, Haukioja E. 1999. Effects of stress and rapid growth on fluctuating asymmetry and insect damage in birch leaves. OIKOS 86: 208-216.

Mateos C, Alarcos S, Carranza J, Sanchez-Prieto S, Valencia J. 2008. Fluctuating asymmetry of red deer antlers negatively realtes to individual condition and proximity to prime age. Animal Behavior 75: 1629-1640.

Mather K. 1953. Genetical control of stability in development. Heredity 7: 297-336.

Matsudaria K, Ishida T. 2010. Phylogenetic relationships and divergence dates of the whote mitochondrial genome sequences among three gibbon genera. Molecular Phylogenetics and Evolution 55: 454-459.

Maynard-Smith J, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L. 1985. Developmental constraints and evolution. Quarterly Review of Biology 60: 265-287.

McGrew WC, Tutin CEG, Collins DA, File SK. 1989. Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal).Am. J. Primatol 17: 147–155.

296

McKenzie JA, Yen JL. 1995. Genotype, environment and the asymmetry phenotype. Dieldrin-resistance in Lucilia cuprina (the Australian sheep blowfly). Heredity 75: 181- 187.

McKey D. 1978. Soils, vegetation, and seed-eating by black colobus monkeys. In Montgomery GG, editor. The Ecology of Arboreal Folivores. Washington, DC: Smithsonian Institution Press. p 423-437.

Merila J, Bjorklund M. 1995. Fluctuating asymmetry and measurement error. Syste Biol 44(1): 97-101.

Mitton JB. 1993. Enzyme heterozygosity, metabolism, and developmental stability. Genetica 89: 47-65.

Mitton JB, Grant MC. 1984. Associations among protein heterozygosity, growth rate, and developmental homeostasis. Annual Review of Ecology and Systematics 15: 479-499.

Moller AP. 1988. Female choice selects for male sexual tail ornaments in monogamous swallow. Nature 332: 640-642.

Møller AP. 1990. Fluctuating asymmetry in male sexual ornaments may reliably reveal male quality. Anim Behav 40: 1185-1187.

Moller AP. 1991. Sexual ornament size and the cost of fluctuating asymmetry. Proc R Soc Lond B 243: 59-62.

Møller AP. 1992. Patterns of fluctuating asymmetry in weapons: evidence for reliable signaling of quality in beetle horns and bird spurs. Proc R Soc Lond B 248: 199-206.

Moller AP. 1993. Developmental stability, sexual selection, and speciation. Journal of Evolutionary Biology 6: 493-509.

Møller AP. 1997. Developmental stability and fitness: a review. Am. Nat. 10:1-6.

Moller AP. 2000. Developmental stability and pollination. Oecologia 123: 149-157.

Moller AP, Cuervo JJ, Soler JJ, Zamora-Munoz C. 1996. Horn asymmetry and fitness in gemsbok, Oryx g. gazelle. Behavioral Ecology 7(3): 247-253.

Møller AP, Hoglund J. 1991. Patterns of fluctuating asymmetry in avian feather ornaments: implications for models of sexual selection. Proc R Sco London Ser B 245:1- 5.

297

Møller AP, Pomiankowski A. 1993. Fluctuating asymmetry and sexual selection. Genetica 89:267-279.

Møller AP, Swadle JP. 1997. Ontogeny of asymmetry and phenodeviants. In: Moller AP, Swaddle JP, editors. Asymmetry, Developmental Stability, and Evolution. New York, NY: Oxford University Press. p 37-66.

Morrogh-Bernard H,Husson SJ,Knott CD,Wich SA,van Schaik CP,Van Noordwijk MA,Lackman-Ancrenaz I,Marshall AJ,Kanamori T,Kuze N,bin Sakong R. 2009. Orangutan activity budgets and diet: a comparison between species, populations, and habitats. In: WichSA,Utami-AtmokoSS,SetiaTM,van SchaikCP, editors. Orangutans: geographic variation in ecology and conservation. Oxford: Oxford University Press. p 119–133.

Mpho M, Holloway GJ, Callaghan A. 2001. A comparison of the effcts of organophosphate insecticide exposure and temperature stress on fluctuating asymmetry and life history traits in Culex quinquefasciatus. Chemosphere 45:713-720.

Nass GG. 1982. Dental asymmetry as an indicator of developmental stress in a free ranging troop of Macaca fuscata. In: Kurten B, editor. Teeth: form, function and evolution. New York: Columbia University Press, p.207-227.

Newell EA. 1998. Dental enamel hypoplasia in non-human primates: a systematic assessment of its occurrence and distribution. Ph.D. dissertation, Temple University, Philadelphia, PA.

Newell EA, Guatelli-Steinberg D, Field M, Cooke C, Feeney RNM. 2006. Life history, enamel formation, and linear enamel hypoplasia in the Ceboidea. Am J Phys Anthrol 131: 252-260.

Nijhout HF, Daviowitz G. 2003. Developmental Perspectives on Phenotypic Variation, Canalization, and Fluctuating Asymmetry. In: Polak M, editor. Developmental Instability: Causes and Consequences. New York: Oxford University Press. p.3-15.

Nosil P, Teimchen TE. 2001. Tarsal asymmetry, nutritional condition, and survival in water boatmen (Callicorixa vulnerata). Evolution 55: 712-720.

Noss JF, Scott GR, Potter RHY, Dahlberg AA. 1983. Fluctuating asymmetry in molar dimensions and discrete morphological traits in pima Indians. Am J Phys Anthrol 61: 437-445.

Nunn CL, Altizer S, Jones KE, Sechrest W. 2003. Comparative Tests of Parasites Speices Richness in Primates. American Naturalist 162: 597-614.

298

Palmer AR. 1994. Fluctuating asymmetry analyses: a primer. In: Markow TA, editor. Developmental instability: its origins and evolutionary implications. Boston: Kluwer Academic. P 335-364.

Palmer AR. 1996. Waltzing with Asymmetry. BioScience 46(7): 518-532.

Palmer AR, Strobeck C. 1986. Fluctuating asymmetry: Measurement, Analysis, Patterns. Ann Rev Ecol Syst 17:391-421.

Palmer AR, Strobeck C. 1992. Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191: 57-72.

Palmer AR, Strobeck C. 2003. Fluctuating asymmetry analyses revisited. In: Polak M (editor). Developmental instability. Causes and consequences. Oxford: Oxford University Press. p.279-319.

Parsons PA. 1962. Maternal age and developmental variability. Journal of Experimental Biology 39: 251-260.

Parsons PA. 1990. Fluctuating asymmetry: An epigenetic measure of stress. Biol Rev 65:131-145.

Parsons PA. 1992. Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68:361-364.

Pereira ME, Leigh SR. 2003. Modes and phases of primate juvenility. In: Kappeier PM, Pereira ME, editors. Primate life histories and socioecology. Chicago: University of Chicago Press. p149-176.

Perrin N, Sibly RM. 1993. Dynamic models of energy allocation and investment. Annual Review of Ecology and Systematics 24: 379-410.

Perzigian AJ. 1977. Fluctuating Dental Asymmetry Variation among Skeletal Populations. Am J Phys Anthrol 47: 81-88.

Pither J, Taylor PD. 2000. Directional and fluctuating asymmetry in black-winged damselfly Calopteryx maculate (Beauvois) (Odonata: Calopterygidae). Can J Zool 78: 1740-1748.

Plavcan JM. 1990. Sexual dimorphism in the dentition of extant anthropoid primates. Ph.D. dissertation, Duke University.

299

Plavcan JM. 1993. Canine size and shape in male anthropoid primates. Am J Phys Anthrol 92(2):201-216.

Plavcan JM. 2000. Inferring social behavior from sexual dimorphism in the fossil record. J Hum Evol 39: 327-344.

Plavcan JM. 2001. Sexual dimorphism in primate evolution. Yrbk Phys Anthropol 44: 25–58.

Plavcan JM. 2004. Sexual selection, measures of sexual selection, and dimorphism in primates. In: Kappeler P, van Schaik C, editors. Sexual selection in primates: new and comparative perspectives. Cambridge: Cambridge University Press. p 230–252.

Plavcan JM. 2011. Understanding dimorphism as a function of changes in male and female traits. Evol Anthro 20: 143-155.

Plavcan JM, Kay RF. 1988. Sexual dimorphism and dental variability in platyrrhine primates. International Journal of Primatology 9(3): 169-178.

Plavcan JM, van Schaik, CP. 1992. Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthrol 87: 461-477.

Plavcan JM, van Schaik CP, Kappeler PM. 1995. Competition, coalitions and canine size in primates. J Hum Evol 28: 245-276.

Plavcan JM, Ward CV, Paulus FL. 2009. Estimating canine tooth crown height in early Australopithecus. J Hum Evol 57:2-10.

Polak M. 1993. Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: implications for sexual selection. Genetica 89: 255-265.

Polak M, Trivers R. 1994. The science of symmetry in biology. TREE 9(4):122-124.

Poulsen JR, Clark CJ, Connor EF, Smith TB. 2002. Differential resource use by primates and hornbills: Implications for seed dispersal. Ecology 83: 228–240.

Prentice S, Jobes AJ, Burness G. 2008. Fault bars and fluctuating asymmetry in birds: are the two measures correlated? J. Field Ornithol 79(1):58-63.

Prowse TL. 2010. Diet and Dental Health through the Life Course in Roman Italy. Social Bioarchaeology, 410.

300

Purvis A, Orme CDL, Dolphin K. 2003. Why are most species small bodied? A phylogenetic view. In: Blackburn TM, Gaston KJ, editors. Macroecology: concepts and consequences. Oxford: Blackwell Science. P 155-173.

Radwan J. 2003. Inbreeding not stress increases fluctuating asymmetry in the bulb mite. Evolutionary Ecology Research. 5: 287-295.

Reichard UH, Barelli C. 2008. Life History and Reproductive Strategies of Khao Yai Hylobates lar: Implications for Social Evolution in Apes. Int J Primatol 29: 823-844.

Reichard UH, Ganpanakngan M, Barelli C. 2012. White-handed gibbons of Khao Yai: Social flexibility, complex, reproductive strategies, and a slow life history. In: Kappeler PM, Watts D, editors. Long-term field studies of primates. Heidelberg: Springer p. 237– 258.

Reid DJ, Dean MC. 2005. Variation in modern human enamel formation times. Journal of Human Evolution 50: 329-346.

Reid DJ, Ferrell RJ. 2006. The relationship between number of striae of Retzius and their periodicity in the imbricational enamel formation. J Hum Evol 50: 195-202.

Reid DJ, Schwartz GT, Chandrasekera MS. 1998. A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes. J Hun Evol 35:427-448.

Remis MJ. 2003. Are gorillas vacuum cleaners of the forest floor? The roles of gorilla body size, habitat and food preferences on dietary flexibility and nutrition. In: Taylor AB, Goldsmith ML, editors. Gorilla biology: a multidisciplinary perspective. Cambridge: Cambridge University Press. p 385–404.

Ricklefs RE. 1968. Patterns of growth in birds. The IBIS 110(4): 419-451.

Ridley M. 1996. Evolution, 2nd edn. Cambridge, MA: Blackwell Science.

Roldan ERS, Cassinello J, Abiagar T, Gomendio M. 1998. Inbreeding, fluctuating asymmetry and ejaculate quality in an endangered ungulate. Proc R Soc Lond B Biol Sci 265: 243-248.

Rose KE, Atkinson RL, Turnbull LA, Rees M. 2009. The costs and benefits of fast living. Ecology Letters 12: 1379-1384.

Ross C. 1998. Primate life histories. Evol Anthro 6: 54-63.

301

Ross C, Jones KE. 1999. Socioecology and the evolution of primate reproductive rates. In: Lee PC, editor. Comparative primate socioecology. Cambridge: Cambridge University Press. p 73–110.

Ross C, MacLarnon A. 1995. Ecological and social correlates of maternal expenditure on infant growth in haplorhine primates. In Pryce C, Martin RD, Skuse D, editors. Motherhood in Human and Nonhuman Primates: Biological and Social Determinants,. Basel: Karger. p 37–46.

Rowe L, Repasky RR, Palmer AR. 1997. Size-Dependent Asymmetry: Fluctuating Asymmetry Versus Antisymmetry and Its Relevance to Condition-Dependent Signaling. Evolution 51(5): 1401-1408.

Roy BA, Stanton ML. 1999. Asymmerty of wild mustard, Sinapis arvensis (Brassicaceae) in response to severe physiological stresses. J Evol Biol 12: 440-449.

Ruiz-Garcia M, Castillo MI, Vasquez C, Rodriguez K, Pinedo-Castro M, Shostell J, Leguizamon N. 2010. Molecular phylogenetics and phlyogeography of the white-fonted capuchin (Cebus albifrons; Cebidae, Primates) by means of mtCOII gene sequences. Molecular Phylogenetics and Evolution 27: 1049-1061.

Rylands, A. B., Coimbra-Filho, A. F. & Mittermeier, R. A. (2009): The systematics and distributions of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and callimico (Callimico) (Callitrichidae, Primates). In: Ford SM, Porter L, Davis LC, editors. The smallest anthropoids: the marmoset/callimico radiation. New York, NY: Springer. P 25- 61.

Rylands AB, Mittermeier RA, Silva JS. 2012. Neotropical primates: taxonomy and recently described species and subspecies. International Zoo Yearbook 46: 11-24.

Rylands AB, Schneider H, Langguth A, Mittermeier RA, Groves CP, Rodriguez-Luna E. 2000. An assessment of the diversity of New World Primates. Neotrop. Primates 8: 61– 93.

Saunders SR, Mayhall JT. 1982. Fluctuating Asymmetry of Dental Morphological Traits: New Interpretations. Human Biology 54(4):789-799.

Schew WA, Ricklefs RE. 1998. Developmental plasticity. In: Starck JM, Ricklefs RE, editors. Avian growth and development. New York: Oxford University Press, p288–304.

Schultz AH. 1935. Eruption and delay of the permanent teeth in primates. Am J Phys Anthrol 19:489-588.

302

Schwartz GT, Dean MC. 2001. The ontogeny of canine dimorphism in extant hominoids. Am J Phys Anthrol 115: 269-283.

Schwartz GT, Miller ER, Gunnell GF. 2005. Developmental processes and canine dimorphism inprimate evolution. J Hum Evol 48:97-103.

Schwartz GT, Reid DJ, Dean CM. 2001. Developmental Aspects of Sexual Dimorphism in Hominoid Canines. International Journal of Primatology. 22(5):837-860.

Schwartz GT, Reid DJ, Dean MC, Zihlman AL. 2006. A faithful record of the stressful life events preserved in the dental developmental record of a juvenile gorilla. International Journal of Primatology 27: 1201-1219.

Sciulli PW, Doyle WJ, Kelley C, Seigel P, Siegel M. 1979. The interaction of stressors in the induction of increased levels of fluctuating asymmetry in the laboratory rate. Am J Phys Anthrol 50(2):279-284.

Sciulli PW. 2003. Dental asymmetry in a Late Archaic and Late Prehistoric Skeletal Sample of Ohio Valley Area. Dental Anthropology Journal. 16(2): 3-14.

Searcy WA, Peters S, Nowicki S. 2004. Effects of early nutrition on growth rate and adult size in song sparrows Melospiza melodia. Journal of Avian Biology 35: 269-279.

Shakarad M, Prasad NG, Rajamani M, Joshi A. 2001. Evolution of faster development does not lead to greater fluctuating asymmetry of sternopleural bristle number in Drosophila. Journal of Genetics 80(1): 1-7.

Shellis RP. 1998. Utilization of periodic markings in enamel to obtain information on tooth growth. J Hum Evol 35:387-400.

Siegel ML, Doyle WJ. 1975. The effects of cold stress on fluctuating asymmetry in the dentition of the mouse. J Exp Zool 193: 385-359.

Siegel SJ, Hof PR, Kraemer G, McKinney WT, Morrison JH. 1992. Effects of postnatal mossy fiber development on CA3 apical dendrites in differentially reared monkeys Soc. Neurosci. Abstr., 18: 34

Siikamaki P, Lammi A. 1998. Fluctuating asymmetry in central and marginal populations of Lychnis viscaria in relation to genetic and environmental factors. Evolution 52:1285- 1292.

Simmons LW, Ritchie MG. 1996. Symmetry in the songs of crickets. Proc R Soc Lond B Biol Sci 263: 305-311.

303

Sirianni JE, Swindler DR. 1982. Growth and Development of the Pigtail Macaque. Boca Raton (FL): CRC Press.

Skinner MF, Dupras TL, Moya-Sola S. 1995. Periodicity of linear enamel hypoplasia among Miocene Dryopithecus from Spain. J Paleopathol 7:195–222.

Skinner MF, Guatelli-Steinberg D. 1997. Distribution of linear enamel hyperplasia in sympatric monkeys and apes. Am J Phys Anthrol Suppl 24:213.

Smith BH. 1989. Dental Developmental as a Measure of Life History in Primates. Evolution 43(3):683-688.

Smith BH. 1992. Life history and the evolution of human maturation. Evolutionary Anthropology 134-142.

Smith BH. 1994. Patterns of Dental Development in Homo, Australopithecus, Pan, and Gorilla. Am J Phys Anthrol 94:307-325.

Smith BH, Garn SM, Cole PE. 1982. Problems of sampling and inference in the study of fluctuating dental asymmetry. Am J Phys Anthrol 58: 281-289.

Smith DR, Crespi BJ, Bookstein FL. 1997. Fluctuating asymmetry in the honey bee, Apis mellifera: Effects of ploidy and hybridization. J Evol Biol 10: 551-574.

Smith TM. 2006. Experimental determination of the periodicity of incremental features in enamel. J Anat 208: 99-113.

Smith TM, Reid DJ, Dean MC, Olejiczak AJ, Martin LB. 2007. Molar development in common chimpanzees (Pan troglodytes) Journal of Human Evolution 52: 201-216.

Smith TM, Smith BH, Reid DJ, Siedel H, Vigilant L, Hublin JJ, Boesch, C. 2010. Dental development of the Tai Forest chimpanzees revisited. Journal of Human Evolution 58: 363-373.

Smith TM, Tafforeau P, Reid DJ, Pouech J, Lazzari V, Zermeno JP, Guatelli-Steinberg D, Olejniczak AJ, Hoffman A, Radovcic J, Makaremi M, Toussanit M, Stringer C, Hublin J-J. 2011. Dental evidence for ontegenetic differneces between modern humans and Neandethals. PNAS 107(49): 20932-20928.

Sokal RR, Rohlf FJ. 1995. Biometry. San Francisco: Freeman.

Soule ME. 1979. Heterozygoisty and developmental stability: another look. Evolution 331: 396-401.

304

Soule ME, Cuzin-Roudy J. 1982. Allomeric Variation. 2. Developmental Instabilty of Extreme Phenotypes. American Naturalist 120: 765-786.

Suarez BK. 1974. Neanderthal dental asymmetry and the probably mutation effect. Am J Phys Anthrol 41:411-416.

Swaddle JP. 1996. Reproductive success and symmetry in Zebra Finches. Animal Behaviour 51: 203-210.

Swaddle JP, Witter MS. 1994. Fluctuating Asymmetry, Competition, and Dominance. Proceedings: Biological Sciences 256(1347): 299-303.

Swaddle JP, Witter MS, Cuthill C. 1994. The analysis of fluctuating asymmetry. Anim Behav 48: 986-989.

Swaddle JP, Witter MS, Cuthill C. 1995. Museum studies measures FA. Anim Behav 49: 1700-1701.

Swaddle JP, Witter MS. 1997. On the ontogeny of developmental stability in a stabilized trait. Proc R Soc Lond B 264:329-334.

Swindler DR. 1985. Nonhman primate dental development and its relationship to human dental development.

Swindler DR, Oshan AF, Sirianni JE. 1982. Sex differences in permanent mandibular tooth development in Macaca nemestrina. Human Biology 54(1):45-52.

Ten Cate AR. 1994. Oral histology: development, structure, and function, 4th ed. St. Louis: CV Mosby.

Thoday JM. 1958. Homeostasis in a selection experiment. Heredity 12: 401-415.

Thomas F, Ward DF, Poulin R. 1998. Fluctuating asymmetry in an insect host: A big role for big parasites? Ecology Letters 1: 112-117.

Thoren S, Lindenfors P, Kappeles PM. 2006. Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size. Am J Phys Anthrol 130(1):50-59.

Thornhill R. 1992. Fluctuating Asymmetry, Interspecific Aggression, and Male Mating Tactics in Two Species of Japanese Scorpionflies. Behavioral Ecology and Sociobiology 30(5): 357-363.

305

Thornhill R, Møller AP. 1998. The relative importance of size and asymmetry in sexual selection. Behav Ecol 9:546-551.

Tilson R, Seal US, Soemarna K, Ramono W, Sumardja E, Poniran S, van Schaik C, Leighton M, Rijksen H, Eudey A. 1993. Orangutan population and habitat viability analysis report. (Medan, Indonesia, Orangutan population and habitat viability analysis workshop).

Tomkins JL, Simmons LW. 1995. Patterns of fluctuating asymmetry in earwig forceps: no evidence for reliable signaling. Proceedings: Biological Sciences 259: 89-96.

Tomkins JL, Simmons LW. 1996. Dimorphisms and fluctuating asymmetry in the forceps of male earwigs. J Evol Bio 9: 753-770.

Townsend GC, Brown T. 1980. Dental asymmetry in Australian Aboriginals. Hum Biol 52: 661-673.

Townsend GC, Garcia-Godoy F. 1984. Fluctuating asymmetry in the deciduous dentition of Dominican mulatto children. Achieves of Oral Biology 29: 483-486.

Trotta V, Calboli C, Garoia F, Grifoni D, Cavicchi S. 2005. Fluctuating asymmetry as a measure of ecological stress in Drosophila melanogaster (Diptera: Drosophilidae). Eur J Entomol 102:195-200.

Tutin CEG, Fernandez M, Rogers ME, Williamson EA, McGrew WC, Altmann SA, Southgate DAT, Crowe I, Tutin CEG, Whiten A, Conklin NL, Barrett L. 1991. Foraging Profiles of Sympatric Lowland gorillas and Chimpanzees in the Lope Reserve, Gabon (and Discussion). Phil Trans R Soc Lond B 334: 179-186.

Uetz GW, McClintock WG, Miller D, Smith EI, Cook KK. 1996. Limb regeneration and subsequent asymmetry in a male secondary sexual character influences sexual selection. Behav Ecol Sociobiol 38: 253-257.

Ulijaszek SJ. 2002. Comparative energetics of primate fetal growth. Amer J Hum Biol 14: 603-608.

Valentine DW, Soule ME. 1973. Effect of p-DDT on developmental stability of pectoral fin rays in the grunion, Leuresthes tenius. Fishery Bulletin 71: 921-920.

Van Dongen S. 1999. Accuracy and power in the statistical analysis of fluctuating asymmetry: effects of between-individual heterogeneity in developmental instability. Ann Zool Fennici 36: 45-52.

306

Van Dongen S. 2000. Unbiased estimation of individual symmetry. Journal of Evolutionary Biology 13: 107-112.

Van Dongen S. 2006. Fluctuating asymmetry and developmental instability in evolutionary biology: past, present, and future. J Evol Biol 19: 1727-1743.

Van Dongen S, Lens L. 2000. The evolutionary potential of developmental stability. J Evol Bio 13:326-335.

Van Dongen S, Molenberghs G, Matthysen E. 1999. The statistical analysis of fluctuating asymmetry: REML estimation of a mixed regression model. J Evol Bio 12: 94-102.

Van Dongen S, Moller AP. 2007. On the distribution of developmental errors: comparing the normal, gamma, and log-normal distribution. Biological Journal of the Linnean Society 92: 197-210.

Van Valen L. 1962. A study of fluctuating asymmetry. Evolution 16:125-142.

van Schaik CP,Marshall AJ,Wich SA. 2009. Geographic variation in orangutan behavior and biology: its functional interpretation and its mechanistic basis. In: Wich SA, Utami- Atmoko SS,Setia TM,van Schaik CP, editors. Orangutans: geographic variation in ecology and conservation. Oxford: Oxford University Press. p 351–361.

Veiga JP, Salvador A, Martin J, Lopez P. 1997. Testosterone stress does not increase asymmetry of a hormonally mediated sexual ornament in a lizard. Behav Ecol Sociobiol 41: 171-176.

Vishalakshi C, Singh BN. 2008.Erratum – Effect of environmental stress on fluctuating asymmetry in certain morphological traits in Drosophila ananassae: nutrition and larval crowding. Canadian Journal of Zoology 86: 427-437.

Vitzthum VJ, Wikander R. 1988. Incidence and correlates of enamel hypoplasia in non- human primates. Am J Phys Anthrol 75:284

Vogel ER, Knott CD, Crowley BE, Blakely MD, Larsen MD, Dominy NJ. 2012. Bornean oranguatans on the brink of protein bankruptcy. Biol Lett 8: 333-336.

Vollestan LA, Hindar K, Moller AP. 1999. A meta-analysis of fluctuating asymmetry in relation to heterozygosity. Heredity 83: 206-218.

Vrijenhoek RC. 1985. Animal population genetics and disturbance: The effects of local extinction and recolonizations on heterozygosity and fitness. In: Pickett STA, White P,

307

editors. The Ecology of Natural Disturbance and Patch Dynamics. New York: Academic Press. p265-285.

Vrijenhoek RC, Lerman S. 1982. Heterozygosity and developmental stability under sexual and asexual breeding systems. Evolution 36: 768-776.

Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563-565.

Waddington CH. 1953. Epigenetics and evolution. J Exp Zool 7:187-199.

Waddington CH. 1957. The Strategy of the Genes. New York: Macmillan.

Waddington CH. 1961. Genetic assimilation. Adv Genet 10:257-293.

Waldman P. 2001. The effect of inbreeding on fluctuating asymmetry in Scabiosa canescens (Dipsacaceae). Evolutionary Ecology 15: 117-127.

Waston PJ, Thornhill R. 1994. Fluctuating asymmetry and sexual selection. TREE 9:21- 25.

Watts DP. 1990. Mountain gorilla life histories, reproductive competition, and sociosexual behavior and some implications for husbandry. Zoo Biol 9:185-200

Waynforth D. 1998. Fluctuating asymmetry and human male life history traits in rural Belize. Proc R Soc Lond B 263: 849-853.

Whitlock M. 1998. The repeatability of fluctuating asymmetry: A revision and extension. Proceedings of the Royal Society of London Series B 256: 1428-1430.

Wich SA, Buij R, van Schaik C. 2004. Determinants of orangutan density in the dryland forests of the Leuser Ecosystem. Primates 45; 177-182.

Wich, S.A., Singleton, I., Utami-Atmoko, S.S., Geurts, M.L., Rijksen, H.D., van Schaik, C.P., 2003. The status of the Sumatran Orangutan Pongo abelii: an update. Oryx 37, 49– 54.

Wich, SA, Utami-Atmoko SS, Setia TM, Djoyosudharmo S, Geruts ML. 2006. Dietary and Energetic Responses of Pongo abelii to Fruit Availability Fluctuations. International Journal of Primatology 27: 1535-1550.

Willmore KE, Young NM, Richtsmeier JT. 2007. Phenotypic variability: Its components, measurement and underlying developmental processes. Evol Biol 34:99-120.

308

Wilson EO. 1975. Sociobiology: The New Synthesis. Cambridge: Belknap Press of Harvard University Press.

Windig JJ, Nylin S. 1999. Adapative wing asymmetry in males of the speckled wood butterfly (Pararge aegeria)? Proc R Soc Lond B Biol Sci 266; 1413-1418.

Wood L. 1996. Frequency and chronological distribution of linear enamel hypoplasia in a North American colonial skeletal sample. Am J Phys Anthrol 100: 247-259.

Woolf CM, Markow TA. 2003. Genetic models for Developmental Homeostasis: Historical Perspectives. In: Polak, M, editor. Developmental Instability: Causes and Consequences. New York: Oxford University Press. p99-115. Wrangham RW. 2000. Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In: Kappeler EP, editor. Male Primates. Cambridge: Cambridge University Press. p248-258.

Wrangham RW, Conklin-Brittain NL, Hunt KD. 1998. Dietary Response of Chimpanzees and Cercopithecines to Seasonal Variation in Fruit Abundance. I. Antifeedants. International Journal of Primatology 19: 949-970.

Yamagiwa J,Kahekwa J,Basabose AK. 2003. Intra-specific variation in social organization of gorillas: implications for their social evolution. Primates 44: 359–369.

Zakharvo A. 1981. Fluctuating asymmetry as an index of developmental homeostasis. Genetika 13: 241-256.

Zakharvo A. 1987. Asymmetry of Animals. Moscow: Nauka.

Zakharvo A. 1989. Future prospects for population phenogenetics. Soviet Sci Rev F Physiol General Biol 4: 1-79.

Zakharvo A. 1992. Population phenogeneitcs: analysis of developmental stability in natural populations. Acta Zool Fennica 191:7-30

Zakharvo A. 1993. Appearance, fixation and stabilization of environmentally stability and population variation. Russ J Ecol 32: 146-150.

Zakharvo A. 1994. Appearance, fixation and stabilization of environmentally induced phenotypic changes as a micro-evolutionary event. In: Markow TA (ed) Developmental Instability: Its Origins and Evolutionary Implications. Dordrecht: Kluwer Academic Publishers. P 229-236.

309

Zakharvo A, Pankakoski E, Sheftel B, Peltonen A, Hanski I. 1991. Developmental stability and population dynamics in the common skew, Sorex araneus. American Naturalist 138: 797-810.

Zakharvo A, Yablokov A. 1990. Skull asymmetry in the Baltic grey seal: Effects of environmental pollution. Ambio 19: 226-269.

310

APPENDIX A

SPECIMEN LISTINGS

Genus Species Subspecies Region MUS* M F Pan troglodytes Unknown CMNH 1 1 Pan troglodytes Bata MCZ 1 0 Pan troglodytes Cameroon CMNH 17 30 MCZ 3 1 NMNH 0 2 Pan troglodytes Congo CMNH 1 0 Pan troglodytes Gabon NMNH 2 4 Pan troglodytes Guinea AMNH 1 0 Pan troglodytes Liberia NMNH 1 1 Pan troglodytes Mete 1 0 Pan troglodytes Nigeria CMNH 0 1 Pan troglodytes West Africa CMNH 1 0 MCZ 0 1 NMNH 0 1 Pan troglodytes troglodytes Unknown AMNH 3 2 Pan troglodytes troglodytes Cameroon AMNH 7 3 Pan troglodytes troglodytes Congo AMNH 1 0 Pan troglodytes troglodytes Guinea AMNH 0 1 Pan troglodytes troglodytes Rwanda AMNH 1 0 Gorilla gorilla Unknown CMNH 3 1 NMNH 2 0 Gorilla gorilla Cameroon CMNH 50 62 NMNH 8 0 Gorilla gorilla Congo CMNH 8 5 NMNH 0 7 Gorilla gorilla Gabon CMNH 1 0 NMNH 4 3 continued

311

Specimen Listing, continued

Gorilla gorilla Nigeria CMNH 0 1 Gorilla gorilla Rwanda NMNH 7 3 Gorilla gorilla West Africa CMNH 4 0 Gorilla gorilla gorilla Unknown AMNH 7 0 FMNH 1 2 MCZ 1 0 Gorilla gorilla gorilla Africa FMNH 0 1 Gorilla gorilla gorilla Cameroon AMNH 11 3 FMNH 4 1 MCZ 2 1 Central African Gorilla gorilla gorilla AMNH 0 1 Republic Gorilla gorilla gorilla DRC FMNH 1 0

Pongo pygmaeus Unknown NMNH 3 0 Borneo MCZ 4 4 Indonesia AMNH 1 0 NMNH 6 3 Malaysia NMNH 1 1 Hylobates lar Unknown FMNH 2 2 NMNH 0 1 Hylobates lar Thailand CMNH 9 5 Hylobates lar carpenteri Thailand NMNH 5 5 Hylobates lar entelloides Unknown AMNH 4 2 Hylobates lar entelloides Burma AMNH 1 0 Hylobates lar entelloides Myanmar NMNH 7 0 Hylobates lar entelloides Thailand AMNH 2 3 FMNH 9 6 NMNH 3 4 Hylobates lar lar Unknown MCZ 0 1 Hylobates lar lar Chieng Dao MCZ 6 6 Hylobates lar lar Malaysia FMNH 2 1 Hylobates lar lar Mount Angka MCZ 22 20 Hylobates lar lar Thailand MCZ 1 0 Hylobates agilis agilis Sumatra AMNH 10 4 Hylobates hoolock hoolock Unknown AMNH 1 1 Hylobates hoolock hoolock Burma AMNH 23 16 Hylobates hoolock hoolock India AMNH 6 1 Symphalangus syndactylus Malaysia NMNH 1 0 continued 312

Specimen Listing, continued

Papio anubis Unknown AMNH 1 0 MCZ 3 1 NMNH 3 2 TP 23 20 Papio anubis DRC AMNH 3 2 FMNH 1 1 Papio anubis Ethiopia AMNH 1 0 FMNH 4 3 Papio anubis Kenya AMNH 3 0 FMNH 3 4 MCZ 1 2 NMNH 8 8 Papio anubis Sudan FMNH 3 0 Papio anubis Tanzania AMNH 3 1 FMNH 2 0 MCZ 2 0 NMNH 1 0 Papio anubis Uganda NMNH 1 0 Macaca mulatta Unknown AMNH 1 1 FMNH 1 0 NMNH 9 35 Macaca mulatta mulatta Unknown AMNH 2 0 Macaca mulatta mulatta Burma AMNH 5 8 Macaca mulatta mulatta China AMNH 4 6 Macaca mulatta mulatta India FMNH 1 0 Macaca mulatta mulatta Laos AMNH 1 0 Macaca mulatta mulatta Nepal FMNH 1 0 Macaca mulatta mulatta Thailand AMNH 2 2 FMNH 1 1 Macaca nemestrina Unknown AMNH 2 1 FMNH 1 0 NMNH 3 2 India AMNH 0 1 Indonesia NMNH 11 2 Malaysia NMNH 0 2 Lophocebus albigena Unknown TP 1 10 Lophocebus albigena albigena Unknown AMNH 1 2 NMNH 1 0 continued 313

Specimen Listing, continued

Lophocebus albigena albigena DRC AMNH 6 4 FMNH 3 3 Lophocebus albigena albigena Gabon NMNH 1 2 Uganda NMNH 4 2 Cercopithecus cephus Unknown AMNH 0 1 NMNH 0 1 Cameroon NMNH 1 0 Cercopithecus cephus cephodes Unknown AMNH 1 1 NMNH 1 0 Cameroon AMNH 3 3 Central African AMNH 0 1 Republic Gabon NMNH 12 8 Guinea FMNH 1 0 Cercopithecus mitis stuhlmanni Unknown AMNH 6 5 MCZ 0 1 Elgonyi MCZ 0 2 Kenya MCZ 2 0 NMNH 6 5 Ruwenzori MCZ 2 0 Rwanda NMNH 1 0 Sudan FMNH 0 3 MCZ 2 1 NMNH 1 0 Tanzania MCZ 2 0 NMNH 1 0 Uganda NMNH 2 12 Zaire AMNH 17 11 FMNH 2 1 Zimbabwe NMNH 0 1 Colobus guereza Unknown FMNH 9 1 Colobus guereza Ethiopia FMNH 4 0 Colobus guereza cadudatus Tanzania FMNH 0 2 Colobus guereza gallarum Ethiopia FMNH 8 2 Colobus guereza guereza Ethiopia FMNH 4 2 Colobus guereza kikuyuensis Kenya FMNH 6 1 Colobus guereza matschiei Sudan FMNH 0 1 Colobus guereza occidentalis DRC FMNH 5 4 Colobus guereza occidentalis Kenya FMNH 0 1 Colobus guereza occidentalis Sudan FMNH 2 0

continued 314

Specimen Listing, continued

Cebus albifrons Unknown TP 2 1 Colombia FMNH 9 2 Ecuador AMNH 5 2 Peru FMNH 10 5 Cebus albifrons aequatorialis Peru AMNH 1 0 Cebus albifrons cuscinus Ecuador MCZ 1 0 Peru AMNH 3 2 Cebus albifrons trinitatis Trinidad AMNH 0 1 FMNH 0 1 Cebus albifrons unicolor Brazil AMNH 2 6 Colombia AMNH 1 0 Peru AMNH 2 2 FMNH 4 2 Rio Tapajos MCZ 0 2 Venezuela AMNH 0 1 Cebus albifrons versicolor Colombia FMNH 1 0 MCZ 2 1 Peru MCZ 1 0 Venezuela FMNH 1 4 Cebus apella Unknown TP 0 1 FMNH 1 0 Cebus apella Bolivia FMNH 1 3 Cebus apella Brazil AMNH 5 2 FMNH 10 5 Cebus apella Colombia AMNH 1 1 FMNH 15 13 Cebus apella Guyana FMNH 0 1 Cebus apella Meta AMNH 0 1 Cebus apella Peru AMNH 2 3 FMNH 18 8 Cebus apella Suriname FMNH 10 6 Cebus apella macrocephalus Brazil AMNH 7 3 Cebus apella macrocephalus Coral Grande MCZ 1 0 Cebus apella macrocephalus Rio Tapajos MCZ 10 6 Cebus apella paraguayanus Unknown AMNH 0 1 Cebus apella paraguayanus Brazil AMNH 20 8 Cebus apella versutus Brazil AMNH 8 0 Ateles geoffroyi Unknown FMNH 0 4 TP 0 1 315

continued

Specimen Listing, continued

Ateles geoffroyi Nicaragua AMNH 0 1 Ateles geoffroyi ornatus Costa Rica AMNH 3 4 Ateles geoffroyi vellerosus Guatemala FMNH 1 1 Ateles geoffroyi vellerosus Honduras AMNH 0 1 Ateles geoffroyi vellerosus Mexico AMNH 5 3 FMNH 4 1 NMNH 1 8 Ateles geoffroyi yucatanensis Guatemala NMNH 1 2 Mexico NMNH 0 1

*Museum Names: AMNH – American Museum of Natural History; CMNH – Cleveland Museum of Natural History; FMNH – Field Museum of Natural History; MCZ – Museum of Comparative Zoology; NMNH – National Museum of Natural History; TP – Tappen Collection (Housed at the University of Minnesota)

316

APPENDIX B

HYPOTHESIS 1a: ANOVA TABLES

Stage 1, Hypothesis 1a: Mandibular First Molars * 2 Species M1 Source df SSQ MSQ FP Si G. gorilla BL Side 1 0.00121070 0.00121070 1903.15 <.0001 Individual 142 0.00000000 0.00000000 0.00 1 I x S 142 0.05771181 0.00040642 638.87 <.0001 0.00013526 Error 572 0.00036388 0.00000064 P. BL Side 1 0.00587644 0.00587644 832.04 <.0001 troglodytes Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.09600479 0.00141184 199.90 <.0001 0.00046826 Error 276 0.00194931 0.00000706 H. lar BL Side 1 0.00026778 0.00026778 69.89 <.0001 Individual 125 0.00000000 0.00000000 0.00 1 I x S 125 0.04456858 0.00035655 93.06 <.0001 0.00011757 Error 504 0.00193108 0.00000383 M. mulatta BL Side 1 0.00001621 0.00001621 7.35 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.00268015 0.00003941 17.88 <.0001 0.00001240 Error 276 0.00060839 0.00000220 P. anubis BL Side 1 0.00002728 0.00002728 16.11 <.0001 Individual 98 0.00000000 0.00000000 0.00 1 I x S 98 0.00702976 0.00007173 42.36 <.0001 0.00002335 Error 396 0.00067058 0.00000169 continued

317

Stage 1, Hypothesis 1a: Mandibular First Molars, continued

G. gorilla MD Side 1 0.00150404 0.00150404 121.03 <.0001 Individual 143 0.00000000 0.00000000 0.00 1 I x S 143 0.10385006 0.00072622 58.44 <.0001 0.00023793 Error 576 0.00715809 0.00001243 P. MD Side 1 0.00629291 0.00629291 8865.62 <.0001 troglodytes Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.13268131 0.00195120 2748.90 <.0001 0.00065016 Error 276 0.00019591 0.00000071 H. lar MD Side 1 0.00000005 0.00000005 0.02 <.0001 Individual 127 0.00000000 0.00000000 0.00 1 I x S 127 0.00351012 0.00002764 13.38 <.0001 0.00000852 Error 512 0.00105730 0.00000207 M. mulatta MD Side 1 0.00002974 0.00002974 22.15 <.0001 Individual 70 0.00000000 0.00000000 0.00 1 I x S 70 0.00092649 0.00001324 9.86 <.0001 0.00000397 Error 284 0.00038139 0.00000134 P. anubis MD Side 1 0.00004659 0.00004659 47.73 <.0001 Individual 98 0.00000000 0.00000000 0.00 1 I x S 98 0.01836662 0.00018741 192.00 <.0001 0.00006214 Error 396 0.00038655 0.00000098 G. gorilla CA Side 1 0.00269590 0.00269590 8.18 <.0001 Individual 141 0.00000000 0.00000000 0.00 1 I x S 141 0.32957133 0.00233739 7.09 <.0001 0.00068147 Error 566 0.18715241 0.00032949

P. CA Side 1 0.02600711 0.02600711 12373.00 <.0001 troglodytes

Individual 67 0.00000000 0.00000000 0.00 1 I x S 67 0.20000106 0.00298509 1420.18 <.0001 0.00099433 Error 272 0.00057172 0.00000210 H. lar CA Side 1 0.00013023 0.00013023 9.13 <.0001 Individual 122 0.00000000 0.00000000 0.00 1 I x S 122 0.04744531 0.00038890 27.27 <.0001 0.00012488 Error 492 0.00701571 0.00001426 continued

318

Stage 1, Hypothesis 1a: Mandibular First Molars, continued

M. mulatta CA Side 1 0.00011049 0.00011049 38.20 <.0001 Individual 67 0.00000000 0.00000000 0.00 1 I x S 67 0.00325018 0.00004851 16.77 <.0001 0.00001521 Error 272 0.00078684 0.00000289 P. anubis CA Side 1 0.00000424 0.00000424 1.49 <.0001 Individual 96 0.00000000 0.00000000 0.00 1 I x S 96 0.01738968 0.00018114 63.91 <.0001 0.00005944 Error 388 0.00109974 0.00000283

*BL = Bucco-lingual Dimension of M1; MD = Mesio-distal Dimension of M1; and CA= Crown Area of M1

Stage 1, Hypothesis 1a: Maxillary First Molars 1* 2 Species M Source df SSQ MSQ FP Si G. gorilla BL Side 1 0.00050782 0.00050782 888.72 <.0001 Individual 142 0.00000000 0.00000000 0.00 1 I x S 142 0.0716626 0.00050467 883.72 <.0001 0.00016803 Error 572 0.00032684 0.00000057

P. BL Side 1 0.00403839 0.00403839 4592.48 <.0001 troglodytes

Individual 71 0.00000000 0.00000000 0.00 1 I x S 71 0.07357688 0.00103629 1178.48 <.0001 0.00034514 Error 288 0.00025325 0.00000088

A. geoffroyi BL Side 1 0.00009855 0.00009855 23.53 <.0001

Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.00301237 0.00007531 17.98 <.0001 0.00002371 Error 164 0.00068695 0.00000419 G. gorilla MD Side 1 0.00133316 0.00133316 28.62 <.0001 Individual 144 0.00000000 0.00000000 0.00 1 I x S 144 0.08648681 0.00600600 12.90 <.0001 0.00018468 Error 580 0.02701303 0.00004657 continued

319

Stage 1, Hypothesis 1a: Maxillary First Molars, continued P. MD Side 1 0.00001908 0.00001908 22.67 <.0001 troglodytes

Individual 73 0.00000000 0.00000000 0.00 1 I x S 73 0.04982792 0.00068257 810.95 <.0001 0.00022724 Error 296 0.00024914 0.00000084

A. geoffroyi MD Side 1 0.00000147 0.00000147 0.24 <.0001

Individual 42 0.00000000 0.00000000 0.00 1 I x S 42 0.00299595 0.00007133 11.81 <.0001 0.00002176 Error 172 0.00103855 0.00000604 G. gorilla CA Side 1 0.00084619 0.00084619 17.33 <.0001 Individual 141 0.00000000 0.00000000 0.00 1 I x S 141 0.11646704 0.00082601 16.91 <.0001 0.00025906 Error 568 0.0277413 0.00004884

P. CA Side 1 0.00475827 0.00475827 2762.74 <.0001 troglodytes

Individual 71 0.00000000 0.00000000 0.00 1 I x S 71 0.12322058 0.00173550 1007.66 <.0001 0.00057793 Error 288 0.00049602 0.00000172

A. geoffroyi CA Side 1 0.00010985 0.00010985 11.78 <.0001

Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.0060209 0.00015052 16.14 <.0001 0.00004707 Error 164 0.00152925 0.00000932

*BL = Bucco-lingual Dimension of M1; MD = Mesio-distal Dimension of M1; and CA= Crown Area of M1

320

Stage 2, Hypothesis 1a: Mandibular First Molars * 2 Species M1 Source df SSQ MSQ FP Si G. gorilla BL Side 1 0.00095782 0.00095782 1526.56 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.03255749 0.00047879 763.08 <.0001 0.00015939 Error 276 0.00017317 0.00000063 P. BL Side 1 0.00587644 0.00587644 832.04 <.0001 troglodytes Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.09600479 0.00141184 199.90 <.0001 0.00046826 Error 276 0.00194931 0.00000706 H. lar BL Side 1 0.00021635 0.00021635 57.79 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.01278247 0.00018798 50.21 <.0001 0.00006141 Error 276 0.00103330 0.00000374 M. mulatta BL Side 1 0.00001621 0.00001621 7.35 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.00268015 0.00003941 17.88 <.0001 0.00001240 Error 276 0.00060839 0.00000220 P. anubis BL Side 1 0.00000787 0.00000787 4.78 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.00370225 0.00005444 33.04 <.0001 0.00001760 Error 276 0.00045478 0.00000165 G. gorilla MD Side 1 0.00211057 0.00211057 83.83 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.08753107 0.00128722 51.13 <.0001 0.00042068 Error 276 0.00694865 0.00002518 P. MD Side 1 0.00629291 0.00629291 8865.62 <.0001 troglodytes Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.13268131 0.00195120 2748.90 <.0001 0.00065016 Error 276 0.00019591 0.00000071 H. lar MD Side 1 0.00000002 0.00000002 0.01 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.00216848 0.00003189 14.65 <.0001 0.00000990 Error 276 0.00060065 0.00000218 continued

321

Stage 2, Hypothesis 1a: Mandibular First Molars, continued

M. mulatta MD Side 1 0.00003106 0.00003106 22.81 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.00091210 0.00001341 9.85 <.0001 0.00000402 Error 276 0.00037582 0.00000136 P. anubis MD Side 1 0.00000002 0.00000002 0.02 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.00178593 0.00002666 27.23 <.0001 0.00000856 Error 272 0.00026626 0.00000098 G. gorilla CA Side 1 0.00676859 0.00676859 5728.74 <.0001 Individual 67 0.00000000 0.00000000 0.00 1 I x S 67 0.19094803 0.00284997 2412.13 <.0001 0.00094960 Error 272 0.00032137 0.00000118 P. CA Side 1 0.02600071 0.02600071 12373.00 <.0001 troglodytes Individual 67 0.00000000 0.00000000 0.00 1 I x S 67 0.20000106 0.00298509 1420.18 <.0001 0.00099433 Error 272 0.00057172 0.00000210 H. lar CA Side 1 0.00019391 0.00019391 18.66 <.0001 Individual 67 0.00000000 0.00000000 0.00 1 I x S 67 0.01315490 0.00019589 18.85 <.0001 0.00006183 Error 272 0.00282660 0.00001039 M. mulatta CA Side 1 0.00011049 0.00011049 38.20 <.0001 Individual 67 0.00000000 0.00000000 0.00 1 I x S 67 0.00325018 0.00004851 16.77 <.0001 0.00001521 Error 272 0.00078684 0.00000289 P. anubis CA Side 1 0.00000026 0.00000026 0.10 <.0001 Individual 67 0.00000000 0.00000000 0.00 1 I x S 67 0.00528994 0.00007895 30.99 <.0001 0.00002547 Error 272 0.00069309 0.00000255

*BL = Bucco-lingual Dimension of M1; MD = Mesio-distal Dimension of M1; and CA= Crown Area of M1

322

Stage 2, Hypothesis 1a: Maxillary First Molars 1* 2 Species M Source df SSQ MSQ FP Si G. gorilla BL Side 1 0.00004132 0.00004132 77.55 <.0001 Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.01285763 0.00032144 603.30 <.0001 0.00010697 Error 164 0.00008738 0.00000053 P. BL Side 1 0.00485670 0.00485670 5479.93 <.0001 troglodytes Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.05124015 0.00128100 1445.39 <.0001 0.00042640 Error 164 0.00014535 0.00000089 A. geoffroyi BL Side 1 0.00009855 0.00009855 23.53 <.0001 Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.00301237 0.00007531 17.98 <.0001 0.00002371 Error 164 0.00068695 0.00000419 G. gorilla MD Side 1 0.00003308 0.00003308 58.94 <.0001 Individual 42 0.00000000 0.00000000 0.00 1 I x S 42 0.00929197 0.00022124 394.13 <.0001 0.00007356 Error 172 0.00009655 0.00000056 P. MD Side 1 0.00017187 0.00017187 223.80 <.0001 troglodytes Individual 42 0.00000000 0.00000000 0.00 1 I x S 42 0.03492039 0.00083144 1082.68 <.0001 0.00027689 Error 172 0.00013209 0.00000077 A. geoffroyi MD Side 1 0.00000147 0.00000147 0.24 <.0001 Individual 42 0.00000000 0.00000000 0.00 1 I x S 42 0.00299595 0.00007133 11.81 <.0001 0.00002176 Error 172 0.00103855 0.00000604 G. gorilla CA Side 1 0.00015033 0.00015033 152.21 <.0001 Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.02660089 0.00066502 673.32 <.0001 0.00022134 Error 164 0.00016198 0.00000099 P. CA Side 1 0.00784175 0.00784175 4477.25 <.0001 troglodytes Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.08552400 0.00213810 1220.75 <.0001 0.00071212 Error 164 0.00028724 0.00000175 continued

323

Stage 2, Hypothesis 1a: Maxillary First Molars, continued A. geoffroyi CA Side 1 0.00010985 0.00010985 11.78 <.0001 Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.00602090 0.00015052 16.14 <.0001 0.00004707 Error 164 0.00152925 0.00000932

*BL = Bucco-lingual Dimension of M1; MD = Mesio-distal Dimension of M1; and CA= Crown Area of M1

324

APPENDIX C

HYPOTHESIS 1b: ANOVA TABLES

Hypothesis 1b: Mandibular First Molars

* 2 Species M1 Source df SSQ MSQ FP Si

G. gorilla CA Side 1 0.00146465 0.00146465 1468.50 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.01311975 0.00043732 438.47 <.0001 0.00014544 Error 124 0.00012368 0.00000100 P. troglodytes CA Side 1 0.00891802 0.00891802 4847.71 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.15153465 0.00505115 2745.74 <.0001 0.00168310 Error 124 0.00022811 0.00000184 H. lar CA Side 1 0.00000049 0.00000049 0.09 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00178966 0.00005966 10.47 <.0001 0.00001799 Error 124 0.00070648 0.00000570 H. hoolock CA Side 1 0.00001546 0.00001546 3.67 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00090807 0.00003027 7.19 <.0001 0.00000869 Error 124 0.00052229 0.00000421 C. guereza CA Side 1 0.00000873 0.00000873 1.45 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00071639 0.00002388 3.97 <.0001 0.00000596 Error 124 0.00074518 0.00000601 C. mitis CA Side 1 0.00000144 0.00000144 0.23 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00410109 0.00013670 21.49 <.0001 0.00004345 Error 124 0.00078872 0.00000636 continued

325

Hypothesis 1b: Mandibular First Molars, Continued

L. albigena CA Side 1 0.00036634 0.00036634 50.17 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00134091 0.00004470 6.12 <.0001 0.00001247 Error 124 0.00090550 0.00000730 M. mulatta CA Side 1 0.00013211 0.00013211 45.20 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00109895 0.00003663 12.53 <.0001 0.00001124 Error 124 0.00036241 0.00000292 M. nemestrina CA Side 1 0.00000234 0.00000234 0.61 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00115980 0.00003866 10.11 <.0001 0.00001161 Error 124 0.00047433 0.00000383 P. anubis CA Side 1 0.00009545 0.00009545 49.43 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00089086 0.00002970 15.38 <.0001 0.00000926 Error 124 0.00023944 0.00000193 A. geoffroyi CA Side 1 0.00096036 0.00096036 92.14 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.01185775 0.00039526 37.92 <.0001 0.00012828 Error 124 0.00128181 0.00001042 C. albifrons CA Side 1 0.00000117 0.00000117 0.23 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00140759 0.00004692 9.20 <.0001 0.00001394 Error 124 0.00063211 0.00000510 C. apella CA Side 1 0.00005280 0.00005280 4.06 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00196652 0.00006555 5.03 <.0001 0.00001751 Error 124 0.00161443 0.00001302

*CA = Crown Area of M1

326

Hypothesis 1b: Maxillary First Molars 1* 2 Species M Source df SSQ MSQ FP Si G. gorilla CA Side 1 0.00017697 0.00017697 173.44 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.02649531 0.00069724 683.33 <.0001 0.00023207 Error 156 0.00015918 0.00000102 P. troglodytes CA Side 1 0.00820806 0.00820806 4623.99 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.08515685 0.00224097 1262.45 <.0001 0.00074640 Error 156 0.00027692 0.00000178 H. lar CA Side 1 0.00000329 0.00000329 0.65 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00534419 0.00014064 27.94 <.0001 0.00004520 Error 156 0.00078522 0.00000503 H. hoolock CA Side 1 0.00006910 0.00006910 19.29 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00095951 0.00002525 7.05 <.0001 0.00000722 Error 156 0.00055893 0.00000358 C. guereza CA Side 1 0.00003310 0.00003310 0.99 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00082378 0.00002168 6.52 <.0001 0.00000612 Error 156 0.00051877 0.00000333 C. mitis CA Side 1 0.00035384 0.00035384 48.36 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00467486 0.00012302 16.82 <.0001 0.00003857 Error 156 0.00114132 0.00000732 L. albigena CA Side 1 0.00000574 0.00000574 0.99 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00226539 0.00005962 10.28 <.0001 0.00001794 Error 156 0.00090489 0.00000580 M. mulatta CA Side 1 0.00003140 0.00003140 5.00 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00334798 0.00008810 1007.66 <.0001 0.00002727 Error 156 0.00098065 0.00000629 continued

327

Hypothesis 1b: Mandibular First Molars, Continued

M. nemestrina CA Side 1 0.00002025 0.00002025 6.44 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00088690 0.00002334 7.42 <.0001 0.00000673 Error 156 0.00049053 0.00000314 P. anubis CA Side 1 0.00004884 0.00004884 26.29 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00072011 0.00001895 10.20 <.0001 0.00000570 Error 156 0.00028983 0.00000186

A. geoffroyi CA Side 1 0.00029912 0.00029912 33.62 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00449178 0.00011820 13.29 <.0001 0.00003643 Error 156 0.00138796 0.00000890

C. albifrons CA Side 1 0.00000252 0.00000252 0.17 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00147493 0.00003881 2.57 <.0001 0.00000790 Error 156 0.00235661 0.00001511

C. apella CA Side 1 0.00000001 0.00000001 0.00 <.0001 Individual 38 0.00000000 0.00000000 0.00 1 I x S 38 0.00322512 0.00008487 10.20 <.0001 0.00002457 Error 156 0.00173973 0.00001115

*CA = Crown Area of M1

328

APPENDIX D

HYPOTHESIS 2: ANOVA TABLES

* 2 Species Sex C1 Source df SSQ MSQ FP Si C. apella M BL Side 1 0.00047034 0.00047034 6.36 <.0001 Individual 102 0.00000000 0.00000000 0.00 1 I x S 102 0.02934236 0.00028767 3.89 <.0001 0.00007123 Error 412 0.03047290 0.00007397 C. apella M MD Side 1 0.00023492 0.00023492 19.41 <.0001 Individual 102 0.00000000 0.00000000 0.00 1 I x S 102 0.01277357 0.00012523 10.35 <.0001 0.00003771 Error 412 0.00498720 0.00001210 C. apella F BL Side 1 0.00082014 0.00082014 222.96 <.0001 Individual 57 0.00000000 0.00000000 0.00 1 I x S 57 0.01019181 0.00017880 48.61 <.0001 0.00005837 Error 232 0.00085339 0.00000368 C. apella F MD Side 1 0.00006254 0.00006254 12.93 <.0001 Individual 58 0.00000000 0.00000000 0.00 1 I x S 58 0.00461254 0.00007953 16.45 <.0001 0.00002490 Error 236 0.00114118 0.00000484 C. mitis M BL Side 1 0.00043300 0.00043300 234.80 <.0001 Individual 47 0.00000000 0.00000000 0.00 1 I x S 47 0.01529233 0.00032537 176.43 <.0001 0.00010784 Error 192 0.00035408 0.00000184 C. mitis M MD Side 1 0.00000203 0.00000203 0.40 <.0001 Individual 47 0.00000000 0.00000000 0.00 1 I x S 47 0.01516962 0.00032276 64.01 <.0001 0.00010591 Error 192 0.00096806 0.00000504 Continued Stage 1, Hypothesis 2: Mandibular Canines *BL = Bucco-lingual Dimension of C1 and MD = Mesio-distal Dimension of C1

329

Stage 1, Hypothesis 2: Mandibular Canines, continued C. mitis F BL Side 1 0.00009473 0.00009473 21.61 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.00374912 0.00021771 49.68 <.0001 0.00007111 Error 128 0.00056098 0.00000438 C. mitis F MD Side 1 0.00219440 0.00219440 358.77 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00814205 0.00027140 44.37 <.0001 0.00008843 Error 124 0.00075843 0.00000612 P. anubis M BL Side 1 0.00006790 0.00006790 24.11 <.0001 Individual 57 0.00000000 0.00000000 0.00 1 I x S 57 0.01287712 0.00022591 80.22 <.0001 0.00007436 Error 232 0.00065337 0.00000282 P. anubis M MD Side 1 0.00000481 0.00000481 2.08 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.00795499 0.00014205 61.55 <.0001 0.00004658 Error 228 0.00052617 0.00000231 P. anubis F BL Side 1 0.00029192 0.00029192 163.37 <.0001 Individual 33 0.00000000 0.00000000 0.00 1 I x S 33 0.00572014 0.00017334 97.01 <.0001 0.00005718 Error 136 0.00024301 0.00000179 P. anubis F MD Side 1 0.00004205 0.00004205 9.07 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.00406965 0.00013128 28.30 <.0001 0.00004221 Error 128 0.00059370 0.00000464 H. lar M BL Side 1 0.00032931 0.00032931 166.89 <.0001 Individual 70 0.00000000 0.00000000 0.00 1 I x S 70 0.09484388 0.00135491 686.64 <.0001 0.00045098 Error 284 0.00056041 0.00000197 H. lar M MD Side 1 0.00020595 0.00020595 43.44 <.0001 Individual 71 0.00000000 0.00000000 0.00 1 I x S 71 0.01785781 0.00025152 53.05 <.0001 0.00008226 Error 288 0.00136548 0.00000474 H. lar F BL Side 1 0.00080537 0.00080537 280.73 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01708113 0.00030502 106.32 <.0001 0.00010072 Error 228 0.00065411 0.00000287 continued

330

Stage 1,Hypothesis 2: Mandibular Canines continued H. lar F MD Side 1 0.00060794 0.00060794 142.99 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01114738 0.00019906 46.82 <.0001 0.00006494 Error 228 0.00096937 0.00000425 P. troglodytes M BL Side 1 0.00031442 0.00031442 3.87 <.0001 Individual 33 0.00000000 0.00000000 0.00 1 I x S 33 0.02113524 0.00064046 7.89 <.0001 0.00018642 Error 136 0.01104362 0.00008120 P. troglodytes M MD Side 1 0.00026346 0.00026346 297.00 <.0001 Individual 33 0.00000000 0.00000000 0.00 1 I x S 33 0.04885901 0.00148058 1669.09 <.0001 0.00049323 Error 136 0.00012064 0.00000089 P. troglodytes F BL Side 1 0.00024651 0.00024651 247.41 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.01859342 0.00059979 601.99 <.0001 0.00019960 Error 128 0.00012753 0.00000100 P. troglodytes F MD Side 1 0.00100756 0.00100756 1118.50 <.0001 Individual 29 0.00000000 0.00000000 0.00 1 I x S 29 0.02771268 0.00095561 1060.83 <.0001 0.00031822 Error 120 0.00010810 0.00000090 G.gorilla M BL Side 1 0.00123749 0.00123749 3351.56 <.0001 Individual 82 0.00000000 0.00000000 0.00 1 I x S 82 0.07343089 0.00089550 2425.32 <.0001 0.00029838 Error 332 0.00012258 0.00000037 G.gorilla M MD Side 1 0.00699509 0.00699509 119.83 <.0001 Individual 82 0.00000000 0.00000000 0.00 1 I x S 82 0.10417368 0.00127041 21.76 <.0001 0.00040401 Error 332 0.01938071 0.00005838 G.gorilla F BL Side 1 0.00002149 0.00002149 35.95 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.02537376 0.00045310 758.09 <.0001 0.00015083 Error 228 0.00013627 0.00000060 G.gorilla F MD Side 1 0.00516867 0.00516867 5312.44 <.0001 Individual 57 0.00000000 0.00000000 0.00 1 I x S 57 0.04754295 0.00083409 857.29 <.0001 0.00027707 Error 232 0.00022572 0.00000097

331

1* 2 Species Sex C Source df SSQ MSQ FP Si C. apella M BL Side 1 0.00007405 0.00007405 0.47 <.0001 Individual 93 0.00000000 0.00000000 0.00 1 I x S 93 0.03938964 0.00042354 2.68 <.0001 0.00008855 Error 376 0.05936278 0.00015788 C. apella M MD Side 1 0.00001358 0.00001358 4.25 <.0001 Individual 93 0.00000000 0.00000000 0.00 1 I x S 93 0.00839822 0.00009030 28.28 <.0001 0.00002904 Error 376 0.00120071 0.00000319 C. apella F BL Side 1 0.00003462 0.00003462 7.44 <.0001 Individual 59 0.00000000 0.00000000 0.00 1 I x S 59 0.00703797 0.00011929 25.65 <.0001 0.00003821 Error 240 0.00111628 0.00000465 C. apella F MD Side 1 0.00016512 0.00016512 4.41 <.0001 Individual 59 0.00000000 0.00000000 0.00 1 I x S 59 0.00819345 0.00013887 3.71 <.0001 0.00003381 Error 240 0.00898984 0.00003746 C. mitis M BL Side 1 0.00036097 0.00036097 137.01 <.0001 Individual 41 0.00000000 0.00000000 0.00 1 I x S 41 0.01026585 0.00025039 95.03 <.0001 0.00008259 Error 168 0.00044263 0.00000263 C. mitis M MD Side 1 0.00020900 0.00020900 117.27 <.0001 Individual 46 0.00000000 0.00000000 0.00 1 I x S 46 0.01635991 0.00035565 199.56 <.0001 0.00011796 Error 188 0.00033506 0.00000178 C. mitis F BL Side 1 0.00039980 0.00039980 4.03 <.0001 Individual 37 0.00000000 0.00000000 0.00 1 I x S 37 0.01308300 0.00035359 3.56 <.0001 0.00008476 Error 152 0.01509629 0.00009932 C. mitis F MD Side 1 0.00121670 0.00121670 369.00 <.0001 Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.01066189 0.00026655 76.15 <.0001 0.00008768 Error 164 0.00057408 0.00000350 P. anubis M BL Side 1 0.00003783 0.00003783 38.27 <.0001 Individual 64 0.00000000 0.00000000 0.00 1 I x S 64 0.01462606 0.00022853 231.18 <.0001 0.00007585 Error 260 0.00025702 0.00000099 Continued Stage 1, Hypothesis 2: Maxillary Canines *BL = Bucco-lingual Dimension of C1 and MD = Mesio-distal Dimension of C1

332

Stage 1, Hypothesis 2: Maxillary Canines, continued P. anubis M MD Side 1 0.00001746 0.00001746 13.88 <.0001 Individual 63 0.00000000 0.00000000 0.00 1 I x S 63 0.01402594 0.00022263 176.99 <.0001 0.00007379 Error 256 0.00032201 0.00000126 P. anubis F BL Side 1 0.00000029 0.00000029 0.15 <.0001 Individual 34 0.00000000 0.00000000 0.00 1 I x S 34 0.00186494 0.00005485 28.26 <.0001 0.00001764 Error 140 0.00027178 0.00000194 P. anubis F MD Side 1 0.00003417 0.00003417 16.92 <.0001 Individual 34 0.00000000 0.00000000 0.00 1 I x S 34 0.00308549 0.00009075 44.93 <.0001 0.00002958 Error 140 0.00028275 0.00000202 H. lar M BL Side 1 0.00000001 0.00000001 0.01 <.0001 Individual 69 0.00000000 0.00000000 0.00 1 I x S 69 0.01699550 0.00015507 71.31 <.0001 0.00005097 Error 280 0.00060891 0.00000217 H. lar M MD Side 1 0.00118055 0.00118055 481.24 <.0001 Individual 68 0.00000000 0.00000000 0.00 1 I x S 68 0.01703660 0.00025054 102.13 <.0001 0.00008270 Error 276 0.00067707 0.00000245 H. lar F BL Side 1 0.00007187 0.00007187 20.71 <.0001 Individual 51 0.00000000 0.00000000 0.00 1 I x S 51 0.00921323 0.00018065 52.05 <.0001 0.00005906 Error 208 0.00072197 0.00000347 H. lar F MD Side 1 0.00036967 0.00036967 134.89 <.0001 Individual 51 0.00000000 0.00000000 0.00 1 I x S 51 0.01220559 0.00023933 87.33 <.0001 0.00007886 Error 208 0.00057004 0.00000274 P. troglodytes M BL Side 1 0.00030030 0.00030030 448.07 <.0001 Individual 36 0.00000000 0.00000000 0.00 1 I x S 36 0.05270624 0.00146406 2185.51 <.0001 0.00048780 Error 148 0.00009919 0.00000067 P. troglodytes M MD Side 1 0.00115048 0.00115048 469.06 <.0001 Individual 37 0.00000000 0.00000000 0.00 1 I x S 37 0.06148717 0.00166182 677.53 <.0001 0.00055312 Error 152 0.00037282 0.00000245 333

continued

Stage 1, Hypothesis 2: Maxillary Canines, continued P. troglodytes F BL Side 1 0.00003211 0.00003211 28.95 <.0001 Individual 35 0.00000000 0.00000000 0.00 1 I x S 35 0.03597534 0.00102787 926.53 <.0001 0.00034225 Error 144 0.00015975 0.00000111 P. troglodytes F MD Side 1 0.00867300 0.00867300 8128.99 <.0001 Individual 36 0.00000000 0.00000000 0.00 1 I x S 36 0.03651510 0.00101431 950.69 <.0001 0.00033775 Error 148 0.00015790 0.00000107 G.gorilla M BL Side 1 0.00013230 0.00013230 240.13 <.0001 Individual 81 0.00000000 0.00000000 0.00 1 I x S 81 0.11844399 0.00146227 2654.14 <.0001 0.00048724 Error 328 0.00018071 0.00000055 G.gorilla M MD Side 1 0.00023859 0.00023859 723.71 <.0001 Individual 85 0.00000000 0.00000000 0.00 1 I x S 85 0.03879680 0.00045643 1384.48 <.0001 0.00015203 Error 344 0.00011341 0.00000033 G.gorilla F BL Side 1 0.00606196 0.00606196 4274.11 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.05088068 0.00090858 640.62 <.0001 0.00030239 Error 228 0.00032337 0.00000142 G.gorilla F MD Side 1 0.00003865 0.00003865 59.46 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01641410 0.00029311 450.87 <.0001 0.00009749 Error 228 0.00014822 0.00000065

334

* 2 Species Sex C1 Source df SSQ MSQ FP Si A. geoffroyi M BL Side 1 0.00001017 0.00001017 1.88 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00080637 0.00005760 10.66 <.0001 0.00001740 Error 60 0.00032416 0.00000540 A. geoffroyi M MD Side 1 0.00003673 0.00003673 2.83 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00401385 0.00028670 22.07 <.0001 0.00009124 Error 60 0.00077934 0.00001299 A. geoffroyi F BL Side 1 0.00006064 0.00006064 18.54 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00067117 0.00004794 14.66 <.0001 0.00001489 Error 60 0.00019624 0.00000327 A. geoffroyi F MD Side 1 0.00020821 0.00020821 48.07 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00316202 0.00022586 52.15 <.0001 0.00007384 Error 60 0.00025987 0.00000433 C. albifrons M BL Side 1 0.00018697 0.00018697 64.06 <.0001 Individual 25 0.00000000 0.00000000 0.00 1 I x S 25 0.00369641 0.00014786 50.66 <.0001 0.00004831 Error 104 0.00030354 0.00000292 C. albifrons M MD Side 1 0.00002050 0.00002050 4.99 <.0001 Individual 27 0.00000000 0.00000000 0.00 1 I x S 27 0.00293856 0.00010884 26.47 <.0001 0.00003491 Error 112 0.00046051 0.00000411 C. albifrons F BL Side 1 0.00018724 0.00018724 48.00 <.0001 Individual 25 0.00000000 0.00000000 0.00 1 I x S 25 0.00232130 0.00009285 23.80 <.0001 0.00002965 Error 104 0.00040572 0.00000390 C. albifrons F MD Side 1 0.00009400 0.00009400 18.74 <.0001 Individual 27 0.00000000 0.00000000 0.00 1 I x S 27 0.00256408 0.00009497 18.93 <.0001 0.00002998 Error 112 0.00056178 0.00000502 Continued Stage 2, Hypothesis 2: Mandibular Canines

*BL = Bucco-lingual Dimension of C1 and MD = Mesio-distal Dimension of C1

335

Stage 2, Hypothesis 2: Mandibular Canines, continued C. apella M BL Side 1 0.00000365 0.00000365 1.33 <.0001 Individual 57 0.00000000 0.00000000 0.00 1 I x S 57 0.01160969 0.00020368 74.25 <.0001 0.00006698 Error 232 0.00063641 0.00000274 C. apella M MD Side 1 0.00061953 0.00061953 173.13 <.0001 Individual 58 0.00000000 0.00000000 0.00 1 I x S 58 0.00713499 0.00012302 34.38 <.0001 0.00003981 Error 236 0.00084449 0.00000358 C. apella F BL Side 1 0.00082014 0.00082014 222.96 <.0001 Individual 57 0.00000000 0.00000000 0.00 1 I x S 57 0.01019181 0.00017880 48.61 <.0001 0.00005837 Error 232 0.00085339 0.00000368 C. apella F MD Side 1 0.00006254 0.00006254 12.93 <.0001 Individual 58 0.00000000 0.00000000 0.00 1 I x S 58 0.00461254 0.00007953 16.45 <.0001 0.00002490 Error 236 0.00114118 0.00000484 C. cephus M BL Side 1 0.00025506 0.00025506 96.71 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00081866 0.00007442 28.22 <.0001 0.00002393 Error 48 0.00012659 0.00000264 C. cephus M MD Side 1 0.00028335 0.00028335 76.66 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00260393 0.00023672 64.04 <.0001 0.00007767 Error 48 0.00017743 0.00000370 C. cephus F BL Side 1 0.00000061 0.00000061 0.30 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00070964 0.00006451 31.66 <.0001 0.00002082 Error 48 0.00009780 0.00000204 C. cephus F MD Side 1 0.00034105 0.00034105 36.74 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00248791 0.00022617 24.37 <.0001 0.00007230 Error 48 0.00044552 0.00000928 C. mitis M BL Side 1 0.00069616 0.00069616 378.15 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.01318128 0.00042520 230.97 <.0001 0.00014106 Error 128 0.00023564 0.00000184 continued

336

Stage 2, Hypothesis 2: Mandibular Canines, continued C. mitis M MD Side 1 0.00000394 0.00000394 0.67 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.01368719 0.00045624 77.93 <.0001 0.00015013 Error 124 0.00072591 0.00000585 C. mitis F BL Side 1 0.00009473 0.00009473 21.61 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.00067491 0.00021771 49.68 <.0001 0.00007111 Error 128 0.00056098 0.00000438 C. mitis F MD Side 1 0.00219440 0.00219440 358.77 <.0001 Individual 30 0.00000000 0.00000000 0.00 1 I x S 30 0.00814205 0.00027140 44.37 <.0001 0.00008843 Error 124 0.00075843 0.00000612 C. guereza M BL Side 1 0.00000001 0.00000001 0.01 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00024176 0.00002015 14.53 <.0001 0.00000625 Error 52 0.00007208 0.00000139 C. guereza M MD Side 1 0.00011071 0.00011071 51.90 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00045592 0.00003799 17.81 <.0001 0.00001195 Error 52 0.00011093 0.00000213 C. guereza F BL Side 1 0.00000002 0.00000002 0.01 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00017695 0.00001475 8.16 <.0001 0.00000431 Error 52 0.00009401 0.00000181 C. guereza F MD Side 1 0.00006725 0.00006725 29.45 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00021064 0.00001755 7.69 <.0001 0.00000509 Error 52 0.00011874 0.00000228 L. albigena M BL Side 1 0.00010287 0.00010287 51.73 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00078910 0.00006070 30.53 <.0001 0.00001957 Error 56 0.00011135 0.00000199 L. albigena M MD Side 1 0.00000488 0.00000488 1.22 <.0001 Individual 10 0.00000000 0.00000000 0.00 1 I x S 10 0.00642395 0.00064240 160.46 <.0001 0.00021280 Error 44 0.00017616 0.00000400 continued

337

Stage 2, Hypothesis 2: Mandibular Canines, continued L. albigena F BL Side 1 0.00009802 0.00009802 25.64 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00078936 0.00006072 15.88 <.0001 0.00001897 Error 56 0.00021408 0.00000382 L. albigena F MD Side 1 0.00004997 0.00004997 7.82 <.0001 Individual 10 0.00000000 0.00000000 0.00 1 I x S 10 0.00201735 0.00020173 31.59 <.0001 0.00006511 Error 44 0.00028099 0.00000639 M. mulatta M BL Side 1 0.00001008 0.00001008 6.13 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00110842 0.00007917 48.18 <.0001 0.00002584 Error 60 0.00009860 0.00000164 M. mulatta M MD Side 1 0.00027758 0.00027758 73.93 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00172661 0.00012333 32.85 <.0001 0.00003986 Error 60 0.00022526 0.00000375 M. mulatta F BL Side 1 0.00007050 0.00007050 19.86 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00107113 0.00007651 21.55 <.0001 0.00002437 Error 60 0.00021299 0.00000355 M. mulatta F MD Side 1 0.00000312 0.00000312 0.40 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00171975 0.00012284 15.77 <.0001 0.00003835 Error 60 0.00046727 0.00000779 M. nemestrina M BL Side 1 0.00028658 0.00028658 275.92 <.0001 Individual 10 0.00000000 0.00000000 0.00 1 I x S 10 0.00086687 0.00008669 83.46 <.0001 0.00002855 Error 44 0.00004570 0.00000104 M. nemestrina M MD Side 1 0.00033951 0.00033951 138.82 <.0001 Individual 10 0.00000000 0.00000000 0.00 1 I x S 10 0.00200768 0.00020077 82.09 <.0001 0.00006608 Error 44 0.00010761 0.00000245 M. nemestrina F BL Side 1 0.00001993 0.00001993 7.38 <.0001 Individual 10 0.00000000 0.00000000 0.00 1 I x S 10 0.00073113 0.00007311 27.08 <.0001 0.00002347 Error 44 0.00011879 0.00000270 continued

338

Stage 2, Hypothesis 2: Mandibular Canines, continued M. nemestrina F MD Side 1 0.00004777 0.00004777 19.40 <.0001 Individual 10 0.00000000 0.00000000 0.00 1 I x S 10 0.00146280 0.00014628 59.39 <.0001 0.00004794 Error 44 0.00010838 0.00000246 P. anubis M BL Side 1 0.00014393 0.00014393 33.98 <.0001 Individual 33 0.00000000 0.00000000 0.00 1 I x S 33 0.00600550 0.00018198 20.40 <.0001 0.00005925 Error 136 0.00057603 0.00000424 P. anubis M MD Side 1 0.00020815 0.00020815 107.60 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.00400309 0.00012913 66.75 <.0001 0.00004240 Error 128 0.00024763 0.00000193 P. anubis F BL Side 1 0.00029192 0.00029192 163.37 <.0001 Individual 33 0.00000000 0.00000000 0.00 1 I x S 33 0.00572014 0.00017334 97.01 <.0001 0.00005718 Error 136 0.00024301 0.00000179 P. anubis F MD Side 1 0.00004205 0.00004205 9.07 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.00406965 0.00013128 28.30 <.0001 0.00004221 Error 128 0.00059370 0.00000464 H. hoolock M BL Side 1 0.00000030 0.00000030 0.14 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00059255 0.00004938 25.50 <.0001 0.00001576 Error 52 0.00010925 0.00000210 H. hoolock M MD Side 1 0.00002141 0.00002141 4.51 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00228435 0.00016317 34.41 <.0001 0.00005281 Error 60 0.00028454 0.00000474 H. hoolock F BL Side 1 0.00008618 0.00008618 68.42 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00079991 0.00006666 52.92 <.0001 0.00002180 Error 52 0.00006550 0.00000126 H. hoolock F MD Side 1 0.00000081 0.00000081 0.22 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00244750 0.00017482 47.50 <.0001 0.00005705 Error 60 0.00022082 0.00000368 continued

339

Stage 2, Hypothesis 2: Mandibular Canines, continued H. lar M BL Side 1 0.00076112 0.00076112 367.73 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.09365247 0.00167237 807.99 <.0001 0.00055677 Error 113 0.00047191 0.00000207 H. lar M MD Side 1 0.00000017 0.00000017 0.04 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01444975 0.00025803 57.90 <.0001 0.00008452 Error 228 0.00101612 0.00000446 H. lar F BL Side 1 0.00080537 0.00080537 280.73 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01708113 0.00030502 106.32 <.0001 0.00010072 Error 113 0.00065411 0.00000287 H. lar F MD Side 1 0.00060794 0.00060794 142.99 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01114738 0.00019906 46.82 <.0001 0.00006494 Error 228 0.00096937 0.00000425 P. troglodytes M BL Side 1 0.00002721 0.00002721 39.98 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.01711520 0.00055210 811.26 <.0001 0.00018381 Error 128 0.00008711 0.00000068 P. troglodytes M MD Side 1 0.00027131 0.00027131 399.22 <.0001 Individual 29 0.00000000 0.00000000 0.00 1 I x S 29 0.04850419 0.00167256 2461.05 <.0001 0.00055749 Error 120 0.00008155 0.00000068 P. troglodytes F BL Side 1 0.00024651 0.00024651 247.41 <.0001 Individual 31 0.00000000 0.00000000 0.00 1 I x S 31 0.01859342 0.00059979 601.99 <.0001 0.00019960 Error 128 0.00012753 0.00000100 P. troglodytes F MD Side 1 0.00100756 0.00100756 1118.50 <.0001 Individual 29 0.00000000 0.00000000 0.00 1 I x S 29 0.02771268 0.00095561 1060.83 <.0001 0.00031822 Error 120 0.00010810 0.00000090 G. gorilla M BL Side 1 0.00078069 0.00078069 26383.09 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.03177369 0.00056739 1917.30 <.0001 0.00018903 Error 228 0.00006747 0.00000030 continued

340

Stage 2, Hypothesis 2: Mandibular Canines, continued G. gorilla M MD Side 1 0.00590714 0.00590714 10580.40 <.0001 Individual 57 0.00000000 0.00000000 0.00 1 I x S 57 0.05881562 0.00103185 1848.17 <.0001 0.00034376 Error 232 0.00012953 0.00000056 G. gorilla F BL Side 1 0.00002149 0.00002149 35.95 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.02537376 0.00045310 758.09 <.0001 0.00015083 Error 228 0.00013627 0.00000060 G.gorilla F MD Side 1 0.00516867 0.00516867 5312.44 <.0001 Individual 57 0.00000000 0.00000000 0.00 1 I x S 57 0.04754295 0.00083409 857.29 <.0001 0.00027707 Error 232 0.00022572 0.00000097

Stage 2, Hypothesis 2: Maxillary Canines 1* 2 Species Sex C Source df SSQ MSQ FP Si A. geoffroyi M BL Side 1 0.00042208 0.00042208 114.63 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00283707 0.00021824 59.27 <.0001 0.00006605 Error 56 0.00020619 0.00000368 A. geoffroyi M MD Side 1 0.00011516 0.00011516 19.26 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00196226 0.00015094 25.24 <.0001 0.00004832 Error 56 0.00033489 0.00000598 A. geoffroyi F BL Side 1 0.00004908 0.00004908 8.32 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00221186 0.00017014 28.83 <.0001 0.00005484 Error 56 0.00033054 0.00000590 A. geoffroyi F MD Side 1 0.00001319 0.00001319 2.86 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00078145 0.00006011 13.02 <.0001 0.00001850 Error 56 0.00025854 0.00000462 Continued Stage 2, Hypothesis 2: Maxillary Canines *BL = Bucco-lingual Dimension of C1 and MD = Mesio-distal Dimension of C1

341

Stage 2, Hypothesis 2: Maxillary Canines, continued C. albifrons M BL Side 1 0.00078155 0.00078155 235.34 <.0001 Individual 27 0.00000000 0.00000000 0.00 1 I x S 27 0.00450344 0.00016679 50.22 <.0001 0.00005449 Error 112 0.00037195 0.00000332 C. albifrons M MD Side 1 0.00005549 0.00005549 12.06 <.0001 Individual 26 0.00000000 0.00000000 0.00 1 I x S 26 0.00357667 0.00013756 29.90 <.0001 0.00004432 Error 108 0.00049697 0.00000460 C. albifrons F BL Side 1 0.00008822 0.00008822 23.99 <.0001 Individual 27 0.00000000 0.00000000 0.00 1 I x S 27 0.00226979 0.00008407 22.86 <.0001 0.00002680 Error 112 0.00041186 0.00000368 C. albifrons F MD Side 1 0.00000991 0.00000991 1.63 <.0001 Individual 26 0.00000000 0.00000000 0.00 1 I x S 26 0.00222682 0.00008565 14.13 <.0001 0.00002653 Error 108 0.00065471 0.00000606 C. apella M BL Side 1 0.00022148 0.00022148 56.31 <.0001 Individual 59 0.00000000 0.00000000 0.00 1 I x S 59 0.01385433 0.00023482 59.70 <.0001 0.00007696 Error 240 0.00094398 0.00000393 C. apella M MD Side 1 0.00000766 0.00000766 2.27 <.0001 Individual 59 0.00000000 0.00000000 0.00 1 I x S 59 0.00395457 0.00006703 19.87 <.0001 0.00002122 Error 240 0.00080972 0.00000337 C. apella F BL Side 1 0.00003462 0.00003462 7.44 <.0001 Individual 59 0.00000000 0.00000000 0.00 1 I x S 59 0.00703797 0.00011929 25.65 <.0001 0.00003821 Error 240 0.00111628 0.00000465 C. apella F MD Side 1 0.00016512 0.00016512 4.41 <.0001 Individual 59 0.00000000 0.00000000 0.00 1 I x S 59 0.00819345 0.00013887 3.71 <.0001 0.00003381 Error 240 0.00898984 0.00003746 C. cephus M BL Side 1 0.00005866 0.00005866 34.75 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00150143 0.00010725 63.53 <.0001 0.00003519 Error 60 0.00010128 0.00000169 continued

342

Stage 2, Hypothesis 2: Maxillary Canines, continued C. cephus M MD Side 1 0.00024669 0.00024669 110.54 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00071902 0.00005136 23.01 <.0001 0.00001638 Error 60 0.00013390 0.00000223 C. cephus F BL Side 1 0.00001817 0.00001817 4.77 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00127373 0.00009098 23.89 <.0001 0.00002957 Error 60 0.00022846 0.00000381 C. cephus F MD Side 1 0.00009978 0.00009978 34.65 <.0001 Individual 14 0.00000000 0.00000000 0.00 1 I x S 14 0.00111330 0.00007952 27.62 <.0001 0.00002555 Error 60 0.00017277 0.00000288 C. mitis M BL Side 1 0.00036632 0.00036632 129.02 <.0001 Individual 37 0.00000000 0.00000000 0.00 1 I x S 37 0.00976521 0.00026392 93.60 <.0001 0.00087033 Error 152 0.00042858 0.00000282 C. mitis M MD Side 1 0.00024698 0.00024698 133.48 <.0001 Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.01601110 0.00040028 216.33 <.0001 0.00013281 Error 164 0.00030345 0.00000185 C. mitis F BL Side 1 0.00039980 0.00039980 4.03 <.0001 Individual 37 0.00000000 0.00000000 0.00 1 I x S 37 0.01308300 0.00035359 3.56 <.0001 0.00008476 Error 152 0.01509629 0.00009932 C. mitis F MD Side 1 0.00121670 0.00121670 369.00 <.0001 Individual 40 0.00000000 0.00000000 0.00 1 I x S 40 0.01066189 0.00026655 76.15 <.0001 0.00008768 Error 164 0.00057408 0.00000350 C. guereza M BL Side 1 0.00012688 0.00012688 43.10 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00023461 0.00002133 7.25 <.0001 0.00000613 Error 48 0.00014130 0.00000294 C. guereza M MD Side 1 0.00008113 0.00008113 75.55 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00033854 0.00003078 28.66 <.0001 0.00000990 Error 48 0.00005154 0.00000107 continued

343

Stage 2, Hypothesis 2: Maxillary Canines, continued C. guereza F BL Side 1 0.00000468 0.00000468 2.24 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00031281 0.00002844 13.61 <.0001 0.00008783 Error 48 0.00010029 0.00000209 C. guereza F MD Side 1 0.00001398 0.00001398 7.42 <.0001 Individual 11 0.00000000 0.00000000 0.00 1 I x S 11 0.00015760 0.00001433 7.61 <.0001 0.00000415 Error 48 0.00009041 0.00000188 L. albigena M BL Side 1 0.00012257 0.00012257 25.11 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00161664 0.00012436 25.47 <.0001 0.00003983 Error 56 0.00027341 0.00000488 L. albigena M MD Side 1 0.00009836 0.00009836 43.24 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00156931 0.00012072 53.07 <.0001 0.00003948 Error 56 0.00012737 0.00000227 L. albigena F BL Side 1 0.00000500 0.00000500 1.26 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00071309 0.00005485 13.84 <.0001 0.00001696 Error 56 0.00022187 0.00000396 L. albigena F MD Side 1 0.00002642 0.00002642 8.20 <.0001 Individual 13 0.00000000 0.00000000 0.00 1 I x S 13 0.00146186 0.00011245 34.90 <.0001 0.00003641 Error 56 0.00018044 0.00000322 M. mulatta M BL Side 1 0.00059281 0.00059281 187.25 <.0001 Individual 18 0.00000000 0.00000000 0.00 1 I x S 18 0.00214132 0.00011896 37.58 <.0001 0.00003860 Error 78 0.00024061 0.00000317 M. mulatta M MD Side 1 0.00151851 0.00151851 711.79 <.0001 Individual 18 0.00000000 0.00000000 0.00 1 I x S 18 0.02059462 0.00114415 536.31 <.0001 0.00038067 Error 76 0.00016214 0.00000213 M. mulatta F BL Side 1 0.00009838 0.00009838 35.91 <.0001 Individual 18 0.00000000 0.00000000 0.00 1 I x S 18 0.00181281 0.00010071 36.75 <.0001 0.00003266 Error 76 0.00020825 0.00000274 continued

344

Stage 2, Hypothesis 2: Maxillary Canines, continued M. mulatta F MD Side 1 0.00008956 0.00008956 29.84 <.0001 Individual 18 0.00000000 0.00000000 0.00 1 I x S 18 0.00602015 0.00033445 111.44 <.0001 0.00011048 Error 76 0.00022808 0.00000300 M. nemestrina M BL Side 1 0.00390364 0.00390364 4889.47 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.01268274 0.00105689 1323.81 <.0001 0.00035203 Error 52 0.00004152 0.00000080 M. nemestrina M MD Side 1 0.00111728 0.00111728 1394.34 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00250263 0.00020855 260.27 <.0001 0.00006925 Error 52 0.00004167 0.00000080 M. nemestrina F BL Side 1 0.00000904 0.00000904 3.17 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00081786 0.00006815 23.88 <.0001 0.00002177 Error 52 0.00014844 0.00000285 M. nemestrina F MD Side 1 0.00017327 0.00017327 118.27 <.0001 Individual 12 0.00000000 0.00000000 0.00 1 I x S 12 0.00209015 0.00017418 118.89 <.0001 0.00005757 Error 52 0.00007618 0.00000147 P. anubis M BL Side 1 0.00028813 0.00028813 315.33 <.0001 Individual 34 0.00000000 0.00000000 0.00 1 I x S 34 0.01154646 0.00033960 371.66 <.0001 0.00011290 Error 140 0.00013792 0.00000091 P. anubis M MD Side 1 0.00010584 0.00010584 89.45 <.0001 Individual 34 0.00000000 0.00000000 0.00 1 I x S 34 0.00854708 0.00025138 212.47 <.0001 0.00008340 Error 140 0.00016564 0.00000118 P. anubis F BL Side 1 0.00000029 0.00000029 0.15 <.0001 Individual 34 0.00000000 0.00000000 0.00 1 I x S 34 0.00186494 0.00000549 28.26 <.0001 0.00001764 Error 140 0.00027178 0.00000194 P. anubis F MD Side 1 0.00003417 0.00003417 16.92 <.0001 Individual 34 0.00000000 0.00000000 0.00 1 I x S 34 0.00308549 0.00009075 44.93 <.0001 0.00002958 Error 140 0.00028275 0.00000202 345

continued

Stage 2, Hypothesis 2: Maxillary Canines, continued H. hoolock M BL Side 1 0.00005689 0.00005689 33.85 <.0001 Individual 17 0.00000000 0.00000000 0.00 1 I x S 17 0.00131920 0.00008188 48.72 <.0001 0.00026733 Error 72 0.00012101 0.00000168 H. hoolock M MD Side 1 0.00134420 0.00134420 579.84 <.0001 Individual 15 0.00000000 0.00000000 0.00 1 I x S 15 0.00202944 0.00013530 58.36 <.0001 0.00004433 Error 64 0.00014837 0.00000232 H. hoolock F BL Side 1 0.00010819 0.00010819 62.57 <.0001 Individual 17 0.00000000 0.00000000 0.00 1 I x S 17 0.00138659 0.00008156 47.17 <.0001 0.00002661 Error 72 0.00012450 0.00000173 H. hoolock F MD Side 1 0.00078226 0.00078226 342.02 <.0001 Individual 15 0.00000000 0.00000000 0.00 1 I x S 15 0.00214937 0.00014329 62.65 <.0001 0.00004800 Error 64 0.00014638 0.00000229 H. lar M BL Side 1 0.00005301 0.00005301 23.76 <.0001 Individual 49 0.00000000 0.00000000 0.00 1 I x S 49 0.00834061 0.00017022 76.28 <.0001 0.00005997 Error 200 0.00044630 0.00000223 H. lar M MD Side 1 0.00070227 0.00070227 275.67 <.0001 Individual 51 0.00000000 0.00000000 0.00 1 I x S 51 0.01325001 0.00025980 101.98 <.0001 0.00008575 Error 208 0.00052988 0.00000255 H. lar F BL Side 1 0.00010835 0.00010835 31.74 <.0001 Individual 49 0.00000000 0.00000000 0.00 1 I x S 49 0.00841289 0.00017169 31.74 <.0001 0.00005609 Error 200 0.00068263 0.00000341 H. lar F MD Side 1 0.00036967 0.00036967 134.89 <.0001 Individual 51 0.00000000 0.00000000 0.00 1 I x S 51 0.01220559 0.00036967 87.33 <.0001 0.00007886 Error 208 0.00057004 0.00000274 P. troglodytes M BL Side 1 0.00016223 0.00016223 237.36 <.0001 Individual 35 0.00000000 0.00000000 0.00 1 I x S 35 0.05200412 0.00148583 2173.91 <.0001 0.00049505 Error 144 0.00009842 0.00000068 346

continued

Stage 2, Hypothesis 2: Maxillary Canines, continued P. troglodytes M MD Side 1 0.00139901 0.00199010 558.47 <.0001 Individual 36 0.00000000 0.00000000 0.00 1 I x S 36 0.06089911 0.00169164 675.29 <.0001 0.00056304 Error 148 0.00037075 0.00002510 P. troglodytes F BL Side 1 0.00003211 0.00003211 28.95 <.0001 Individual 35 0.00000000 0.00000000 0.00 1 I x S 35 0.03597534 0.00102787 926.53 <.0001 0.00034225 Error 144 0.00015975 0.00000111 P. troglodytes F MD Side 1 0.00867300 0.00867300 8128.99 <.0001 Individual 36 0.00000000 0.00000000 0.00 1 I x S 36 0.03651510 0.00101431 950.69 <.0001 0.00033775 Error 148 0.00015790 0.00000107 G. gorilla M BL Side 1 0.00000729 0.00000729 14.84 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.08503550 0.00151849 3090.28 <.0001 0.00050600 Error 228 0.00011203 0.00000049 G. gorilla M MD Side 1 0.00028965 0.00028965 881.22 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01656458 0.00029580 899.93 <.0001 0.00009849 Error 228 0.00007494 0.00000033 G. gorilla F BL Side 1 0.00606196 0.00606196 4274.11 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.05088068 0.00090858 640.62 <.0001 0.00030239 Error 228 0.00032337 0.00000142 G. gorilla F MD Side 1 0.00003865 0.00003865 59.46 <.0001 Individual 56 0.00000000 0.00000000 0.00 1 I x S 56 0.01641410 0.00029311 450.46 <.0001 0.00009749 Error 228 0.00014822 0.00000065

347