Patterns and Processes in the Dental Evolution of North American Plesiadapiforms and

Euprimates from the Late Paleocene and Early Eocene

DISSERTATION

Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of

Philosophy in the Graduate School of The Ohio State University

By

Naava Hadassah Schottenstein, B.S.

Graduate Program in Evolution, Ecology and Organismal Biology

The Ohio State University

2020

Dissertation Committee:

John P. Hunter, Advisor

Mark Hubbe

Bryan Carstens

Debbie Guatelli-Steinberg

Copyright by

Naava Hadassah Schottenstein

2020

Abstract

This dissertation explores the radiation of Primates during the Paleogene. The first radiation of Primates began with the plesiadapiforms near the Cretaceous-Paleogene boundary and the second radiation marked the introduction and diversification of euprimates at the beginning of the Eocene. Questions surrounding these radiations include their general patterns of evolution, rates of dental evolution, and potential influences of abiotic and biotic drivers.

I explore these questions in euprimates by presenting a study of the Tetonius-

Pseudotetonius primate lineage. Rates of evolution and the roles of neutral and adaptive processes across this lineage remain unclear. Linking Tetonius and Pseudotetonius are a series of stratigraphic and morphologic intermediates revealing possible functional and developmental reorganization within the dentition. Notable changes involved a reduction of the P3 and the P4 became a robust tall-cusped tooth. I test whether neutral evolution can explain the phenotypic differences in the lineage, and whether P4 lost developmental association with P3 and became integrated with the molars. I calculate the rate of evolutionary differentiation, based on the ratio between inter- and intra-species variation in length and width of the premolars and molars, between lineage segments and the entire lineage. I test for correlations between teeth within lineage segments. Correlations between P3 and the molars diminished, whereas correlations between P4 and the molars increased. I found evidence of varying degrees of stabilizing selection in the lengths and

ii widths of most tooth metrics and neutral evolution in P4 width. This suggests a trend towards P4 becoming integrated into the molar field and that rates of evolution and selective pressures vary through time.

The following chapters focus on the radiation of the family Paromomyidae during the late Paleocene and early Eocene. Their focus is on two paromomyid genera, Ignacius and Phenacolemur, which provide a series of long-lived lineages that experienced episodes of biotic turnover and dietary shifts.

The second chapter explores evolutionary modes and rates that produced the changes in the dentitions of Ignacius and Phenacolemur, and the influence of the biotic turnover events. I test whether directional selection can explain the morphological changes that occurred with a dietary shift and if the changes that occurred with no dietary shift is marked by stasis. A random walk was the dominant model, followed by an

Ornstein-Uhlenbeck process and strict stasis. Often, differences in tooth metrics between species are explained by neutral evolution. Dietary shifts did not always produce directional modes, and stasis was not always the best model when no dietary shift occurred.

The third chapter focuses on the Ignacius frugivorus – Phenacolemur citatus lineage and assesses whether morphological changes in the dentition can be explained by changing paleotemperatures. I compare the magnitude and timing of dental changes to the paleotemperature curve and found significant positive correlations with temperature over the entire lineage. I found positive correlations between tooth metrics during both warming periods and both positive and negative correlations during the cool period.

iii These findings suggest that paleotemperature may have played an important role in the evolution of paromomyids, but exactly how remains unclear.

iv Dedication

I dedicate this dissertation to my daughter Rose, who’s individuality and sense of self is truly inspiring to me. To my husband Michael, who always shows me patience and kindness and who’s support has helped me get through this stage of my life. To my mother, father, and sister who have been there for me always. Our yearly fishing trips to the beach provided a necessary escape to look forward to. To my Uncle Larry Grimes, who inspired me with his love of science. Visiting him and his lab at Meredith University as a young girl is one of the reasons this dissertation was ever written. To David

Goldstein, for being my first academic mentor and a friend during one of the most challenging times of my life.

v

Acknowledgements

I would foremost like to thank my advisor, John Hunter, for his encouragement, ideas, support, and patience throughout my PhD. I can’t imagine ever finding an advisor that would have been better for me. His academic guidance throughout these years has been incredibly helpful and has helped me create a body of work, of which I can be proud.

I would also like to thank Mark Hubbe for his support and time spent helping me work through so much of the statistics involved in this dissertation. The insights he provided me throughout the years was immensely helpful. I would like to thank Bryan

Carstens and Debbie Guatelli-Steinberg for agreeing to be on my committee. I learned a great deal about teeth from Debbie, and I always appreciated her kindness and encouragement. I am thankful to Bryan for the fun times teaching Evolution and

Mammalogy, and for allowing me opportunities to guest lecture and get creative in the

Mammology lab.

I would like to thank Mary Silcox for providing me with a huge portion of the data needed to make this dissertation possible. I am grateful to her for allowing me to visit her lab in Scarborough and for the hospitality and kindness she showed me during my visits.

I would like to thank Kenneth Rose and Thomas Bown for their thorough work and publications on the Tetonius – Pseudotetonius lineage, which inspired a portion of

vi this research. I thank Kenneth Rose, Johns Hopkins School of Medicine, Smithsonian

National Museum of Natural History, and the University of Michigan Museum of

Paleontology for allowing me to measure additional Tetonius – Pseudotetonius specimens housed in their collections. I also thank Will Clyde for his work and help in establishing sediment ages and correlating the sediments of the Clarks Fork and Bighorn Basins, which allowed me to estimate ages of individual Tetonius – Pseudotetonius specimens.

vii

Vita

B.S. Biological Sciences, Wright State University ...... 2014

Graduate Teaching Associate, Department of Evolution, Ecology and Organismal

Biology, The Ohio State University ...... 2014 to present

Publications

Schottenstein, N. H., Hubbe, M., Hunter, J. P. 2019. Modules and mosaics in the evolution of the Tetonius-Pseudotetonius dentition. Journal of Mammalian Evolution.

Evolution doi: 10.1007/s10914-019-09488-3

Fields of Study

Major Field: Evolution, Ecology and Organismal Biology

viii

Table of Contents

Abstract ...... ii

Dedication ...... v

Acknowledgements ...... vi

Vita ...... viii

List of Tables ...... xii

List of Figures ...... xv

Chapter 1. Modules and Mosaics in the Evolution of the Tetonius – Pseudotetonius

Dentition ...... 1

1.1 Introduction ...... 1

1.2 Materials and Methods ...... 7

1.3 Results ...... 15

1.4 Discussion ...... 22

1.5 Conclusion ...... 33

1.6 Figures ...... 36

1.7 Tables ...... 42

1.8 Literature Cited ...... 47

Chapter 2. Rates and Modes of Dental Evolution in Late Paleocene and Early Eocene

Paromomyids ...... 56

2.1 Introduction ...... 56

ix

Table of Contents Continued

2.2 Materials and Methods ...... 63

2.3 Results ...... 74

2.4 Discussion ...... 92

2.5 Conclusions ...... 115

2.6 Figures ...... 124

2.7 Tables ...... 133

2.8 Literature Cited ...... 158

Chapter 3. The Role of Climate Change on the Dental Evolution of Late Paleocene and

Early Eocene Paromomyids ...... 173

3.1 Introduction ...... 173

3.2 Materials and Methods ...... 179

3.3 Results ...... 183

3.4 Discussion ...... 189

3.5 Conclusions ...... 195

3.6 Figures ...... 196

3.7 Tables ...... 208

3.8 Literature Cited ...... 211

Chapter 4. Conclusions ...... 219

4.1 Conclusions ...... 219

x

Table of Contents Continued

Comprehensive Literature Cited ...... 222

Appendix A: Locality Information for Each Lineage Segment of the Tetonius –

Pseudotetonius Lineage ...... 249

Appendix B: Sample size, Sample Means and Variances, and Sample Ages for Ignacius and Phenacolemur Lineage Segments ...... 251

Appendix C: Estimating Body Weight and Generation Time in Fossil Primates ...... 261

C.1 Introduction ...... 261

C.2 Materials and Methods ...... 263

C.3 Results ...... 264

C.4 Discussion and Conclusions ...... 267

C.5 Figures ...... 268

C.6 Tables ...... 270

C.7 Literature Cited ...... 274

xi

List of Tables

Table 1.1 Descriptive Statistics: Tooth Lengths and Widths ...... 42

Table 1.2 Results from Bivariate Correlation for Tooth Metrics and MAT ...... 43

Table 1.3 Number of Generations Between Lineage Segments ...... 43

Table 1.4 Descriptive Statistics and U-Test Results for Clarks Fork and Bighorn Basin

Samples ...... 44

Table 1.5 Results: Evolutionary Rates ...... 45

Table 1.6 Results from Bivariate Correlation Between Tooth Metrics ...... 46

Table 2.1 List of Operational Stratigraphic Units, Sample Sizes, and Estimated Ages . 133

Table 2.2 Evolutionary Divergence for Three Models of Evolution ...... 134

Table 2.3 Estimates and Ranges for Population Genetic Parameters: I. fremontensis – I. frugivorus ...... 135

Table 2.4 Evolutionary Model-Fitting Results: I. fremontensis – I. frugivorus ...... 135

Table 2.5 Estimates and Ranges for Population Genetic Parameters: I. frugivorus – I. graybullianus ...... 137

Table 2.6 Evolutionary Model-Fitting Results: I. frugivorus – I. graybullianus ...... 138

Table 2.7 Estimates and Ranges for Population Genetic Parameters: I. frugivorus – P. pagei ...... 140

Table 2.8 Evolutionary Model-Fitting Results: I. frugivorus – P. pagei ...... 141

Table 2.9 Evolutionary Model-Fitting Results: P. pagei – P. praecox ...... 143

xii

List of Tables Continued

Table 2.10 Evolutionary Model-Fitting Results: P. praecox – P. fortior ...... 146

Table 2.11 Evolutionary Model-Fitting Results: P. fortior – P. citatus ...... 149

Table 2.12 Evolutionary Model-Fitting Results: P. praecox – P. citatus ...... 152

Table 2.13 Estimates and Ranges for Population Genetic Parameters: P. simonsi – P. willwoodensis ...... 155

Table 2.14 Evolutionary Model-Fitting Results: P. simonsi – P. willwoodensis ...... 155

Table 3.1 List of Operational Stratigraphic Units, Sample Sizes, and Mean Ages for each

Species of Ignacius and Phenacolemur ...... 208

Table 3.2 Descriptive Statistics for Tooth Metrics for the Early, Middle, and Late Periods

...... 209

Table 3.3 Results: Shapiro-Wilk Test for Tooth Metrics for the Early, Middle, and Late

Periods and the Entire Lineage ...... 209

Table 3.4 Results: Spearman’s Rho Correlation Tests for Each Tooth Metric and Mean

Annual Temperature ...... 210

Table 3.5 Body Size Changes During the Early, Middle, and Late Periods ...... 210

Table A.1 Locality Information for Each Lineage Segment (Tetonius – Pseudotetonius

Lineage) ...... 249

Table B.1 Sample Sizes, Means and Variances, and Ages for Each Tooth Loci (Ignacius and Phenacolemur) ...... 251

xiii

List of Tables Continued

Table C.1 Regression Equations, Ln Body Weight on Ln Lower First Molar Area in

Prosimian Primates ...... 270

Table C.2 Regression Equations, Ln Generation Time on Ln Body Weight in Prosimian

Primates ...... 270

Table C.3 Analysis of Variance in the Regressions of Ln Body Weight on Ln Lower First

Molar Area in Prosimian Primates ...... 271

Table C.4 Estimated Body Weights for Ignacius and Phenacolemur Species ...... 272

Table C.5 Estimated Generation Times Ignacius and Phenacolemur Species ...... 273

xiv

List of Figures

Figure 1.1 Stages of Morphological Evolution in the Lower Dentition of the Tetonius –

Pseudotetonius Lineage ...... 36

Figure 1.2 Results from Two-Sample U-tests: Lengths ...... 37

Figure 1.3 Results from Two-Sample U-tests: Widths ...... 38

Figure 1.4 Scatterplots of Log Transformed Length Measurements ...... 39

Figure 1.5 Scatterplots of Log Transformed Width Measurements ...... 40

Figure 1.6 Rates of Evolution for Tooth Lengths and Widths ...... 41

Figure 2.1 Temporal Ranges of Ignacius and Phenacolemur ...... 124

Figure 2.2 Trends in Tooth Metrics: I. fremontensis – I. frugivorus ...... 125

Figure 2.3 Trends in Tooth Metrics: I. frugivorus – I. graybullianus ...... 126

Figure 2.4 Trends in Tooth Metrics: I. frugivorus – P. pagei ...... 127

Figure 2.5 Trends in Tooth Metrics: P. pagei – P. praecox ...... 128

Figure 2.6 Trends in Tooth Metrics: P. praecox – P. fortior ...... 129

Figure 2.7 Trends in Tooth Metrics: P. fortior – P. citatus ...... 130

Figure 2.8 Trends in Tooth Metrics: P. praecox – P. citatus ...... 131

Figure 2.9 Trends in Tooth Metrics: P. simonsi – P. willwoodensis ...... 132

Figure 3.1 Temporal Ranges of North American Species of Ignacius and Phenacolemur

...... 196

Figure 3.2 Scatterplots of Tooth Metrics for the I. frugivorus – P. citatus lineage ...... 197

xv

List of Figures Continued

Figure 3.3 Scatterplots of Tooth Metrics for the Early Period of Climate Warming .... 198

Figure 3.4 Scatterplots of Tooth Metrics for the Middle Period of Climate Cooling .... 199

Figure 3.5 Scatterplots of Tooth Metrics for the Late Period of Climate Warming ...... 200

Figure 3.6 Box Plots of Tooth Metrics for the Early, Middle, and Late Periods ...... 201

Figure 3.7 Scatterplots of Tooth Metrics Versus Mean Annual Temperature: Early Period

...... 202

Figure 3.8 Scatterplots of Tooth Metrics Versus Mean Annual Temperature: Middle

Period ...... 203

Figure 3.9 Scatterplots of Tooth Metrics Versus Mean Annual Temperature: Late Period

...... 204

Figure 3.10 Scatterplots of Tooth Metrics Versus Mean Annual Temperature: Entire

Lineage ...... 205

Figure 3.11 Scatterplots of Evolutionary Size Increments Versus Mean Annual

Temperature ...... 206

Figure 3.12 Evolutionary Changes in Tooth Metrics with Respect to the Age of the

Descendant Population ...... 207

Figure C.1 Regression of Ln Body Weight on Ln M1 Size in Prosimian Primates ...... 268

Figure C.2 Regression of Ln Generation Time on Ln Body Weight in Prosimian Primates

...... 269

xvi

Chapter 1: Modules and Mosaics in the Evolution of the Tetonius – Pseudotetonius

Dentition

1.1 Introduction

The Tetonius – Pseudotetonius Lineage

Ancestor-descendant relationships that are documented by a continuous series of transitional or intermediate fossil forms are rare in the fossil record (but see Foote 1996).

This rarity increases as the age of the fossil record increases. When such a complete record is available, it provides a unique opportunity to study evolution on a timescale of tens or hundreds of thousands of years instead of millions of years. The Eocene fossil record in the Willwood Formation of the Bighorn Basin in Wyoming provides such a record and showcases several plant and animal evolutionary transitions (Gingerich 1980a;

Bown et al. 1994b; Clyde et al. 1994; Clyde and Gingerich 1994; Gingerich and Gunnell

1995). Among these are several primate lineages that appear at the beginning of the

Eocene, at the base of the Willwood Formation.

This article focuses on a single lineage of Eocene primates from the Willwood

Formation, the Tetonius-Pseudotetonius (T-P) lineage. Taxonomically, the T-P lineage represents a group of Eocene omomyiform primates that are basal members of the

Anaptomorphinae within the fossil primate family Omomyidae, which also includes the

Omomyinae (Szalay and Delson 1979; Gunnell and Rose 2002; Gebo et al. 2012).

Omomyidae is one of three haplorrhine families included within Tarsiiformes, the other

1 two families being Microchoeridae and Tarsiidae (Szalay and Delson 1979; Gunnell and

Rose 2002; Gebo et al. 2012). The taxonomic framework used here follows that of Szalay and Delson (1979) and Gunnell and Rose (2002) except for Microchoeridae being raised to the level of family. Along with adapiforms, omomyiforms are considered the most primitive members of the crown primate clade (Morse et al. 2019). Omomyiforms were small primates weighing around 500g or less, mostly thought to have been frugivorous, nocturnal based on the large size of their orbits, and resembled modern tarsiers (Simpson

1940; Szalay 1976; Szalay and Delson 1979; Gingerich 1981; Beard et al. 1991; Strait

1991, 2001; Covert 1997; Ross et al. 1998; Dagosto et al. 1999; Ross 2000; Ross and

Covert 2000; Ni et al. 2004; Rose 2006; Gunnell et al. 2008). As such, there is phylogenetic support for omomyiforms being closely related to extant tarsiers (Seiffert et al. 2009).

Omomyiforms have been extensively studied since originally described by

Trouessart in 1879. However, most studies have focused on systematics and phylogenetic relationships of omomyiforms (Tornow 2008; Gunnell et al. 2008), on the evolutionary relationships between omomyiforms and other primate families (Bown and Rose 1987;

Bloch et al. 2007; Silcox et al. 2008; Seiffert et al. 2009; Williams et al. 2010), or adaptations in cranial and post cranial morphology (Bown and Rose 1987; Dagosto and

Schmid 1996; Gebo et al. 2012).

The T-P lineage, experienced several changes in their dental morphology throughout the Eocene, including the development of lower crowned and more robust molars, as well as facial shortening (Bown and Rose 1987). The dental adaptations that

2 the T-P lineage underwent resulted in an evolutionary transition from genus Tetonius to a new genus, Pseudotetonius. This genus-level transition is marked by the evolution of a compact dentition in a short jaw with varying degrees of tooth reduction between the prominent central incisors and the cheek teeth (I2, C, P3, Fig. 1.1). The sample documenting the transition from Tetonius to Pseudotetonius for the upper antemolar dentition is smaller than that of the lower dentition, and P4-M3 size and morphology remain relatively conserved throughout the series (Bown and Rose 1987; Rose 1995).

However, the dental adaptations of the lower dentition make this group an excellent model to study evolutionary trends.

The bulk of the T-P fossil record consists of individual teeth and jaw fragments, which offer detailed documentation of dental evolution in this Eocene primate. This study focuses on the reduction in size of P3 and its morphological transition to becoming similar in size and shape to the I2 and C, and on the increase in the size of P4 and its transition to a larger, tall cusped tooth. I use third and fourth premolars and first and second molars (P3, P4, M1, and M2) to quantify dental patterns because of the large morphological changes observed in P3 and P4 relative to that of the M1 and M2. These cheek teeth also comprise most of the sample on record for the taxa, with too few I2, P2, or M3 teeth to include in the current study.

The most notable analysis on the T-P lineage to date was done by Bown and Rose

(1987), who suggested that the morphological changes observed in the lower dentition of the T-P lineage was the result of gradual evolution. They used dental characters to suggest a mode of evolutionary diversification within multiple lineages of omomyid

3 primates. The study presented here aims to add to the work done on the T-P lineage, by using quantitative methods to investigate patterns of dental integration among teeth and establish rates of morphological evolution within the posterior dentition. No studies to date have attempted to identify shifting correlations among cheek teeth within the dentition or to quantify rates of morphological evolution in individual teeth within the T-

P lineage. Therefore, it is still unclear as to what evolutionary processes shaped the dentition of this lineage or why the P3 and P4 would evolve along different trajectories.

The robustness of the T-P lineage’s fossil record provides enough data to analyze trends in dental morphology through time. Analyses that address questions about the evolutionary process, like those undertaken here, improve our understanding of how the earliest members of the primate order evolved. Additionally, applying statistical analyses to fossil records, like that of the T-P lineage’s, make it possible to discern how different evolutionary forces, such as directional selection, stabilizing selection, and neutral evolution acted during different phases of a morphological evolutionary transition. I test the following two hypotheses: (1) neutral evolution can explain the phenotypic differences observed in tooth size across the T-P lineage; (2) P4 loses a developmental association with P3 and comes under the control of the molar field.

Given that the T-P lineage’s transition is an often-cited example of phyletic gradualism (Rose and Bown 1984, 1986; Bown and Rose 1987; Hunter 1999), I anticipate that morphological rates of evolution will vary through time but will deviate intermittently from the neutral expectation. This expectation contrasts with the bimodal distribution of evolutionary rates that I would expect from a lineage that evolved under

4 punctuated equilibrium. Furthermore, my study may explain how differential trends of dental morphological evolution occurred in the lineage, by suggesting that the premolars lost developmental integration as each tooth was coopted by the neighboring developmental fields (canine and molar fields, respectively). I expect that P3 and P4 dimensions became less correlated with each other, and P4 showed increased correlations with the molar dimensions through time.

Biohorizons and Paleotemperature of the Bighorn Basin

The extensive research done on the lower Eocene Willwood Formation of the

Bighorn Basin allows us to provide a paleoecological context to my study that will aid in our understanding of the potential ecological influences that affected the evolution of the

T-P lineage. Research in the Bighorn Basin has resulted in a dense record of Paleogene mammals and a detailed record of their stratigraphic ranges (Gingerich 1980a; Bown et al. 1994b). Analyses on Willwood mammalian biostratigraphy have resolved multiple biostratigraphic zones between events of faunal turnover, marked by species appearance and disappearance (Schankler 1980; Chew 2009). Schankler (1980) termed these faunal turnover events biohorizons A, B, and C, of which he found there to be three distinct events. There is some debate on the validity (Badgley and Gingerich 1988) and the number of biohorizons (Chew 2009). For instance, Badgley and Gingerich (1988) suggested that the definition of Biohorizon A was the product of small sample sizes, and as such may not be reliable. Chew (2009) used a much larger sample of Willwood mammals than was available to Schankler (1980) and found support for biohorizons A and B but could not substantiate the increased appearance rate for Shankler’s Biohorizon

5 C. Chew (2009) found Biohorizon A to span from approximately 55.1 – 54.8 Ma and

Biohorizon B to span from approximately 54.2 – 54.0 Ma. Both biohorizons A and B from Schankler (1980) are within the respective meter levels for biohorizons A and B proposed by Chew (2009). Chew (2009) found the earliest individuals of the T-P lineage,

Tetonius matthewi, to have disappeared in the central Bighorn Basin near the beginning of Biohorizon A (~ 55.2 – 55.1 Ma). The Tetonius matthewi – Pseudotetonius ambiguus intermediates appeared during Biohorizon A around approximately 55.06 – 55.04 Ma and

Pseudotetonius ambiguus appeared after Biohorizon A around 54.9 Ma (Chew 2009).

Many authors have discussed possible relationships between the biohorizon turnover events and climate change in the Bighorn Basin (Schankler 1980; Bown and

Kraus 1993; Bown et al. 1994a; Bao et al. 1999; Wing et al. 2000; Lourens et al. 2005;

Clyde et al. 2007; Chew 2009). Specifically, there is evidence of a relationship between the onset of cooling at the beginning of Biohorizon A and a return to warmer temperatures that corresponds with Biohorizon B (Bao et al. 1999; Wing et al. 2000;

Chew 2009).

A combination of climate reconstructions using leaf margins and oxygen isotope ratios of hematitic soil nodules in the Bighorn Basin throughout the early Eocene document a quick transition from relatively warm temperatures (mean annual temperatures [MAT] ~15-18°C) before Biohorizon A to cool temperatures that declined rapidly near the beginning of Biohorizon A (Wing 1998; Bao et al. 1999; Chew 2009;

Wing et al. 1991, 2000, 2005). Temperatures dropped as low as 10°C between

6 biohorizons A and B, before returning to warmer temperatures after Biohorizon B (Wing

1998; Bao et al. 1999; Chew 2009; Wing et al. 1991, 2000, 2005).

1.2 Materials and Methods

The Evolutionary Series

The fossil record of the T-P lineage has fine temporal and stratigraphic resolution within the lower Eocene Willwood Formation of the Bighorn and Clarks Fork Basins,

Wyoming, and occur within the Wasatchian land-mammal age (55.8 and 52.6 Ma.). The lineage consists of two defined species, Tetonius matthewi and Pseudotetonius ambiguus, at the beginning and end of the lineage, respectively, linked by a detailed record of intermediate stages (Fig. 1.1). The diagnoses of these species were established by Bown and Rose (1987) based largely on premolar and molar morphology. Intermediate stages were classified by Bown and Rose (1987) based on shared combinations of derived and ancestral traits.

The Data

Linear measurements (maximum length and maximum width) of the P3, P4, M1, and M2 teeth from 182 specimens were obtained from Bown and Rose (1987), which represents the majority of the published specimens. Bown and Rose (1987) reported these data from the T-P lineage and other anaptomorphine primates from the central Bighorn and Clarks Fork basins in the collections of the University of Michigan Museum of

Paleontology, Ann Arbor, Michigan (UMMP); United States Geological Survey, Denver,

Colorado (USGS); United States National Museum, Washington, D.C. (USNM); Yale

Peabody Museum of Natural History, New Haven, Connecticut (YPM), as well as a few

7 smaller collections (see Bown and Rose 1987). Fifteen additional previously unpublished specimens were measured using the same methods reported by Bown and Rose (1987) by me. I was allowed access to these additional specimens by Kenneth Rose at Johns

Hopkins School of Medicine, the Smithsonian National Museum of Natural History, and the University of Michigan Museum of Paleontology. Measurements of the incisors, canines, P2 and M3 were not reported in Bown and Rose (1987) and P2 was not present in some intermediate stages or Pseudotetonius ambiguus, so these teeth were not included in my analysis.

Stratigraphy

The stratigraphic association of each specimen was obtained based on 49

Willwood Formation fossil localities (32 from the central Bighorn Basin stratigraphic sections, 17 from the Clarks Fork Basin stratigraphic sections that are in the northern

Bighorn Basin). Bown and Rose (1987) were unable to chronostratigraphically correlate the sections from the Clarks Fork Basin in the northern Bighorn Basin to the sections in the central Bighorn Basin because of differing sediment thickness, varying accumulation rates between the Bighorn and Clarks Fork basins, and incomplete paleomagnetic data

(Bown and Kraus 1993; Bown et al. 1994b; Clyde et al. 1994, 2007; Tauxe et al. 1994;

Chew 2005). However, since the publication of Bown and Rose (1987), issues tying the two basins together have largely been resolved and headway has been made in the correlation of several disparate parts of the Bighorn Basin (Bown et al. 1994b; Clyde et al. 1994; Tauxe et al. 1994; Chew 2005). Sediment accumulation rates, meter levels, and their corresponding biochrons were provided to the authors by William Clyde and were

8 based on several works (Gradstein et al. 2012; Butler et al. 1981; Bown and Rose 1987;

Bown et al. 1994b; Tauxe et al 1994; Hamzi 2003). The ability to correlate the two basins allowed us to combine data from both the Bighorn and Clarks Fork basins together in the same analyses, which increased sample sizes. A large sample size is essential in the evolutionary rate estimation approach, which depends on reliable estimates of variance within and between species.

Addressing Potential Taphonomic Issues in Study Design

The central Bighorn and Clarks Fork basins differ in sampling area, sedimentation rate, and paleosol structure and age, which may create biases in the fossil record (Clyde et al. 2005; Chew and Oheim 2009). The Clarks Fork Basin section has sediment accumulation rates that are greater than those in the central Bighorn Basin, which results in less mature paleosols in the Clarks Bighorn Basin (Clyde et al. 2007). Previous studies have shown that more mature paleosols preserve smaller species, or smaller individuals of the same species, in greater proportion than those from less mature paleosols (Bown and Beard 1990; Clyde et al. 2005). Thus, I would expect individuals from the central

Bighorn Basin to be smaller than those from Clarks Fork Basin. To address the issue of potential taphonomic bias influencing the results of the rate study, I performed U-tests on tooth length and width for each tooth loci to test for differences between Clarks Fork and

Bighorn Basin individuals.

Age Estimates

Correlating both the Clarks Fork and central Bighorn Basin sections was important for the robustness of the combined sample. However, to estimate rates of

9 morphological change, which is calculated as a ratio of morphological variance within and between species over time, I needed to establish ages for individual samples collected from localities within the two basins. This allowed us to estimate time between samples that could then be divided by an estimate of the number of generations separating populations in the T-P lineage. Extensive stratigraphic and paleomagnetic research in the

Bighorn Basin has made it possible to interpolate the ages from both the Clarks Fork and the central Bighorn Basin sections (Butler et al. 1981; Clyde et al. 1994, 2001, 2007;

Bown et al. 1994b; Tauxe et al. 1994; Clyde 1997, 2001; Wing et al. 2000; Gingerich

2001; Chew 2005; Secord et al. 2006), allowing their inclusion in the same analyses in this current study. Locality information including basin and meter level for each specimen was obtained from Bown and Rose (1987) to estimate the age of individual specimens (Appendix A, Table A.1).

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Establishment of Operational Taxonomic Units (OTUs)

Sample size at each locality was relatively small. Additionally, many specimens were classified as intermediates by Bown and Rose (1987) but were not assigned to a particular intermediate stage. As such, grouping specimens into end members and intermediate stages would further reduce sample sizes needed for the analyses. To avoid the issue of potentially small sample size at any stage of the lineage, the specimens were 10 grouped into four chronologically non-overlapping operational taxonomic units (OTUs)

(Appendix A, Table A.1). Mann-Whitney U-tests were used to test if specimens from different adjacent sediment layers within each OTU differed significantly in size. If they did not differ significantly in size, they would be grouped into the same OTU. Individuals from subsequent adjacent meter levels would then be compared to the group of individuals from all meter levels before it. When sample size from a meter level was too small to perform a U-test, those specimens would be included if all tooth measurements fell within two standard deviations from the means of the OTU group it was being compared to. Divisions between OTUs were made where individuals from adjacent meter levels differed significantly in size. In only five comparison (out of 33) were specimens significantly different (p < 0.05), initially creating six OTUs before outliers were removed.

After combining the specimens into OTUs, 26 outliers were identified and removed from the sample to limit the possibility of including potentially misidentified specimens into the analyses. An entire specimen was removed if one or more of the teeth in the jaw of that individual was an outlier to the OTU, due to the inability to infer the correct affinity of the individual to its assigned OTU. Consequently, I present here a conservative analysis in terms of morphological variance within OTUs, choosing to prioritize internal morphological consistency over morphological variance in each OTU.

Mann-Whitney U-tests were repeated to determine if significant differences remained in tooth length and width between adjacent OTUs after outliers were removed. Two of the six OTUs showed no significant differences from an adjacent OTU and were combined.

11 This resulted in four distinct OTUs (named, from oldest to youngest, OTU A, B, C, and

D), supporting the general assumption that the OTUs used represent internally consistent morphological units (Figs. 1.2 and 1.3). OTU A includes specimens that Bown and Rose

(1987) classified as stage 1 individuals of the genus Tetonius, OTU B includes specimens classified as stage 1 and intermediate stage 2, OTU C includes intermediate stage 2 and stage 3 individuals, and OTU D includes individuals classified as advanced stage 2, stage

3, and stages 4 and 5 of the genus Pseudotetonius. OTU ages were obtained by averaging the ages of all localities included within a designated OTU (Appendix A, Table A.1).

The time period under study has an average range from 55.52 Ma at OTU A to

54.56 Ma at OTU D; however, specimens are found from localities that range from 55.71

– 54.32 Ma (Appendix A, Table A.1). This places specimens from OTU A and OTU B before Biohorizon A when local MATs were warm (Wing et al. 1991, 2000, 2005), OTU

C specimens are contemporaneous with Biohorizon A and the onset of cooling, while

OTU D specimens are dated to between biohorizons A and B where MAT reached as low as 10 °C (Wing et al. 1991, 2000, 2005) and are present until the beginning of Biohorizon

B when warmer temperatures began to rise again (Figs. 1.4 and 1.5). The entire time series, from OTU A to OTU D, spans a period of 963,626 years.

Trends in Tooth Dimensions

Mean length and width of individual teeth for each OTU were calculated to establish overall patterns and evolutionary trends in tooth size throughout the lineage

(Table 1.1). U-tests were performed for the lengths and widths (Figs. 1.2 and 1.3, respectively) of each tooth between adjacent OTUs (A to B, B to C, and C to D) and

12 between the end members of the lineage (OTU A and OTU D) to see where significant differences in tooth dimensions exist. For each tooth position, scatterplots of the lengths and widths and their means for each OTU were created to show how tooth size evolved over time (Figs. 1.4 and 1.5).

Paleotemperature and Biohorizon A

Patterns of tooth length and width throughout the lineage were compared to changes in MAT and the timing of Biohorizon A (Figs. 1.4 and 1.5). I used Pearson

Product-Moment Correlation tests to compare changes in tooth length and width to changes in MAT (Table 1.2), and I visually compared changes in tooth length and width to the timing and duration of Biohorizon A. For the visual comparison between tooth dimension and Biohorizon A, measurements for all cheek teeth were transformed to their natural log and plotted in a scatterplot with the timing and duration of Biohorizon A superimposed. Mean annual temperature was obtained from previous studies that used data obtained from leaf margin analysis in the Bighorn Basin throughout the early Eocene

(Wing et al. 1991, 2000, 2005), and the zonation of Biohorizon A was obtained from

Schankler (1980) and Chew (2009).

Evolutionary Rates

To test the first hypothesis, that dental morphology of the lineage evolved neutrally with respect to natural selection, I calculated the rate of morphological evolution proposed by Lynch (1990). Lynch (1990) introduced a rate statistic, based on population-genetic theory that is conceptually similar to the neutral model of phenotypic evolution (Lande 1976, 1979; Chakraborty and Nei 1982; Lynch and Hill 1986; Lynch

13 1990), which calculates the rate of evolutionary differentiation based on the ratio of inter- to intraspecies variance of measurable morphological characters:

$%& (()*) ∆ = ! , $%&"(()*) where varw(lnz) and varB(lnz) are the observed within- and between-species phenotypic variance for log-transformed measures, respectively, and t is the total number of generations separating the samples (Lynch 1990). Here, I obtained within and between- species variances from the mean squares generated by an ANOVA (Snedecor and

Cochran 1967; Lynch 1990).

Lynch (1990) evaluated a number of cranial characters from multiple groups of extant and fossil mammals to establish an expected range for rates of morphological evolution under neutral processes and suggested that rates of neutral phenotypic evolution for mammals are in the range of 10-4 to 10-2. This expected range of neutral phenotypic evolution allows us to compare observed rates of morphological evolution with those expected under specific evolutionary scenarios. Accordingly, for mammals, low rates (< 10-4) are consistent with a pattern of stasis and suggests stabilizing selection acting to prevent phenotypic divergence. High rates (> 10-2) are consistent with a pattern of phenotypic divergence and suggest directional selection bringing about phenotypic differentiation. Using a range of 10-4 to 10-2 for the neutral expectation should provide a conservative estimate of the minimum and maximum neutral thresholds for dental characters.

To successfully calculate rates of phenotypic differentiation for the sample, I assumed generation time to be two years for the T-P lineage, based on the M1 tooth size 14 of Tarsius spectrum, which is within the size range of the T-P specimens (Shekelle et al.

2008). Given that M1 size is considered a good proxy for body mass, and body mass is highly correlated with generation times among mammals (Millar and Zammuto 1983), this seems to be a suitable assumption for the study. Therefore, for the calculation of the rate, the absolute age duration of the OTUs were transformed into number of generations

(Table 1.3). The number of generations between OTUs was calculated as the absolute value of the mean age difference between OTUs, divided by two years. As a means of comparison and to assess the influence of generation time on the results of the rate statistic, a generation time of one year was also used to derive rates of evolution and are also reported here. All statistical analyses were performed with Microsoft Excel 2016 for

Mac (Microsoft Corporation 2016) and IBM SPSS 2017.

Correlations

To test the hypothesis that P4 loses association with P3 and comes under the developmental controls of the molar field, I used Pearson Product-Moment Correlation tests between lengths and widths of all teeth for each OTU. Under this hypothesis, it is expected that correlations between P3 and P4 will decrease through time and correlations between P4, M1, and M2 will increase through time.

1.3 Results

Taphonomic Biases

Descriptive statistics and results from Mann-Whitney U-tests performed on individual tooth length and width measurements, to identify differences between Clarks

Fork and Bighorn Basin individuals for each OTU, are reported in Table 1.4. At OTU A

15 and C there are no significant differences found between tooth loci length or width between Clarks Fork and Bighorn Basin individuals. At OTU B, the only significant difference found is in M1 width (U=163.5, p=0.043). Average M1 width at OTU B is smaller in the Bighorn Basin sample (M=2.12 mm, SD=0.091 mm, n=19) than in the

Clark’s Fork Basin sample (M=2.17 mm, SD=0.044 mm, n=12). Significant differences are not found at OTU B in the lengths and widths of P3, P4, and M2 or in M1 length. At

OTU D, sample sizes are too low to use a Mann-Whitney U-test, so significant differences are assumed if the means differ by more than two standard deviations from each other. The only significant difference found between basins at OTU D is in P4 width. At OTU D, P4 width of the single Clarks Fork Basin specimen (UM 75037 P4 width=1.75 mm) is smaller by more than two standard deviations from the average P4 widths of the Bighorn Basin sample (M=2.10 mm, SD=0.147 mm, n=24). Consequently, these results support grouping the individuals of the two basins in the four OTUs proposed here.

Trends in Tooth Dimensions

The average measurements for all teeth for each OTU and for the entire series can be found in Figs. 1.4 and 1.5 and Table 1.1. Significant trends in mean length include an overall decrease of P3 from OTU A (M=1.73 mm, SD=0.069 mm) to OTU D (M=1.52 mm, SD=0.24 mm; U=21.5, p=0.049), an overall increase of P4 from OTU A (M=1.95 mm, SD=0.065 mm) to OTU D (M=2.11 mm, SD=0.13 mm; U=241.0, p<0.001), an increase of P4 from OTU A to OTU B (M=2.09 mm, SD=0.13 mm; U=246.0, p=0.001), an increase of M1 from OTU A (M=2.23 mm, SD=0.090 mm) to OTU B (M=2.30 mm,

16 SD=0.083 mm; U=240.5, p=0.044), a decrease of P3 from OTU B (M=1.75 mm,

SD=0.094 mm) to OTU C (M=1.68 mm, SD=0.089 mm; U=124.5, p=0.014) an increase of P4 from OTU B to OTU C (M=2.17 mm, SD=0.14 mm; U=660.5, p=0.048), a decrease of P3 from OTU C (M=1.68 mm, SD=0.089 mm) to OTU D (U=94.0, p=0.036), and a decrease of M1 from OTU C (M=2.32 mm, SD=0.12 mm) to OTU D (M=2.23 mm,

SD=0.098 mm; U=361.0, p=0.002).

Significant trends in mean width include an overall increase of P4 from OTU A

(M=1.87 mm, SD=0.078 mm) to OTU D (M=2.08 mm, SD=0.16 mm; U=238.0, p<0.001), an increase of M1 from OTU A (M=2.07 mm, SD=0.068 mm) to OTU B

(M=2.14 mm, SD=0.079 mm; U=246.5, p=0.028), an increase of P3 from OTU B

(M=1.57 mm, SD=0.090 mm) to OTU C (M=1.67 mm, SD=0.12 mm; U=331.0, p=0.005), an increase of P4 from OTU B (M=1.95 mm, SD=0.12 mm) to OTU C

(M=2.10 mm, SD=0.15 mm; U=782.0, p<0.001).

As expected, significant trends in tooth dimensions reflect the overall pattern of dental evolution observed in the T-P lineage: an overall reduction in P3 length, which produced a shortened jaw, and an overall increase in P4 width, which produced a squarer more robust tooth.

Trends in Tooth Dimension Compared to Paleotemperature and Biohorizon A

The comparison of the changes with information on paleoclimate and Biohorizon

A is shown in Figs. 1.4 and 1.5. The overall trends in tooth length and width when compared to the timing of Biohorizon A show that variance for all teeth increases as the lineage progresses, with the highest values found at either OTU C or OTU D (Table 1.1,

17 Figs. 1.4 and 1.5). Mean length of P3 and M1 shows the greatest statistically significant decrease at the transition between individuals from Biohorizon A (OTU C) to those after

Biohorizon A (OTU D). Mean width of P3 and P4 shows the greatest statistically significant increase from individuals just before Biohorizon A (OTU B) to those during

Biohorizon A (OTU C). These trends coincide with a rapid decrease in MAT at the start of Biohorizon A that continues until nearly the end of the lineage (Figs. 1.4 and 1.5).

Visual appraisal of the leaf-margin paleotemperature curve plotted against the temporal records of tooth length and width for each OTU reveals a possible correlation between MAT and P3 length within OTU D (Figs. 1.4 and 1.5). A Pearson correlation test supports this observation with a significant positive correlation found within OTU D between MAT and P3 length (r=0.726, p=0.001) as well as M2 width (r=0.471, p=0.017).

A significant negative correlation is found within OTU A between MAT and P3 length

(r=-0.883, p=0.020) and from OTU A to OTU D, significant correlations are found between MAT and P3 length (r=0.715, p<0.001), P4 width (r=-0.291, p=0.003), and M1 length (r=0.255, p=0.006). Results from the Pearson correlation tests are reported in

Table 1.2.

Rates of Evolutionary Differentiation

The rates of evolutionary phenotypic differentiation in length and width of each tooth for the T-P lineage suggest different evolutionary histories for each tooth locus over the course of the lineage’s existence (Table 1.5; Fig. 1.6). The rates calculated under the assumption of a one-year generation time effectively reduce the rate calculated under a two-year generation time by half and serve as a conservative estimate of the evolutionary

18 rates for individual tooth loci. Over the entire lineage, OTU A to OTU D, rates for P3, P4,

-6 -5 -7 M1, and M2 length are 4.05 x 10 , 1.66 x 10 , 0, and 5.19 x 10 and rates for P3, P4, M1,

-5 -7 -7 and M2 width are 0, 1.78 x 10 , 7.78 x 10 , and 7.78 x 10 , respectively. From OTU A to

-6 -5 -5 OTU B, rates for P3, P4, M1, and M2 length are 1.02 x 10 , 4.07 x 10 , 2.44 x 10 , and 0

-6 -5 -5 and rates for P3, P4, M1, and M2 width are 1.02 x 10 , 1.32 x 10 , 2.14 x 10 , and 3.05 x

-6 10 , respectively. From OTU B to OTU C, rates for P3, P4, M1, and M2 length are 1.97 x

-5 -5 -6 -5 10 , 1.64 x 10 , 1.64 x 10 , and 0 and rates for P3, P4, M1, and M2 width are 3.03 x 10 ,

5.44 x 10-5, 4.37 x 10-6, and 6.56 x 10-6, respectively. From OTU C to OTU D, rates for

-5 -6 -5 -6 P3, P4, M1, and M2 length are 2.24 x 10 , 8.31 x 10 , 3.78 x 10 , and 3.02 x 10 and

-6 -7 -8 rates for P3, P4, M1, and M2 width are 7.55 x 10 , 5.04 x 10 , 0, and 8.28 x 10 , respectively. Rates calculated using a one-year generation time are reported in Table 1.5.

When considering a generation time of two years, the rates calculated for length of P3, P4, M1, and M2 over the entire lineage, OTU A to OTU D, are consistent with

- stabilizing selection (Table 1.5 and Fig. 1.6a) with P4 having the highest rate (4.98 x 10

5 -6 -6 ), followed by P3 (8.10 x 10 ), and M2 (1.04 x 10 ), while M1 experienced a rate consistent with absolute stasis (0). Rates calculated between intermediate stages show differences from the overall pattern. At the earliest interval, OTU A to OTU B, P3, P4, and

-6 -5 -5 M1 have the highest rates (2.03 x 10 , 8.14 x 10 and 4.88 x 10 , respectively) yet still

-4 fall below the minimum neutral expectation of 10 , while M2 experienced a rate consistent with absolute stasis (Fig. 1.6a). From OTU B to OTU C, rates calculated for

-5 -5 -6 P3, P4, and M1 fall just below the neutral expectation (3.94 x 10 , 3.28 x 10 , 3.28 x 10 , respectively), while the rate for M2 is consistent with absolute stasis (Fig. 1.6a). At the

19 latest interval, OTU C to OTU D, rates for P3, P4, M1, and M2 fall below that of the minimum neutral expectation (4.49 x 10-5, 1.66 x 10-5, 7.55 x 10-5, and 6.04 x 10-6, respectively; Table 1.5 and Fig. 1.6a).

The rates calculated for width, also show similar varying patterns (Table 1.5 and

Fig. 1.6b). Over the entire lineage, OTU A to OTU D, rates for P3, P4, M1, and M2 are below the neutral expectation and are congruent with the expectation of stabilizing selection (Table 1.5 and Fig. 1.6b). Over the entire lineage, OTU A to OTU D, rates for

P3 are consistent with absolute stasis, rates for P4 are highest but still below the minimum

-5 -6 neutral expectation (3.57 x 10 ), and rates for M1 and M2 are both 1.56 x 10 . Over the earliest interval, OTU A to OTU B, rates for P3, P4, M1, and M2 are below the range of

-5 -5 the neutral expectation with P4 and M1 having higher rates (2.64 x 10 and 4.27 x 10 ,

-6 -6 respectively) than P3 and M2 (2.03 x 10 and 6.10 x 10 , respectively; Fig. 1.6b). From

OTU B to OTU C, rates for P3, M1, and M2 are consistent with stabilizing selection (6.07

-5 -6 -5 x 10 , 8.74 x 10 , and 1.31 x 10 , respectively), while P4 falls above the minimum neutral expectation (1.09 x 10-4) and is compatible with neutral evolution (Fig. 1.6b).

From OTU C to OTU D, rates for P3, P4, M1 and M2 are consistent with a pattern of

-5 stabilizing selection with P3 exhibiting the highest rate (1.51 x 10 ) and M1 exhibiting a rate consistent with absolute stasis (Fig. 1.6b).

Under the assumption of a two-year generation time, I find that where significant changes in mean length and width occur, rates range from 8.10 x 10-6 to 1.09 x 10-4.

However, there are six instances where significant differences are not found in tooth loci

20 length or width between OTUs, yet rates at those intervals fall within this range (Table

1.5).

In summary, under the assumption of a two-year generation time, all tooth loci show rates that fall below the minimum neutral expectation except for P4 width from

OTU B to OTU C, which demonstrates an evolutionary rate within the neutral expectation. When considering only the end members, OTU A and OTU D, differences can be explained by varying degrees of stasis with P3 width and M1 length exhibiting rates consistent with absolute stasis. Additionally, I have shown that U-tests on magnitude of change are insufficient for identifying high rates of change and that significant changes in morphology can occur within a pattern consistent with stasis.

Correlations between tooth dimensions

Pearson correlation tests for length of each tooth (Table 1.6) show that initially, at

OTU A, P3 was correlated with P4 and M2; however, the correlation between P3 and M2 was lost by OTU B. At OTU B a strong correlation remained among P3 and P4; however, this correlation was lost by OTU C but regained by the end of the lineage at OTU D. A correlation in length among P4 and M2 developed at OTU B and remained at OTU C where M1 also developed a correlation with P4. By OTU D, P4 loses its correlation with

M1 and M2. M1 and M2 maintained a significant correlation in length throughout the sequence, except at OTU A (Table 1.6).

Correlation results for width of each tooth (Table 1.6) show that P3 shared a strong negative correlation with M2 at OTU A but this correlation was lost by OTU B. By

OTU B, P4 width became correlated with both M1 and M2 and significant correlations

21 remained at OTU C. At OTU D, the correlation between P4 and M1 remained but was lost between P4 and M2. Except for OTU A, correlations among widths of M1 and M2 were shared throughout the lineage. Sample size for the correlation tests are not as robust as they are for analyses using the rate statistic because some specimens do not have all four teeth present in the jaw. Consequently, even results with large r values might not be considered significant (Table 1.6).

In general, the results do not show that P3 became less correlated with P4 but do show that correlations between P3 and the M1 and M2 teeth diminished. Additionally, I find that P4 became more correlated with M1 and M2, as the lineage progressed through time; however, the correlation gained between the lengths and widths of P4 and M2 at

OTU B and OTU C was lost at OTU D.

1.4 Discussion

The morphological changes observed in the T-P lineage have been attributed to a process of anagenetic gradual evolution (Bown and Rose 1987). This inference was based on the observation that changes in the dentition throughout the lineage did not occur all at once and did not include the entire population. Transitions to derived characters were gradual, resulting first in an increase in variation within the population and then later to the derived conditions becoming the dominant morphology (Bown and Rose 1987).

Within this overall interpretation of an anagenetic gradual origin of the characters of

Pseudotetonius, the analyses revealed additional complexity as detailed in the subsequent sections.

22 Taphonomic Biases

Various taphonomic processes can influence statistical analyses on fossil assemblages and can result in incorrect inferences made from those analyses

(Behrensmeyer 1991; Behrensmeyer and Hook 1992; Behrensmeyer et al. 1995, 2000).

Specific taphonomic processes that may result in differences between samples from the

Clarks Fork and Bighorn basins include sedimentation rate and paleosol maturity.

Sedimentation rates are lower and hence paleosol age is more mature in the central

Bighorn Basin compared to the Clarks Fork Basin (Clyde et al. 2007). These differences may influence the size of individuals found between the two basins (Bown and Beard

1990; Clyde et al. 2005), with a greater proportion of smaller individuals expected in the central Bighorn Basin when compared to the Clarks Fork Basin. As an internal check on potential taphonomic biases influencing the results from the rate analysis and correlation study, I performed U-tests on tooth length and width for each tooth loci to test for differences between Clarks Fork and Bighorn Basin individuals. In only two comparisons, M1 width at OTU B and P4 width at OTU D, did individuals from the

Clarks Fork Basin differ significantly from Bighorn Basin individuals. Average M1 width in Clarks Fork Basin individuals was greater than M1 width in central Bighorn Basin individuals, which aligns with the expectation that smaller individuals would be found in the central Bighorn Basin section. Conversely, P4 width of the single Clarks Fork Basin individual was less than the average P4 width of central Bighorn Basin individuals by more than two standard deviations, which contrasts with the expected alluvial size sorting of smaller fossils in mature paleosols.

23 My findings suggest that any influences from taphonomic biases in the sample are minimal and likely similar between basins for the T-P lineage. However, further investigation to resolve whether the evolutionary trends observed are temporal in nature or potentially driven by geography is warranted but outside the scope of this paper. One approach to address this question would be to look at the central Bighorn and Clarks Fork

Basins separately to see if the same evolutionary patterns observed in the combined basin analysis hold. Unfortunately, current sample sizes for the T-P lineage in the Clarks Fork

Basin and in the oldest sections of the Bighorn Basin are too low to perform the same rate and correlation analyses on each basin independently. If sample sizes increase in the future this would be an interesting question worth investigating.

Trends in Tooth dimension

This study focused on the reduction in size of P3 and its morphological transition to becoming similar in size and shape to the I2 and C, and on the increase in the size of P4 and its transition to a larger, tall cusped tooth. The mean lengths and widths of the P3, P4,

M1, and M2 teeth for each OTU were calculated to reveal the overall patterns and evolutionary trends in tooth dimensions throughout the lineage. U-tests were performed to see where there were significant differences in tooth dimensions between OTUs. I found that the overall transition to a much reduced P3 by the end of the lineage occurred later in the evolutionary series with significant decreases occurring between OTU B and

OTU C and between OTU C and OTU D. The overall increase in P4 length and width that is observed over the entire lineage occurred earlier in the lineage between OTU A and

OTU B and between OTU B and OTU C. I also found that M1 length and width increased

24 significantly early on, between OTU A and OTU B, but decreased in length later between

OTU C and OTU D, which resulted in no significant net change when only the end members of the lineage, OTU A and OTU D, were considered. These trends in tooth dimension are revealing in that P4 and M1 increased in length before the reduction in P3 length occurred, which suggests that the increase in the former may have created a selective pressure on P3 to reduce its length. In other words, it illustrates that the evolution of the T-P lineage dentition was not occurring simultaneously and that there might have been selective feedback between the posterior and anterior premolars over time.

Paleotemperature and Biohorizon A

The T-P lineage, having persisted through a biotic turnover event and rapid climate change, provides a unique opportunity to observe how dental morphology may have responded to environmental influences. To address this question, patterns of tooth length and width throughout the lineage were compared to changes in MAT and the timing of Biohorizon A (Figs. 1.4 and 1.5). I found that the variance of length and width measurements for all teeth increased as the lineage progressed (Table 1.1, Figs. 1.4 and

1.5), the greatest statistically significant changes in tooth length and width occurred at transitions either into or out of Biohorizon A and coincided with a rapid decrease in MAT

(Figs. 1.4 and 1.5), and that MAT had a potentially variable influence on individual tooth dimensions throughout the lineage.

The analyses show that, as the lineage progressed, morphological variance of tooth dimensions for all teeth increased (Table 1.1). This directly contrasts with the

25 expectation of phenotypic characters under stabilizing selection, which predicts morphological variance should decrease as individuals from the tails of frequency distributions are selected against (Møller and Pomiankowski 1993). Conversely, persistent directional selection for trait values at one extreme of a frequency distribution will select for existing genes, new mutants for the extreme trait values, and for the relaxation of developmental controls (Møller and Pomiankowski 1993). As such, the degree of phenotypic variability increases under strong directional selection, as demonstrated in several laboratory experiments (MacArthur 1949; Reeve and Roberson

1953; Falconer 1955; Robertson 1955; Clayton and Robertson 1957) and on paleontological time-scales (Skinner and Kaisen 1947; Hooper 1957; Guthrie 1965;

Williamson 1981). An increase in morphological variance towards the end of the T-P lineage may indicate relaxed control on the T-P lineage’s dental development. The increased morphological variance in the dentition that occurred during and after

Biohorizons A may have been a side effect of rapidly changing temperatures or a response to the faunal turnover event during that time (Figs. 1.4 and 1.5). There are a couple of scenarios that can explain this pattern. For example, the opening of ecological niches from species extinctions may have provided a release of stabilizing selection that allowed for gradual morphological evolution to occur. It is also plausible that neighboring populations were introduced back into the Bighorn Basin around the OTU C

– OTU D transition and this led to an increase in variation among individuals in the T-P lineage.

26 Previous researchers have discussed morphological trends in mammalian evolution in the Bighorn Basin through episodes of climate change (Rea et al.1990; Bown et al. 1994a; Clyde and Gingerich 1994, 1998; Alroy et al. 2000; Gingerich 2003; Silcox et al. 2008; Zack 2011). Early Eocene Bighorn Basin mammals have demonstrated an increase in molar size that corresponds to the cooling event between Biohorizons A and B

(Bown et al. 1994a; Dunn and Rose 2015). However, not all Bighorn Basin mammals conform to this pattern (Clyde and Gingerich 1994; Zack 2011). Bown et al. (1994a) found that, in accordance with Bergmann’s rule (Bergmann 1847; Mayr 1956, 1963), M1 area appeared to have an inverse correlation with MAT in the T-P lineage. The visual observations made by Bown et al. (1994a) are weakly corroborated by the findings of a significant increase in M1 length and width before Biohorizon A, when temperatures were warm but beginning to cool, and a decrease in M1 size, driven by a significant decrease in length, after Biohorizon A when temperatures were cool. It should be emphasized, however, that I did not find a significant inverse correlation between MAT and M1 length or width but did find a positive correlation between MAT and M1 length, which contrasts with the expectations of Bergmann’s rule. The investigations into correlations between MAT and tooth dimension revealed that MAT potentially had a variable influence on individual tooth dimensions throughout the lineage and that these correlations were transient at best. Further research is necessary to determine whether changing MAT played a significant role in the trends observed in the T-P lineage.

27 Evolutionary Rates

The dentition of the T-P lineage evolved anagenetically, from the accumulation of incremental changes to its dental morphology over the duration of the lineage (Bown and Rose 1987). These changes are observed to be substantial enough that individuals at the beginning of the lineage are not recognizable as being of the same genus as those at the end of the lineage. The dentitions of some individuals at the earliest stages (OTU A and OTU B) of the lineage contain a much reduced second premolar. At these early stages, there are four clear tooth types (incisor, canine, premolar, and molar) that are recognizably different from one another (Fig. 1.1). By the end of the lineage, P2 disappeared from the dentition, P3 reduced its dimensions and became strongly similar phenotypically to the incisors and canines, and P4 increased its dimensions and became a square tall cusped tooth. The analyses of length and width of individual teeth reveal that the evolution towards a shorter more compact and robust dentition noted by Bown and

Rose (1987) was complex, in that length and width of the cheek teeth of the lower dentition did not change at the same time, rate, or magnitude.

One major goal of this research was to establish rates of morphological evolution within the posterior dentition of the T-P lineage. I used the method proposed by Lynch

(1990) to derive rates of morphological evolution for the length and width of the P3, P4,

M1, and M2 teeth. I found that rates for all tooth positions over the entire lineage (OTU A to OTU D) are consistent with a pattern of stabilizing selection, suggesting that it was the release of selective pressures, rather than the addition of new diversifying selective pressures that explain the changes observed in the lineage. Similarly, I found rates

28 consistent with stasis for intermediate stages throughout the lineage with one exception,

P4 width from OTU B to OTU C falls within the range of the neutral expectation. Though rates were largely below the threshold of the minimum neutral expectation, I found varying degrees of stabilizing selection that range from complete stasis to just below the neutral threshold.

The results from the evolutionary rate analysis are interesting in that I found rates consistent with varying degrees of morphological retention in a lineage that experienced significant genus-level morphological changes in the cheek teeth. I found evidence of strong stabilizing selection (evolutionary rate equal to zero) occurring in the molars, specifically M1 width from OTU C to OTU D, and M2 length from OTU A to OTU B and

OTU B to OTU C. Interestingly, the rate of evolution for P3 width and M1 length over the entire lineage (OTU A to OTU D) was zero, suggesting that effectively no change occurred in the width of these teeth when considering only the end members of the lineage. However, when considering transitions between intermediate stages for P3 width and M1 length, rates were found that were several orders of magnitude higher, albeit still below the minimum neutral threshold. This observation provides a nice example of how gaps, formed when only the end members of a lineage are preserved, in the fossil record may lead to incorrect conclusions about the evolutionary history of fossil organisms.

Additionally, I found that at no point throughout the lineage do statistically significant changes in the P3, P4, M1, and M2 teeth correspond with a pattern of divergence by directional selection. This pattern illustrates well how U-tests and phenotypic difference

29 in general is insufficient in discussions about selective forces, unless the number of generations separating the populations observed is taken into account.

Even though my results indicate that stabilizing selection was the main evolutionary force acting on tooth length and width throughout the lineage, there were times when I identified a relative release of stabilizing selection. This release of constraint led to rates close to the minimum neutral threshold or, in the case of P4 width from OTU B to OTU C, just above this threshold. This study found that the most significant changes and highest evolutionary rates occurred in the lengths of P3 and M1 between intermediate stage individuals concurrent with Biohorizon A (OTU C) and those after Biohorizon A (OTU D), which corresponds to later intermediates stage individuals and Pseudotetonius ambiguus. P4 length and M1 width showed the largest significant increase and highest rates during the transition from Tetonius matthewi individuals (OTU

A) to intermediate stage individuals occurring before Biohorizon A (OTU B). P3 and P4 width experienced the most significant changes during the OTU B to OTU C transition.

These results illuminate the potential impact that Biohorizon A had on the T-P lineage’s dental evolution, as significant changes to length and width and high rates are closely associated with transitions into or out of Biohorizon A. Such a finding is not surprising as

Biohorizon A represents a time period when there was a great deal of faunal turnover and climate cooling occurring in the Bighorn Basin (Schankler 1980; Bao et al. 1999; Wing et al. 1991, 2000, 2005; Chew 2009). It is possible that competition between newly arriving species, the opening up of ecological niches from extinction or emigration, or climate

30 cooling caused a release from strong stabilizing selection on individual tooth loci, allowing for gradual morphological changes to occur in the dentition.

While my study did not identify directional selection as a process for the evolutionary changes that occurred in the dentition of the T-P lineage, it is still possible that directional selection played a role but the temporal resolution of the fossil record is not adequate enough for detecting such a pattern in this lineage. Furthermore, I cannot rule out the possibility that the T-P lineage evolved under punctuated equilibrium, a process by which new species arise relatively quickly followed by long periods of equilibrium and not through a gradual cumulative process (Eldredge 1971; Eldredge and

Gould 1972). It is possible that changes arose quickly, but the temporal resolution of the sample is not yet fine enough to detect rates above the neutral expectation. Under this scenario, rates would appear to be in stasis throughout the lineage’s existence.

Regardless of this study’s limitations, I reject the null hypothesis, that morphological changes observed in the dentition can be explained by neutral processes alone. Moreover, the results also reject the interpretation that the T-P lineage evolved under sustained directional selection. However, I cannot rule out brief pulses of directional selection that were too short-lived to detect. Such pulses, even if they were present, were not strong enough to overcome the dominant signal of stabilizing selection and release from it. When taking into account the time frame of the lineage, it is more likely that the dental morphological change was strongly selected against, and it is the partial release from these restrictive selective forces that explain the differences observed in the T-P lineage.

31 Correlations

The second major goal of this study was to investigate patterns of dental integration among teeth in the T-P lineage. I used Pearson correlation tests between lengths and widths of all teeth for each OTU to investigate patterns of dental integration among teeth. My findings show that P4 gained a significant correlation with the molars, while P3 became less correlated with the molars. As tooth size changed throughout the lineage, so too did the dental formula, with the loss of the P2, and phenotypic correlations between individual teeth. Previous studies suggested a direct correlation between the size of the molar field and the posterior dentition tooth formula (Ribeiro et al. 2013). This inference is supported by the observation that the P2 is often lost, to accommodate the molars of the maxilla, when the relative length of the molar field reaches a threshold limit

(Ribeiro et al. 2013). It is likely that similar mechanisms took place in the lower dentition of the T-P lineage and the loss of P2 and decrease in length of P3 occurred to accommodate the molars of the mandible. Results from the correlation analyses indicate that there was an increasing correlation between the lengths and widths of P4 and the molar field over the duration of the lineage (Table 1.6); however, I did not find evidence of P4 losing an association with P3. If the molar field expanded to incorporate P4, it is plausible that P2 was lost and P3 reduced its length, at least in part, to accommodate the expanding cheek teeth. The disappearance of P2 by the end of OTU B and the reduction in the length of P3, may have provided available space for the P4 to significantly increase its length during the OTU B to OTU C transition. Alternatively, the increase in the size of

32 P4 may have created a selective pressure on the P3 to reduce its length to provide space for a larger P4.

The evolutionary patterns observed in the mean lengths and widths of the cheek teeth can be explained by the assembly of phenotypes, here lengths and widths of individual teeth in the dentition of the T-P lineage, into developmental fields or modules.

Modules, in this sense, can organize into networks, which are subject to selective forces acting upon their individual units, or the network of which the modules are part (Gómez-

Robles and Polly, 2012). Throughout the evolution of mammals, the dentition has been divided into incisor, canine, premolar, and molar fields (Dahlberg 1945; Butler 1978;

Townsend et al. 2009). McCollum and Sharp (2001) provided evidence to support the theory of dental fields by analyzing gene expression during dental development in mice.

The lengths and widths of premolars and molars may be influenced by a larger and hierarchically superior module that encompasses both the premolar and molar fields, as the lengths and widths of teeth appear to be on their own evolutionary trajectories.

However, to test this hypothetical postcanine module, further analyses focused on identifying modules and developmental fields are needed. Given that my data support a scenario of P4 becoming integrated into the molar morphogenetic field, I cannot reject hypothesis two.

1.5 Conclusions

The present study adds to previous groundwork on the evolution of omomyiforms by presenting a unique case study that analyzes changing correlations and morphological rates of change among tooth loci within the dentition of the Tetonius – Pseudotetonius

33 lineage. With such a complete fossil record, I am provided the opportunity to test hypotheses of morphological evolution within a single lineage from different angles. I conclude the following from the analyses:

1. An initial increase in the lengths of P4 and M1 from OTU A to OTU B

may have created a selective pressure on P3 to subsequently reduce its

length.

2. Trends in tooth length and width when compared to the timing of

Biohorizon A and the estimated mean annual temperature in the Bighorn

Basin suggest an increase in variance at the end of Biohorizon A and OTU

D, which may indicate a relaxation of developmental control.

3. The decrease in P3 length and M2 width in OTU D may have been

correlated with decreasing MAT or a morphological response to the faunal

turnover event at Biohorizon A. However, further research is warranted to

rule out other confounding variables.

4. Rates of phenotypic evolution found in the T-P lineage are congruent with

a pattern of stabilizing selection, except in the case of P4 width from OTU

B to OTU C where the rate was found to be indistinguishable from the

neutral expectation.

5. Varying degrees of stabilizing selection occurred on individual tooth loci,

producing rates ranging from absolute stasis (no change between OTUs) to

rates just below the minimum neutral threshold (rates below 10-4). These

rates support that, throughout the T-P lineage’s evolutionary history, there

34 were times where a release of the selective pressure towards stasis

occurred, allowing for the tooth lengths and widths to change.

6. Comparing rates calculated between the two end members of the lineage,

OTU A and OTU D, versus rates between stratigraphically contiguous

parts of the lineage, I find that rates of phenotypic evolution are sensitive

to the effects of time averaging. This highlights the limitation in less

complete fossil records, where intermediate forms are unknown,

phenotypic divergence may appear to have been largely conserved when,

in fact, the evolutionary story may be more complex with a history of

neutral evolution and/or divergence acting at different times throughout a

lineage’s existence.

7. There is a clear gain in association between P4 and the molars and a loss in

association between P3 and the molars; however, I did not find evidence of

P4 losing an association with P3. This inference is evidenced by an

increasing correlation between the P4 and the molars, which is observed

physically by the diverging phenotypes of the premolars. Results from

correlation tests support my hypothesis only in part, as I did not find that

P4 loses association with P3 but did find that P4 comes under the

developmental controls of the molar field.

35 1.6 Figures

Stage 5 346 – 374 m Pseudotetonius ambiguus

Stage 4 334 – 370 m Intermediate 1 mm

Stage 3 278 – 348 m Intermediate P C 3 I2 Stage 2 190 – 290 m Intermediate P4 P3 I1 P2` M1 I2 C Stage 1 140 – 190 m Tetonius matthewi

Fig. 1.1 Stages of morphological evolution in the lower dentition of the Tetonius – Pseudotetonius lineage. Meter levels represent the range at which specimen types are found in the Bighorn Basin. Abbreviations: I1, lower first incisor; I2, lower second incisor; c, lower canine; P2, lower second premolar; P3, lower third premolar; P4, lower fourth premolar; M1, lower first molar. Adapted from Bown and Rose (1987).

36 Length

OTU D BHB 290-374 CFB 575 P3: U=94.0, p=0.036* 54.70-54.32 Ma P4: U=355.5, p=0.090 M1: U=361.0, p=0.002** OTU C M2: U=343.0, p=0.457 BHB 212-282 m CFB 450-545 m P3: U=124.5, p=0.014** 55.06-54.74 Ma P3: U=21.5, p=0.049* P4: U=660.5, p=0.048* P4: U=241.0, p<0.001** M1: U=815.5, p=0.463 M : U=142.5, p=0.987 OTU B 1 M2: U=316.5, p=0.656 M : U=151.0, p=0.496 BHB 160-190 m 2 CFB 320-395 m P3: U=79.5, p=0.460 55.28-55.15 Ma P4: U=246.0, p=0.001** M1: U=240.5, p=0.044* OTU A M2: U=122.5, p=0.706 BHB 64-150 m CFB 240 m 55.71-55.30 Ma

Fig. 1.2 Results from two-sample U-tests between the mean lengths of each tooth position for adjacent OTUs, and for the entire lineage OTU A to D. Significant results are indicated by asterisks at P < 0.05 (*) and P < 0.01 (**)

37 Width

OTU D BHB 290-374 CFB 575 P3: U=105.5, p=0.083 54.70-54.32 Ma P4: U=487.5, p=0.860 M1: U=675.0, p=0.562 OTU C M2: U=319.0, p=0.255 BHB 212-282 m CFB 450-545 m P3: U=331.0, p=0.005** 55.06-54.74 Ma P3: U=53.5, p=0.693 P4: U=782.0, p<0.001** P4: U=238.0, p<0.001** M1: U=606.0, p=0.162 M : U=175.5, p=0.285 OTU B 1 M2: U=372.0, p=0.117 M : U=212.0, p=0.289 BHB 160-190 m 2 CFB 320-395 m P3: U=56, p=0.604 55.28-55.15 Ma P4: U=206.5, p=0.061 M1: U=246.5, p=0.028* OTU A M2: U=150.0, p=0.553 BHB 64-150 m CFB 240 m 55.71-55.30 Ma

Fig. 1.3 Results from two-sample U-tests between the mean widths of each tooth position for adjacent OTUs, and for the entire lineage OTU A to D. Significant results are indicated by asterisks at P < 0.05 (*) and P < 0.01 (**)

38 19 19 1999, 1999, 2000, 17 17 ( Pseudotetonius Pseudotetonius 0.9 0.9 -

15 15 nius MAT 13 13 ℃ ℃ 11 11 Length Length 2 4 MAT MAT MAT MAT P M ln ln 9 9 0.7 0.7 7 7 teeth for each OTU in the Teto the in OTU each for teeth

latest occurring OTU C C individuals OTU occurring latest )

5 5 d Mean Length Mean (

2 3 3 ), and M and ), c BiohorizonA BiohorizonA ( 1 1

0.5 0.5 1 55 55

54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 Age, Ma Age, Age, Ma Age, M ), b d b (

4 OTU D ),P a 1 (

3 hich coincides with all but the but all with coincides hich P 19 19 he 17 17 0.8 0.9 54.8 Ma, w 54.8 - OTU C measurements measurements and Mean Annual Temperature (MAT) obtained from Wing et al.

15 15 asurements for t for asurements 13 13 0.6 ℃ ℃ 11 11 OTU B Length Length 1 3 MAT MAT MAT MAT P M ln ln 9 9 0.4 0.7 e time period between 55.1 between period time e 7 7 OTU A 5 5 0.2 3 3 BiohorizonA BiohorizonA Scatterplots of log transformed length me length transformed log of Scatterplots

0 1 1 0.5 . Biohorizon A spans th spans A . Biohorizon ) 55 55

54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 Age, Ma Age, Age, Ma Age, a c 1.4 Fig. lineage. Also plotted are log mean transformed length 2005 39

s 19 19 1999, 1999, 2000, 17 17 ( Pseudotetoniu 0.9 0.9 -

15 15 MAT 13 13 ℃ ℃ 11 11 Width Width 2 4 P M MAT MAT MAT MAT OTU C C individuals OTU ln ln 9 9 0.7 0.7 7 7 Mean Width Mean ) teeth for each OTU in the Tetonius the in OTU each for teeth ) 5 5 d (

2 3 3 ), and M BiohorizonA BiohorizonA c 1 1 ( 0.5 0.5

1 55 55

54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 Age, Ma Age, Age, Ma Age, ), M b d b ( OTU D

4 ), P 1 a ( and and Mean Annual Temperature (MAT) obtained from Wing et al.,

3 19 19 17 17 OTU C 0.8 0.9 54.8 Ma, which coincides with all but the latest occurring occurring the latest but all with coincides Ma, which 54.8 - 15 15 13 13 0.6 OTU B ℃ ℃ 11 11 Width Width 1 3 P M MAT MAT MAT MAT ln ln 9 9 med width measurements for the P the for measurements width med r 0.4 0.7 ransformed ransformed mean width measurements 7 7 OTU A 5 5 0.2 3 3 BiohorizonA BiohorizonA 0 1 1 Scatterplots of log transfo log of Scatterplots 0.5

55 55 . Biohorizon A spans the time period between 55.1 between period time the spans A . Biohorizon

)

54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 54.2 54.4 54.6 54.8 55.2 55.4 55.6 55.8 Age, Ma Age, Age, Ma Age, a c

1.5 Fig. lineage. Also plotted are log t 2005 40 Stasis Neutral A-D Divergence er the entire lineage (A (A lineage entire the er C-D v 2 D) and o and D)

M – B-C C, C C, C

– B, B

– A-B 1 M

1.0E-1 1.0E-2 1.0E-3 1.0E-4 1.0E-5 1.0E-6 1.0E-7 1.0E-8 1.0E-9

1.0E+0

Δ Width b 4 Stasis P Neutral A-D ) of each tooth loci between OTUs (A (A OTUs between loci tooth each of ) Divergence b C-D and width ( width and ) a 3 P B-C A-B The rates calculated for the length ( length the for calculated The rates

1.6

1.0E-1 1.0E-2 1.0E-3 1.0E-4 1.0E-5 1.0E-6 1.0E-7 1.0E-8 1.0E-9

1.0E+0

Δ Length Length D)

a Fig. – 41 1.7 Tables

Table 1.1

Tooth OTU n Length Width

Mean s s2 Mean s s2

P3 A 6 1.73 0.069 0.005 1.59 0.049 0.002

B 22 1.75 0.094 0.009 1.57 0.090 0.008 C 20 1.68 0.089 0.008 1.67 0.12 0.014 D 16 1.52 0.24 0.058 1.60 0.13 0.016 A-D 64 1.67 0.17 0.028 1.61 0.11 0.013

P4 A 11 1.95 0.065 0.004 1.87 0.078 0.006

B 27 2.09 0.13 0.017 1.95 0.12 0.015 C 38 2.17 0.14 0.02 2.10 0.15 0.024 D 25 2.11 0.13 0.017 2.08 0.16 0.026

A-D 101 2.11 0.14 0.021 2.03 0.16 0.027

M1 A 11 2.23 0.090 0.008 2.07 0.068 0.005

B 31 2.30 0.083 0.007 2.14 0.079 0.006

C 48 2.32 0.12 0.015 2.11 0.13 0.017

D 26 2.23 0.098 0.010 2.12 0.15 0.024 A-D 116 2.28 0.11 0.012 2.11 0.12 0.014

M2 A 14 2.20 0.087 0.007 2.06 0.099 0.010

B 19 2.18 0.11 0.012 2.09 0.11 0.011 C 31 2.19 0.11 0.012 2.14 0.13 0.018

D 25 2.17 0.097 0.009 2.10 0.13 0.018 A-D 89 2.18 0.10 0.010 2.10 0.12 0.016

Table 1.1 Descriptive statistics for the lengths and widths of individual teeth for OTU A, B, C, and D and the entire lineage, OTU A through OTU D. Abbreviations: OTU, operational taxonomic unit; n, sample size; s, standard deviation; s2, sample variance

42 Table 1.2

OTU P3 P4 M1 M2 r (L | W) r (L | W) r (L | W) r (L | W) n n n n A MAT -0.883* | -0.094 -0.261 | -0.341 -0.262 | -0.127 0.263| 0.200

6 11 11 14

B -0.292 | 0.144 0.017 | 0.068 0.230 | -0.031 0.077 | 0.130 MAT 22 27 31 19 C 0.083 | -0.044 -0.055 | -0.094 0.041 | -0.134 0.072 | -0.137 MAT 20 38 48 31 D 0.726** | 0.249 0.178 | -0.054 0.357 | 0.280 0.157 | 0.471* MAT 16 25 26 12 0.715** | 0.034 -0.062 | -0.291** 0.255** | 0.079 0.123 | 0.114 A-D MAT 64 101 116 89

Table 1.2 Results from a bivariate correlation using the Pearson Product-Moment Correlation test (r) for tooth length (L), width (W), and mean annual temperature (MAT) for OTUs A, B, C, D, and the entire lineage OTU A to OTU D. Values listed next to bars are of r values. Significant results are indicated by asterisks at P < 0.05 (*) and P < 0.01 (**). Abbreviations: OTU, operational taxonomic unit; n, sample size

Table 1.3 Number of Generations Lineage segment (OTU) 1-year generation time 2-year generation time assumed assumed A – B 327,709 163,855 B – C 304,944 152,472 C – D 330,973 165,486 A – D 963,626 481,813 Table 1.3 Number of generations between adjacent lineage segments (A – B, B – C, C – D) and the entire lineage (A – D) for one and two-year generation times.

43 Table 1.4

OTU Tooth U-Test Result; p- (L/W) Bighorn Basin Sample Clarks Fork Basin Sample value OR within two St. Dev’s n Mean s n Mean s from Mean (Yes/No) A P3 L 3 1.73 0.104 3 1.72 0.029 U=5.0; p=1.000

P3 W 3 1.62 0.029 3 1.57 0.058 U=2.0; p=0.400

P4 L 7 1.94 0.073 4 1.95 0.058 U=15.0; p=1.000

P4 W 7 1.89 0.091 4 1.85 0.058 U=12.0; p=0.788

M1 L 7 2.23 0.095 4 2.23 0.096 U=13.5; p=0.927

M1 W 7 2.07 0.081 4 2.08 0.050 U=15.0; p=1.00

M2 L 12 2.19 0.088 2 2.25 0.071 U=17.0; p=0.440

M2 W 12 2.04 0.097 2 2.15 0.071 U=19.5; p=0.198

B P3 L 16 1.75 0.092 6 1.75 0.110 U=50.5; p=0.858

P3 W 16 1.56 0.098 6 1.61 0.058 U=62.5; p=0.294

P4 L 16 2.06 0.134 11 2.14 0.109 U=121.0; p=0.110

P4 W 16 1.93 0.141 11 1.98 0.087 U=112.5; p=0.231

M1 L 19 2.28 0.085 12 2.34 0.064 U=162.0; p=0.053

M1 W 19 2.12 0.091 12 2.17 0.044 U=163.5; p=0.043

M2 L 17 2.18 0.114 2 2.20 0 Yes

M2 W 17 2.07 0.100 2 2.23 0.035 Yes

C P3 L 11 1.66 0.086 9 1.69 0.095 U=63.5; p=0.295

P3 W 11 1.68 0.147 9 1.66 0.082 U=41.0; p=0.552

P4 L 17 2.18 0.164 21 2.16 0.127 U=160.5; p=0.601

P4 W 17 2.06 0.189 21 2.12 0.119 U=224.0; p=0.189

M1 L 19 2.31 0.127 29 2.32 0.118 U=291.0; p=0.740

M1 W 19 2.12 0.156 29 2.11 0.112 U=272.0; p=0.941

M2 L 17 2.22 0.119 14 2.16 0.096 U=86.0; p=0.200

M2 W 17 2.13 0.121 14 2.14 0.152 U=127.0; p=0.769

D P3 L 16 1.52 0.241 0 - - -

P3 W 16 1.60 0.125 0 - - -

P4 L 24 2.11 0.132 1 2.15 - Yes

P4 W 24 2.10 0.147 1 1.75 - No

M1 L 23 2.24 0.096 3 2.13 0.058 Yes

M1 W 23 2.15 0.141 3 1.92 0.104 Yes

M2 L 23 2.18 0.089 2 2.05 0.141 Yes

M2 W 23 2.10 0.133 2 2.03 0.177 Yes Table 1.4 Comparison of Bighorn Basin sample to Clarks Fork Basin sample for individual tooth loci at each OTU. Descriptive statistics and Mann-Whitney U-test results are listed for each tooth loci and each OTU. Abbreviations: OTU, operational taxonomic unit; n, sample size; s, standard deviation

44

Table 1.5

Tooth Lineage Segment 1-year generation 2-year generation (OTU) Length ∆ Width ∆ Length ∆ Width ∆

-6 -6 P3 A –D 4.05 x 10 0 8.10 x 10 0

A – B 1.02 x 10-6 1.02 x 10-6 2.03 x 10-6 2.03 x 10-6

B – C 1.97 x 10-5 3.03 x 10-5 3.94 x 10-5 6.07 x 10-5

C – D 2.24 x 10-5 7.55 x 10-6 4.49 x 10-5 1.51 x 10-5

-5 -5 -5 -5 P4 A – D 1.66 x 10 1.78 x 10 4.98 x 10 3.57 x 10

A – B 4.07 x 10-5 1.32 x 10-5 8.14 x 10-5 2.64 x 10-5

B – C 1.64 x 10-5 5.44 x 10-5 3.28 x 10-5 1.09 x 10-4

C – D 8.31 x 10-6 5.04 x 10-7 1.66 x 10-5 1.01 x 10-6

-7 -6 M1 A – D 0 7.78 x 10 0 1.56 x 10

A – B 2.44 x 10-5 2.14 x 10-5 4.88 x 10-5 4.27 x 10-5

B – C 1.64 x 10-6 4.37 x 10-6 3.28 x 10-6 8.74 x 10-6

C – D 3.78 x 10-5 0 7.55 x 10-5 0

-7 -7 -6 -6 M2 A – D 5.19 x 10 7.78 x 10 1.04 x 10 1.56 x 10

A – B 0 3.05 x 10-6 0 6.10 x 10-6

B – C 0 6.56 x 10-6 0 1.31 x 10-5

C – D 3.02 x 10-6 8.28 x 10-8 6.04 x 10-6 9.06 x 10-6

Table 1.5 Rates of evolutionary differentiation based on the ratio between inter- and intra-species variation in length and width of P3, P4, M1, and M2 teeth over the entire lineage (A – D) and between OTUs (A – B, B – C, and C – D) for 1 and 2 year generation times. Abbreviation: OTU, operational taxonomic unit

45 Table 1.6

P3 P4 M1 M2 OTU Tooth loci r (L | W) r (L | W) r (L | W) r (L | W) n n n n A P3 1 0.889* | 0.485 0.945 | -0.945 -1.000** | -1.000**

6 6 3 2

1 0.927 | 0.000 0.115 | 0.866 P4 - 11 4 3 1 0.312 | 0.238 M1 - - 11 5 1 M2 - - - 14 B 1 0.917** | 0.850** -0.044 | 0.474 -0.891 | 0.422 P3 22 18 10 4 1 -0.084 | 0.711** -0.909* | 0.852* P4 - 27 18 6 1 0.724* | 0.898** M1 - - 31 9 1 M2 - - - 19 C 1 0.173 | 0.527* -0.97 | 0.506* -0.196 | 0.364 P3 20 20 16 14 1 0.765** | 0.657** 0.664** | 0.625** P4 - 38 31 23 1 0.584** | 0.772** M1 - - 48 28 1 M2 - - - 31 D 1 0.600* | 0.518* 0.306 | 0.508 0.356 | 0.463 P3 16 15 13 12 1 0.232 | 0.624** 0.131 | 0.452 P4 - 25 21 17 1 0.637** | 0.743** M1 - - 26 20 1 M2 - - - 25

Table 1.6 Correlation matrix showing results from a bivariate correlation using the Pearson Product-Moment Correlation test (r) for tooth length (L) and width (W) for OTUs A, B, C, and D. Values listed next to bars are of r values. Significant results are indicated by asterisks at P < 0.05 (*) and P < 0.01 (**). Abbreviations: OTU, operational taxonomic unit; n, sample size 46 1.8 Literature Cited

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55

Chapter 2. Rates and Modes of Dental Evolution in Late Paleocene and Early Eocene

Paromomyids

2.1 Introduction

Plesiadapiforms (Simons and Tattersall in Simons 1972) are a paraphyletic or polyphyletic (Szalay and Delson 1979; Silcox et al. 2017) group of euarchontan mammals that appeared near the Cretaceous-Paleogene boundary and survived into the late Eocene (Silcox et al. 2017). Plesiadapiforms were a diverse and widespread group, which includes more than 140 identified species in 11 families (Silcox et al. 2017; Silcox and López-Torres 2017). The evolutionary diversification of Plesiadapiforms resulted in a wide range of dental and skeletal adaptations that afforded them the ability to explore different ecological niches (Silcox and Gunnell 2008; Silcox et al. 2017).

The majority of plesiadapiforms were small bodied, with the exception of some species of Plesiadapis, which are estimated to have weighed up to 2.5 kg (Gunnell and

Silcox 2008). Plesiadapiforms were arboreal but skeletal evidence suggests that they did not have special adaptations for leaping like most early euprimates (Szalay and Decker

1974; Szalay et al. 1975, Szalay and Dagosto 1980; Szalay and Drawhorn1980; Beard

1989, 1993a; Gingerich and Gunnell 1992; Boyer et al. 2001; Bloch and Boyer 2002,

2003; Bloch et al. 2003; Silcox and Gunnell 2008). Other skeletal evidence that indicate arboreality include hand proportions necessary for grasping. This adaptation has been observed in several plesiadapiform fossil taxa (Bloch and Boyer 2002, 2003; Silcox and

56 Gunnell 2008). For example, Carpolestes simpsoni had hands adapted for grasping and an opposable big toe with a nail like euprimates (Bloch and Boyer 2002; Gunnell and

Silcox 2008; Silcox and Gunnell 2008). In general, plesiadapiforms had claws on most digits, which would have afforded them the ability to climb on vertical supports.

Much of the plesiadapiform cranial morphology can be characterized as primitive and not euprimate like (Gunnell and Silcox 2008; Silcox and Gunnell 2008). They had long, low skulls with small brains and laterally facing orbits and lacked post orbital bars

(Gunnell and Silcox 2008; Silcox and Gunnell 2008). Plesiadapiforms often had well- developed sagittal crests and broad, widely splayed zygomatic arches where strong chewing muscles attached. They had large olfactory lobes (Gingerich and Gunnell 2005).

There are certain derived features of the cranium that they share with euprimates, which further supports plesiadapiforms being stem primates. In particular, the plesiadapids and

Carpolestes had auditory bullae that were formed from the petrosal bone (Russell 1959;

Szalay et al. 1987; Boyer et al. 2004; Bloch and Silcox 2006; Gunnell and Silcox 2008).

However, the paromomyids had auditory bullae that are more similar to non-euprimate archontans with an entotympanic element in the bulla (Kay et al. 1992; Bloch and Silcox

2001; Silcox 2003).

Dental characteristics shared between the euprimates and the plesiadapiforms included a postprotocingulum on the upper fourth premolar, low crowned bunodont molars, and a third lower molar (M3) hypoconulid that in most cases was larger than the hypoconulid on the first lower molar (M1; Gunnell and Silcox 2008; Silcox and Gunnell

57 2008). These derived cranial, dental, and skeletal traits are the basis for the argument that plesiadapiforms should be included in the Order Primates.

This article centers on the dental evolution of two genera, Ignacius and

Phenacolemur, within the plesiadapiform family Paromomyidae. The aims of this research are (1) to make an assessment of the general evolutionary patterns, or modes, of dental evolution that occurred in Ignacius and Phenacolemur; (2) to quantify rates of dental evolution that produced the morphological differences observed within and between species of Ignacius and Phenacolemur; and (3) to determine if biohorizon events coincide with increased rates of paromomyid dental evolution.

The Ignacius and Phenacolemur genera are closely related in both time and space and are similar in their dental morphology, which has made distinguishing them apart from one another a point of debate (Matthew and Granger 1921; Simpson 1935b; 1955;

Robinson 1968; Gazin 1971; Schiebout 1974; Krishtalka et al. 1975; Bown and Rose

1976; Krishtalka 1978; Rose 1981). Most researchers now agree that Ignacius and

Phenacolemur are sufficiently different to merit generic distinction (Bown et al. 1994b;

Bloch and Silcox 2001, 2006; Bloch et al. 2007; Secord 2008; Silcox et al. 2008; among others). Ignacius is hypothesized by several authors to be the ancestor of Phenacolemur

(Bown and Rose 1976; Szalay and Delson 1976; Rose and Gingerich 1976; Secord 2008).

In this case, Phenacolemur archus would be the link between the two genera as a morphological intermediate between Ignacius frugivorus and Phenacolemur pagei

(Secord 2008).

58 The genus Ignacius is known temporally to range in North America from the middle Paleocene, at the beginning of the North American land-mammal age (NALMA) second Torrejonian biochronological zone (biochron; To-2, ~62.7 Ma), to the top of the fourth Wasatchian biochron (Wa-4, ~54.2 Ma) of the early Eocene (Delson 1971; Scott et al. 2013; Schankler 1980; Rose 1981; Clyde 1997; Rose et al. 2012). The Phenacolemur genus overlaps temporally with the Ignacius genus, with its earliest representative known from the bottom of the fourth Tiffanian biochron (Ti-4, ~59.1 Ma) but extends beyond the temporal range of Ignacius to the end of the Wasatchian land-mammal age (Wa-7

~50.3 Ma; Sloan 1987; Gunnell 1994; Silcox et al. 2008).

Over a century of collecting from the Bighorn Basin has provided a large fossil record of Paleocene and early Eocene mammals, including the paromomyid primates

Ignacius and Phenacolemur, with a detailed record of their stratigraphic ranges (Sinclair and Granger 1912; Simpson 1928; Bown 1979; Gingerich 1975, 1976, 1980b; Schankler

1980; Bown and Kraus 1993; Bown et al. 1994b; Gingerich and Clyde 2001). The

Ignacius and Phenacolemur lineages survive two biostratigraphic zones of increased rates of species appearances and disappearances, termed Biohorizon A and B have been firmly established among the Bighorn Basin’s Willwood Formation mammals (Schankler 1980;

Chew 2009).

Ignacius fremontensis is the earliest known species of the genus and likely gave rise to I. frugivorus (Fig. 2.1; Bown and Rose 1976). Ignacius frugivorus is replaced by I. clarkforkensis, which is excluded from the present study due to small sample size, and I. clarkforkensis is replaced by I. graybullianus (Fig. 2.1; Bloch et al. 2007). Ignacius

59 graybullianus survives Biohorizon A but goes extinct at the beginning of Biohorizon B. I. frugivorus is the hypothesized ancestor to P. archus (also excluded from the present study due to a small sample), which is considered an intermediate form between I. frugivorus and P. pagei (Secord 2008). Phenacolemur praecox is a descendant species of

P. pagei (Fig. 2.1; Rose 1981; Secord 2008). Phenacolemur fortior descended from P. praecox around the beginning of Biohorizon A. This particular evolutionary transition is evidenced by the presence of intermediate forms collectively known as the P. praecox –

P. fortior intermediates (Fig. 2.1; Silcox et al. 2008). Phenacolemur citatus may have evolved from P. fortior (Fig. 2.1; Lopez-Torres et al. 2018) by budding cladogenesis but it is also possible that it evolved anagenetically from P. praecox around the beginning of

Biohorizon A (Fig. 2.1; Silcox et al. 2008). Phenacolemur simonsi is a likely ancestor of

P. willwoodensis, but the relationship between these two species and all other

Phenacolemur species remains unresolved (Fig. 2.1; Silcox et al. 2008). Phenacolemur simonsi survives Biohorizon A but goes extinct at Biohorizon B and P. willwoodensis appears after Biohorizon B (Silcox et al. 2008).

There are several instances where an evolutionary step from ancestor to descendant involved a shift in diet in this group of paromomyids. Lopez-Torres et al.

(2018) performed dental topographic analyses on the Paromomyidae, which included a

Dirichlet Normal Energy (DNE) analysis of the second lower molars. A DNE analysis calculates occlusal surface curvature (Bunn et al. 2011; Pampush et al. 2016; Winchester

2016). Lopez-Torres et al. (2018) compared their DNE results of paromomyid lower second molars to published data from modern primates of known diet, to reconstruct

60 paromomyid dietary categories. Lopez-Torres et al. (2018) concluded that the earliest

Ignacius species, I. fremontensis, was an omnivore based on the amount of occlusal surface curvature that it possessed. A shift from an omnivorous diet to an omnivorous- frugivorous diet occurred from I. fremontensis to I. frugivorus, which was evidenced by lesser amounts of occlusal surface curvature (smaller DNE values) in I. frugivorus (Fig.

2.1, López-Torres et al. 2018). All other later species of Ignacius were found to have

DNE values consistent with an omnivorous-frugivorous diet (Fig. 2.1, López-Torres et al.

2018). Phenacolemur archus, the likely intermediate between I. frugivorus and P. pagei, was an omnivore-insectivore, as indicated by higher DNE values, and P. pagei was an omnivore that exhibited DNE values that were intermediate between I. frugivorus and P. archus (Fig. 2.1, López-Torres et al. 2018). This suggests that two dietary shifts occurred between I. frugivorus and P. pagei. Later occurring paromomyid species included the omnivorous P. praecox and P. citatus. Phenacolemur fortior was an omnivore-frugivore with DNE values more similar to I. clarkforkensis and I. graybullianus (Fig. 2.1, López-

Torres et al. 2018). Therefore, a dietary shift occurred from P. praecox to P. fortior and then another shift occurred from P. fortior to P. citatus. Alternatively, if P. citatus descended from P. praecox and not P. fortior, then no dietary shift would have occurred between these two species (Fig. 2.1). Phenacolemur simonsi was an omnivore and P. willwoodensis was an insectivore-omnivore that exhibited some of the highest DNE values within Ignacius and Phenacolemur, suggesting a dietary shift occurred between these two species (Fig. 2.1, López-Torres et al. 2018).

61 The fine stratigraphic and temporal resolution of the samples and our knowledge of the paleoecological patterns during the late Paleocene and early Eocene allows me to test hypotheses about the tempo and mode of dental evolution that occurred in this group.

Based on ancestor-descendant relationships and dietary shifts (Fig. 2.1), I test the following hypotheses about the rate and mode of dental divergence for lower fourth premolar length, width, crown height, and protoconid height, as well as first, second, and third molar length and width: (1) directional evolution can explain the phenotypic differences observed in tooth metrics between I. fremontensis and I. frugivorous, since a dietary shift occurred; (2) since no dietary shifts occurred, the transition between I. frugivorus and I. graybullianus is marked by stasis in the tooth metrics; (3) directional evolution can explain the phenotypic differences observed in tooth metrics between I. frugivorus and P. pagei, since a dietary shift occurred; (4) since no dietary shifts occurred, the transition between P. pagei and P. praecox is marked by stasis in the tooth metrics; (5) directional evolution can explain the phenotypic differences observed in tooth metrics between P. praecox and P. fortior, since a dietary shift occurred; (6) directional evolution can explain the phenotypic differences observed in tooth metrics between P. fortior and P. citatus, since a dietary shift occurred; (7) since no dietary shifts occurred, the transition between P. praecox and P. citatus is marked by stasis in the tooth metrics; and (8) directional evolution can explain the phenotypic differences observed in tooth metrics between P. simonsi and P. willwoodensis, since a dietary shift occurred.

62 2.2 Materials and Methods

The Sample

The majority of the paromomyid fossil record consists of individual teeth and jaw fragments. The sample includes individuals of the paromomyid species Ignacius frugivorus, Ignacius grabullianus, Phenacolemur praecox, Phenacolemur fortior,

Phenacolemur citatus, Phenacolemur simonsi, and Phenacolemur willwoodensis from the

Willwood Formation of the southern Bighorn Basin, Wyoming. To ensure coverage of as many Ignacius and Phenacolemur species in my research, a few smaller published samples were from the Fort Union Formation of the northern Bighorn Basin, the Wasatch

Formation of the Chappo Type Locality of the Green River Basin, Wyoming (Secord

2008), and the Porcupine Hills Formation in the southwestern parts of the Alberta Basin,

(Scott 2003). These smaller samples included individuals of Ignacius frugivorus and

Phenacolemur pagei from the Fort Union Formation, Ignacius fremontensis specimens from localities in the Porcupine Hills Formation, and some individuals of Ignacius frugivorus from the Wasatch Formation.

All specimens included in this study have known stratigraphic levels within the

Fort Union Formation (Tiffanian, Ti-1 through Ti-6 and Clarkforkian, Cf-1 through Cf-3

NALMA; Rose 1981; Gingerich 1975, 1976), Porcupine Hills Formation (Torrejonian,

To-1 through To-3 NALMA; Archibald et al. 1987; Lofgren et al. 2004), Wasatch

Formation (Tiffanian NALMA; Dorr and Gingerich 1980; Gunnell 1994; Secord 2008) and the Willwood Formation (Wasatchian, Wa-0 through Wa-7 NALMA; Bown et al.

1994b). Fossils were either excavated, surface collected, or screenwashed from the

63 southern Bighorn Basin by expeditions from Yale (Y), University of Wyoming (UW),

United States Geological Survey (USGS), and Johns Hopkins University (JHU) between

1960 and the mid-1990s (Silcox et al. 2008). The sample from the Chappo Type Locality of the Green River Basin was collected by University of Michigan (UM) field crews and fossils from the Alberta Basin were collected by the Royal Tyrrell Museum of

Paleontology.

Ancestor – descendant relationships of Ignacius and Phenacolemur

Several authors have proposed relationships within and between species of

Ignacius and Phenacolemur (Bown and Rose 1976; Rose and Gingerich 1976; Szalay and

Delson 1979; Rose 1981; Bloch et al. 2007; Secord 2008; Silcox et al. 2008). These authors based their hypotheses of interspecies relatedness on similar dental and postcranial morphology, and geographic and stratigraphic occurrence. It is from these previous hypotheses that I compiled a proposed phylogeny of Ignacius and

Phenacolemur species (Fig. 2.1).

Eight proposed ancestor – descendant relationships between species of Ignacius and Phenacolemur were indicated from this phylogeny. Since my hypotheses of evolutionary mode rely on the presence or absence of a dietary shift between species, I needed to analyze each ancestor – descendant relationship independently. The following ancestor – descendant relationships were analyzed: Ignacius fremontensis – Ignacius frugivorus, Ignacius frugivorus – Ignacius graybullianus, Ignacius frugivorus –

Phenacolemur pagei, Phenacolemur pagei – Phenacolemur praecox, Phenacolemur praecox – Phenacolemur fortior, Phenacolemur fortior – Phenacolemur citatus,

64 Phenacolemur praecox – Phenacolemur citatus, and Phenacolemur simonsi –

Phenacolemur willwoodensis.

The Data

I obtained dental metrics for each species from published samples of Ignacius and

Phenacolemur collected in Wyoming and a small sample collected in Alberta. Maximum length and maximum width measurements of the P4, M1, M2, and M3 teeth, as well as P4 height and protoconid height of 653 individuals were obtained from the primary literature. Tooth measurement data for 549 individuals of Ignacius graybullianus,

Phenacolemur praecox, Phenacolemur fortior, Phenacolemur citatus, Phenacolemur simonsi, and Phenacolemur willwoodensis were provided by Mary Silcox, University of

Toronto who reported in Silcox et al. (2008) that measurements were made to the nearest

0.05 mm using digital calipers and followed the guidelines provided by Bloch and

Gingerich (1998: fig. 1). Eight individuals of Ignacius fremontensis were obtained from

Scott (2003) who measured length as the maximum anteroposterior length of the crown and measured both maximum labiolingual width of the talonid and trigonid separately; however, I took the maximum measurement of the widths reported by Scott (2003) for each tooth. I measured 68 individuals of Ignacius frugivorus and 28 individuals of P. pagei that were housed in the University of Michigan Museum of Paleontology in the same manner as that reported by Silcox (2008) and included them in this study.

Measurements of upper tooth positions or the anterior teeth of the lower dentition were excluded from the study due to small sample size.

65 Stratigraphy

The bulk of the specimens included in this study had known locality information that included a meter level within the southern or northern parts of the Bighorn Basin.

Sediment accumulation rates and maximum and minimum meter levels for middle

Paleocene to early Eocene North American Land Mammal Ages were provided to the authors by William Clyde and were based on works by several authors (Butler et al.

1981; Bown and Rose 1987; Bown et al. 1994b; Tauxe et al. 1994; Hamzi 2003;

Gradstein et al. 2012).

Geologic Age Estimates

To estimate rates of morphological evolution, a geologic age for each individual had to be determined. The stratigraphic and paleomagnetic research in the Bighorn Basin by several authors over the last few decades have made it possible to interpolate the geologic ages from the southern and northern Bighorn Basin sections (Bown et al. 1994b;

Clyde et al. 1994, 2001, 2007; Tauxe et al. 1994; Clyde 1997, 2001; Gingerich 2001;

Chew 2005; Secord et al. 2006). Meter level for each locality was provided in the dataset from Silcox et al. (2008). Basin, locality, and meter level was indicated on the specimen tags that I measured at the University of Michigan Museum of Paleontology. Individuals of Ignacius frugivorus from the type locality of the Chappo Member of the Wasatch

Formation in the Green River Basin are Ti-3 in age. Secord (2008) biostratigraphically correlated the Chappo Type Locality to the Polecat Bench section of the northern

Bighorn Basin. This provided the authors the ability to place the individuals from the

Chappo Type Locality in stratigraphic context with the rest of the Bighorn Basin sample.

66 Individuals of Ignacius fremontensis from the Who Nose? locality in the Porcupine Hills

Formation of the Alberta Basin are To-3 in age. The Alberta Basin has not been stratigraphically correlated to the Bighorn Basin so the authors used the average age of

To-3 (~61.3 Ma) for the eight Ignacius fremontensis individuals. For all other individuals age was calculated using equation one.

!"#$%&#' )#*+*)%$ ,)# = *+.#!/ ,)# *0 1%*2*'# 1*3'.,45 (7,) −

!"#"$ &"'"& () &(*+&,#- (!)0&(1"2# &"'"& () 3,(4(5" 3(657+$- (!) : ! ; (1) 2"7,!"5#+#,(5 $+#" ( ) "#

Establishment of Operational Stratigraphic Units (OSUs)

Operational stratographic units (OSUs) were created by binning samples from adjacent meter levels into a single unit. This was necessary because the method used to fit evolutionary models to a lineage requires an input of variable means and variances for each population forming the ancestor – descendant sequence. A challenge in dealing with paleontological data is that the number of specimens at each locality can vary and is at times small. Moreover, evolutionary mode cannot be predicted robustly from a short sequence of samples (Hunt 2008). To maximize both the number of OSUs in a sequence and the sample size in each OSU, species were divided into as many chronologically non- overlapping OSUs as possible while simultaneously avoiding individual tooth sample sizes lower than five, where possible, in any one OSU.

Ignacius fremontensis was poorly sampled with only eight individuals and could not be divided into multiple OSUs; however, I opted to keep I. fremontensis in the

67 analysis because it is the earliest member of the group and represents the starting point of the group’s radiation. Similarly, Phenacolemur willwoodensis only had eight individuals and was not divided into multiple OSUs but was kept in the analysis because it is of the youngest members of the group and represents one of the end points of the group. All other species were divided into two or more OSUs. Sample sizes and mean age for each

OSU are provided in Table 2.1.

Evolutionary Model Fitting and Rates

I performed time series analyses of morphological evolution on eight proposed ancestor – descendant relationships between species of Ignacius and Phenacolemur. I used the likelihood-based procedure described by Hunt (2006) using PaleoTS in the statistical package, RStudio. The variable means and variance, sample size, and age for each OSU was required to implement the test (Appendix B, Table B.1). Since some samples in the evolutionary sequences were poorly represented, I assumed that phenotypic variances were constant over all samples. For each analysis I performed a test for variance heterogeneity (Sokal and Rohlf 1995) to assess whether the data were consistent with this assumption. As suggested by Hunt (2006), I substituted each estimate of phenotypic variance with the variance pooled over all samples to increase the precision with which phenotypic variance is estimated.

Sample ages for each OSU were measured in years, since I assumed a one-year generation time for species of Ignacius and Phenacolemur. This assumption was based

2 on the average M1 tooth size for all species (4.43 mm ) included in the analysis. I used the regression equation, Ln B = 1.563 x Ln A + 2.728, to estimate an average body mass

68 for species of Ignacius and Phenacolemur (174.25 grams; see Appendix C). I then used the regression equation, Ln B = 0.355 x Ln A -1.801, to estimate generation time in years

(1.0 years; see Appendix C).

I fit five evolutionary models (strict stasis, stasis, an unbiased random walk

(URW), directional evolution (GRW), and an Ornstein-Uhlenbeck (OU) process) to each natural log transformed variable (P4, M1, M2, and M3 length and width and P4 height and protoconid height). Strict stasis was modeled as zero variance around the long-term mean

(Hunt et al. 2015) and stasis was modeled as uncorrelated variation around a stable mean

(Sheets and Mitchell 2001; Hunt 2006). An unbiased random walk was modeled as independent trait increments that have an equal likelihood of increasing or decreasing.

Directional evolution was modeled as independent trait increments that have either a greater likelihood of increasing or decreasing through time (Hunt 2006). An Ornstein-

Uhlenbeck process was modeled as a combination of directional and stabilizing natural selection, with an initial directional trend that becomes increasingly more stabilizing as the population nears the adaptive optimum (Hunt et al. 2008). Model fit was measured using the bias-corrected version of the Akaike Information Criterion (AICc) (Akaike

1974; Hurvich and Tsai 1989; Anderson et al. 2000). Relative support for the models was determined with Akaike weights of 0 to 1, where 0 represents no support and 1 represents full support of the models (Anderson et al. 2000).

Hunt (2012) derived rate metrics by formulating an expected change in a trait as a function of time. The models predict that evolutionary changes will have a Gaussian distribution with means and variance that depend on elapsed time and the model

69 parameters (Hunt 2006, 2008). The model for stasis has two parameters: - and . (Table

2.2). The parameter - is analogous to the position of the trait at the adaptive optimum and the parameter . represents the amount of variance that fluctuates around a fixed mean.

When . is zero, this is considered stasis in its strictest sense implying that no real evolutionary variation occurred in a trait (i.e. strict stasis). The directional evolution model selects an evolutionary change for each generation from a distribution of evolutionary “steps” that has a mean step, /#, corresponding to the directional bias in trait

' values per-generation and a step variance, 0#$%&, which represents the deviations from the trend (Table 2.2; Hunt 2012). Ancestor – descendant changes, ∆X, will have a normal

' distribution after t generations with a mean /#$%&t and variance 0#$%&t (Table 2.2; Hunt

2006, 2012). The random walk model is similar to the directional model, except with a mean of zero (/#$%&= 0), thus ∆X will have a normal distribution and variance equal to

' 0#$%&, (Table 2.2; Hunt 2006, 2012). The OU model, as applied here, describes the evolution of a population near a fixed adaptive peak. The parameters z0 and -, define the ancestral trait, or initial trait value, and the position of the trait at the adaptive optimum,

' respectively. The parameters 1 and 0#$%& define the nature of the evolutionary trend from the ancestral trait as it approaches the adaptive optimum (Table 2.2; Hunt et al. 2008).

When values of 1 increase, so too does the pull of the selective force to the optimum. If values of 1 are very high, species are pulled so quickly to the optimum that the evidence of this history is not likely to be preserved in the fossil record (Felsenstein 1988; Hansen

1997). Hunt’s (2006, 2008) likelihood methods developed for the PaleoTS R package

' ' estimate the model parameters ., 0#$%&, and /#$%&, 1, and -. 70 For instances where the OU model receives the highest support, I use the OU model parameters, which can be related to the population genetic characteristics of the evolving lineage and to the nature of the adaptive landscape (Hunt et al. 2008), to estimate the underlying population genetic and selective conditions. Genetic drift produces the step variance component of the OU model and is equal to

' 2 ' 0#$%&= h 0& /3%, (2)

2 ' where h represents trait heritability, 0& is the trait variance of the sample, and 3% is the effective population size (Lande 1976). The pull of the selective force is

! ! ( )" 1 = ! ! , (3) * +)" where the parameter .' indicates the strength of stabilizing natural selection (Lande

1976). When stabilizing selection is weak and normally distributed, the fitness of individuals (Lande 1976; Estes and Arnold 2007) can be expressed as:

( )! 4(*) = 567 8− -./ :. (4) '*!

The above term, .', is equivalent to a variance; the fitness function becomes increasingly dispersed and stabilizing selection gradually weaker as .' increases. When

' ' . is much greater than 0& , stabilizing selection is weak and therefore, the parameter 1 is directly proportional to the additive genetic variance and inversely proportional to .'.

' Using the above expressions, the parameter estimates of 1 and 0#$%& are used to estimate the population genetic and selective conditions. To obtain an estimate of 3%, equation 2 is rearranged to give

! ! ( )" 3% = ! . (5) )#$%" 71 For the term h2, the range 0.1 to 0.7 is used as plausible values for morphological trait heritability (Roff 1997; Relyea 2005). The other terms in equation 5 are estimated from

' ' the model fit (0#$%&) and the samples themselves (0& ). Estimates of 3% offer another way to check the OU model fit to the lineage because if the model is true, estimates of 3% will be similar among different phenotypes measured from the same lineage and should be plausible given the lineage under study (Hunt et al. 2008). Using equation 3 I can solve for .' by

' ' ' . = 0& (ℎ 1 − 1), (6) which provides us with an estimate of the strength of stabilizing selection around the optimum trait (Hunt et al. 2008). Alternatively, the strength of the restrictive force around the optimum can be expressed as

, = 34 ('), (7) 1/' 6 the amount of time of time it takes for a population to evolve halfway to the phenotypic optimum (Hansen 1997) and is considered the phylogenetic half-life.

The tempo of evolutionary change is tightly linked to the mode of evolution

(Roopnarine 2003). Traditional rate metrics are influenced by temporal scale, which differs under different evolutionary scenarios and renders comparisons of rates among different modes of evolution impractical (Gingerich 1993; Roopnarine 2003). To avoid this issue, I use the estimated squared divergence (ESD) as a means to compare rates of phenotypic divergence among sequences of different evolutionary modes. I calculate

ESD using the resulting parameter estimates of the best-supported model for one generation and one million generations. An ESD measures an average of squared 72 deviations taken with respect to the ancestral trait value (X0; Hunt 2012). ESD is equal to

?' + A for any probability distribution of evolutionary changes with mean ? and variance A (Kendall and Stuart 1969: p. 58). This equation is characterized by a directional component, ?', and a non-directional component, A (Hunt 2012). Given that mean and variance of ∆X is known for the five models of evolution, one can simply calculate ESD for each model as a function of elapsed time (Table 2.2; Hunt 2012).

These predicted ESDs are comparable across sequences even if the underlying model of evolution is different.

The ESD for the random walk model is determined by the variance of the

' distribution of evolutionary steps, 0#$%& (Hunt 2012). There is a positive correlation

' between ESD and time, and the variance of the distribution of evolutionary steps, 0#$%&, is equal to the slope, or rate of phenotypic change. For the stasis models, the ESD is calculated using the terms - − B7, which comprises the pull of the trait to the long-term mean, and ., the variance around the optimal trait value (Hunt 2012). ESD for the stasis model is predicted by taking the expectation over all ancestral trait values, where the value of - − B8 equals the trait variance, ., resulting in the expression 2. for ESD

(Table 2.2; Hunt 2012). Elapsed time is not a factor in the computation of ESD under stasis (Hunt 2012). As a result, the same amount of phenotypic change is expected regardless of the number of generations separating samples (Hunt 2012). For directional evolution, ESD is calculated as the sum of the maximum-likelihood estimate of the mean

' ' (/#$%&) step distribution and the maximum-likelihood estimate of the variance (0#$%& ) of

73 the step distribution (Table 2.2; Hunt 2012). Hansen (1997) provides the expected (mean) trait value over time for an Ornstein-Uhlenbeck process as:

?(B) = [(1 − exp (−1,)- + exp (−1,)B9] (3) with parameters -, the position of the trait at the adaptive optimum, and 1, the pull of the selective force around the adaptive optimum (Hunt et al. 2008) as explained above. The change in a trait from ancestor to descendant, ∆X, is equal to the initial trait value, X0, subtracted from the expression above, which simplifies to

?(∆B) = [1 − exp(−1,)](- − B9). (4)

The variance of the trait value provided by Hansen (1997) can be equated to the variance of the difference between ancestral and descendant trait values and is

)! A(∆B) = #$%" (1 − 567[−21,]). (5) '6

Equations three and four can be substituted for ? and A in the ESD equation, ?' + A.

' ' All model parameters (., 0#$%&, and /#$%&, 1, and -) were estimated using Hunt’s (2006)

PaleoTS R package.

2.3 Results

Modes and Rates of Morphological Evolution: Ignacius fremontensis – Ignacius frugivorus

The transition between I. fremontensis and I. frugivorus included a dietary shift from an omnivorous diet to an omnivorous-frugivorous diet during the late Paleocene. As a result, I expected that directional evolution occurred in the tooth metrics that I observed.

74 The best fit mode of evolutionary phenotypic differentiation in length and width of each tooth for the Ignacius fremontensis – Ignacius frugivorus suggest that the P4 and

M1 teeth were experiencing similar evolutionary pressures that were different from the

M2 teeth. Length and width for all teeth increased over the course of the lineage (Fig.

2.2). Directional change is the most strongly supported model for P4 and M1 length and width and an Ornstein-Uhlenbeck process is strongly supported for M2 length and width.

Estimates and ranges for population genetic and selective parameters are listed in Table

2.3 and maximum-likelihood parameter estimates and ESD estimates for one generation and one million generations for each model are listed in Table 2.4.

Model fitting results for P4 and M1 length and width show that directional evolution is the most strongly supported model. Visually, the observed phenotypic changes for P4 and M1 length and width fit reasonably well to the directional model, with most sample means aligning within the 95% probability range (Fig. 2.2). The latest I. frugivorus OSU sample mean falls slightly below the 95% probability interval for P4 length, width, and M1 width (Fig. 2.2). For the P4 and M1 teeth, the mean evolutionary

-8 -7 transition, /#$%&, ranged from 7.31 x 10 to 1.60 x 10 natural log transformed

' millimeters (ln mm) per generation and the variance of the evolutionary transitions, 0#$%&, ranged from 0.000 to 1.68 x 10-8 ln mm2 per generation (Table 2.4).

Model fitting results for M2 length and width show that the OU model outperforms all other models. Qualitatively, the observed trait trajectories for M2 length and width show a good fit to the OU model, with all OSU sample means within the 95% probability interval. Though it appears that the populations are climbing to a new

75 adaptive peak, with only three sample means available for this lineage, it is difficult to ascertain whether the trends in trait means reflect a true OU process or if they are merely mimicking that of an OU process.

For M2 length and width, there is a net displacement of 4.75 and 4.45 standard deviation units, respectively, between the initial trait value and the optimal phenotype

' (Table 2.3). The variance of evolutionary transitions, 0#$%&, for M2 length and width are both 1.00 x 10-10 ln mm2 per generation, which suggests that input from genetic drift was very small. Assuming a trait heritability range for morphological characters of 0.1 to 0.7, the strength of stabilizing selection around the optimum phenotype is calculated from the parameter .'. Estimates for .' are much larger than the sample phenotypic variances,

' 0 &, for both length and width of M2 (Table 2.3), indicating that these traits experienced weak stabilizing selection around the optimal phenotype. The time estimated for the population to reach half the distance to the optimum phenotype, t1/2, is quite large,

' between 433,000 and 630,000 generations. Estimates of t1/2 and . are consistent with each other because if stabilizing selection around the optimum phenotype is weak, then large estimates of t1/2 are reasonable as it would take longer for the population to reach the phenotypic optimum. The effective population size, Ne, calculated for length and width are in agreement with each other, which is expected for traits evolving within the same population.

Expected squared divergence estimates for P4 and M1 tooth metrics increase by a factor of six from one generation to one million generations. For P4 length and width

ESD is 5.13 x 10-14 and 3.44 x 10-14, respectively, per generation and 5.13 x 10-8 and 3.44

76 -8 x 10 , respectively, per one million generations (Table 2.4). M1 length and width have

ESD estimates of 1.68 x 10-8 and 2.69 x 10-14, respectively, per generation and 1.68 x 10-2

-8 and 2.69 x 10 per one million generations (Table 2.4). The M2 tooth length and width

ESD estimates were both 1.00 x 10-10 per generation and 4.91 x 10-2 and 7.11 x 10-2, respectively, per one million generations.

Modes and Rates of Morphological Evolution: Ignacius frugivorus – Ignacius

graybullianus

The Ignacius frugivorus – Ignacius graybullianus lineage persists through

Biohorizon A and goes extinct just before Biohorizon B. The transition between I. frugivorus and I. graybullianus involved the transition species I. clarkforkensis.

However, the sample of I. clarkforkensis was insufficient to include in the analysis. There was no dietary shift that occurred between these species and I predicted that the transition would be marked by stasis in the tooth metrics I observed.

My results show that the best fit mode of evolutionary phenotypic differentiation in tooth metrics of each tooth for the Ignacius frugivorus – Ignacius graybullianus suggest that all teeth experienced the same evolutionary pressures. Length and width of the molars and P4 height increased, while P4 protoconid height decreased over the course of the lineage (Fig. 2.3). The model for an Ornstein-Uhlenbeck process has full support for all teeth. Estimates and ranges for population genetic and selective parameters are listed in Table 2.5 and maximum-likelihood parameter estimates and ESD estimates for one generation and one million generations for each model are listed in Table 2.6.

77 Model fitting results for all tooth metrics show that the OU model outperforms all other models. Visual appraisal of the observed phenotypic trajectories for all tooth metrics could be interpreted as populations climbing an adaptive peak – trait shifts to the new optimum are large, but then become smaller and nondirectional when the optimum is reached (Fig. 2.3). However, having only two OSUs for each species makes it challenging to differentiate between a real or mimicked OU process. The OSU sample means for the P4 tooth metrics are not in good agreement with the expectation of the OU model, as several means fall outside of the 95% probability interval (Fig. 2.3). The match between model and sample means fit better for the M1 and M2 tooth metrics, with only the first I. graybullianus OSU falling outside of the 95% probability interval (Fig. 2.3).

There is a net displacement between the initial trait value and the optimum trait value of 0.560 to 3.08 standard deviation units for all tooth metrics (Table 2.5). The

' variance of evolutionary transitions, 0#$%&, for P4 length, width, protoconid height, and

-10 2 height are all 1.00 x 10 ln mm per generation (Table 2.6) and step variance for M1 and

-10 2 M2 length and width ranged from 2.87 x 10 ln mm per generation (M2 length) to 8.32 x

-9 2 10 ln mm per generation (M1 length), which suggests minimal input from genetic drift.

Assuming plausible values of trait heritability (0.1 – 0.7), the strength of stabilizing selection around the optimal phenotype is computed from the parameter, .'. With the

' exception of P4 length and protoconid height, the estimates for . are much greater than

' the sample phenotypic variances, 0 &, for all tooth metrics (Table 2.5), suggesting that these traits experienced weak stabilizing selection around the optimal phenotype (Lande

1976; Estes and Arnold 2007). This finding aligns with the time estimated for the

78 population to traverse half the distance to the optimum phenotype, which for all tooth metrics other than P4 length and protoconid height is between 685,000 – 1,370,000

' generations (Table 2.5). The opposite is found for P4 length and protoconid height, . is lower than the phenotypic variances of the sample, which suggests that stabilizing selection around the optimum phenotype was strong. The estimated time for the population to traverse half the distance to the optimum P4 length and protoconid height phenotype is between 0.441 and 1.12 generations (Table 2.5). Estimates of Ne for M1 length and width are in good agreement with each other; however, Ne estimates for P4 and

M2 have a large range, between 885,000 and 879,000,000, which may indicate that the

OU model is not true for some of these tooth metrics (Table 2.5).

Estimates for ESD at the per generation time scale range from 1.00 x 10-10 to 8.44 x 10-3 and at the per one million generations time scale range from 4.42 x 10-3 to 3.98 x

-2 -3 10 for all teeth. ESD estimates are highest for P4 protoconid height (8.44 x 10 per

-2 generation and 3.98 x 10 per million generations; Table 2.6). For P4 length, width, and height ESD estimates are 2.77 x 10-3, 1 x 10-10, and 1.00 x 10-10, respectively, per generation and 4.42 x 10-3, 1.93 x 10-2, and 8.30 x 10-3, respectively, per one million

-9 generations (Table 2.6). M1 length and width have ESD estimates of 8.32 x 10 and 7.90 x 10-9, respectively, per generation and 7.11 x 10-3 and 2.00 x 10-2, respectively, per one million generations (Table 2.6). The M2 tooth length and width ESD estimates are 2.87 x

10-10 and 5.85 x 10-10, respectively, per generation and 7.21 x 10-3 and 4.41 x 10-3, respectively, per one million generations (Table 2.6).

79 Modes and Rates of Morphological Evolution: Ignacius frugivorus – Phenacolemur pagei

The transition between Ignacius frugivorus – Phenacolemur pagei occurred during the late Paleocene and included a dietary shift. I predicted that directional evolution occurred in the tooth metrics that I observed.

The best fit mode of evolutionary phenotypic differentiation in tooth metrics for the I. frugivorus – P. pagei suggest that the P4 and M1 teeth were experiencing similar evolutionary pressures that were different from the M2 teeth. All tooth metrics increased over the course of the lineage (Fig. 2.4). The model of an Ornstein-Uhlenbeck process has the highest support for the P4 and M1 teeth and directional evolution is strongly supported for M2 length and width. Estimates and ranges for population genetic and selective parameters are listed in Table 2.7 and maximum-likelihood parameter estimates and ESD estimates for one generation and one million generations for each model are listed in Table 2.8.

The Ornstein-Uhlenbeck model is strongly supported for the P4 and M1 teeth.

Visually, the P4 and M1 tooth metrics are in good approximation with the expectation of the OU model, as almost all OSU sample means fall within the 95% probability interval

(Fig. 2.4). The phenotypic trajectories of the P4 and M1 teeth could be interpreted as populations climbing towards a new adaptive peak; however, when a lineage consists of only four OSUs it is difficult to know if true evolutionary patterns are being depicted.

The model fits for P4 length, width, protoconid height and height suggest a net displacement between the initial trait value (I. frugivorus OSU-1) and the optimum trait

80 value of 5.03, 6.81, 3.10, and 4.83 standard deviation units (Table 2.7). The model fits for

M1 length and width suggest a net displacement between the initial trait value and the optimum trait value of 1.86 and 3.89 standard deviation units (Table 2.7). The variance of

' the evolutionary transitions, 0#$%&, for P4 length, width, protoconid height, and height are

5.06 x 10-8 ln mm2, 1.16 x 10-7 ln mm2, 6.96 x 10-8 ln mm2 and 6.22 x 10-8 ln mm2,

-9 -9 respectively, per generation and for M1 length and width are 6.97 x 10 and 1.53 x 10 , respectively, suggesting minimal input from genetic drift (Table 2.8). The strength of stabilizing selection around the optimal phenotype, .', are much greater than the sample phenotypic variances for all tooth metrics (Table 2.7), which indicates that these traits experienced weak stabilizing selection around the optimal phenotype. This is in good agreement with phylogenetic half-life estimates, t1/2, which range from 715,000 to

1,410,000 generations (Table 2.7). Apart from P4 width and M1 width, effective population sizes are comparable across traits and aligns with the expectation for traits measured from the same evolving populations. Effective population size estimates are lower for P4 width are higher for M1 width than estimates for the other traits (Table 2.7) and may indicate that an OU process was not responsible for producing the observed trait evolution in these teeth.

Directional evolution is strongly supported for M2 length and width. Visually, there is good agreement between the expectation for directional evolution, with sample means that fall within the 95% probability interval. For the M2 teeth, the mean

-8 evolutionary transition, /#$%&, is ≤ 4.48 x 10 ln mm per generation for length and width

81 ' 2 and the variance of the evolutionary transitions, 0#$%&, is 0 ln mm per generation for both length and width (Table 2.8).

Expected squared divergence estimates for P4 length, width, and height are 5.06 x

10-8, 1.16 x 10-7, and 6.22 x 10-8, respectively, per generation and 1.16 x 10-1, 1.75 x 10-1,

-1 and 1.56 x 10 , respectively, per one million generations (Table 2.8). M1 length and width have ESD estimates of 6.97 x 10-9 and 1.53 x 10-9, respectively, per generation and

-3 -2 6.44 x 10 and 1.89 x 10 , respectively, per one million generations (Table 2.8). The M2 tooth length and width ESD estimates are 4.01 x 10-15 and 2.85 x 10-15, respectively, per generation and 4.01 x 10-9 and 2.85 x 10-9, respectively, per one million generations

(Table 2.8).

Modes and Rates of Morphological Evolution: Phenacolemur pagei – Phenacolemur praecox

The Phenacolemur pagei – Phenacolemur praecox lineage goes extinct at the beginning of Biohorizon A. No dietary shift occurred between these species and I predicted that the transition between P. pagei and P. praecox is marked by stasis in the tooth metrics I observed.

The best fit modes of evolutionary phenotypic differentiation in tooth metrics for the Phenacolemur pagei – Phenacolemur praecox suggest that the M1 and M2 teeth were experiencing similar evolutionary pressures that were different from the P4 teeth. All tooth metrics except for P4 width increased, to some degree, over the course of the lineage (Fig. 2.5). The model of an unbiased random walk has the highest support for P4 protoconid height and width and M1, M2 and M3 length and width. The strict stasis model

82 is strongly supported for P4 height and length (Fig. 2.5; Table 2.9). Maximum-likelihood parameter estimates and ESD estimates for one generation and one million generations for each model are listed in Table 2.9.

For P4 height and length, the strict stasis model shows the highest support.

Visually, the data fit reasonably well to the model. The second P. pagei OSU for both P4 length and height lie outside of the 95% probability range and the third P. praecox OSU sample mean for P4 height lies outside of this interval (Fig. 2.5). Under the strict stasis model, trait means converge immediately to the optimum, -, and have essentially zero

2 variance around the optimum (. = 0 ln mm ). The optimum phenotypes for P4 height and length are 1.14 and 1.19 ln mm, respectively. The model of a random walk has the highest support for P4 protoconid height and P4 width and M1, M2 and M3 length and width. The data fit well within the expectation of a random walk, with all sample means falling within the 95% probability interval (Fig. 2.5).

Under the random walk model, ESD is solely reliant on the magnitude of the step variance. The step variances for P4 width, P4 protoconid height, and M1, M2, and M3

-9 2 -8 2 length and width ranges from 5.11 x 10 ln mm (M1 width) to 3.67 x 10 ln mm (M2 length) per generation, which subsequently corresponds to the lowest and highest ESD estimates (Table 2.9). Expected squared divergence estimates for P4 length, protoconid height, and crown height, are 1.12 x 10-3 and 3.32 x 10-3, respectively, per generation and

1.12 x 10-3 and 3.32 x 10-3, respectively, per one million generations (Table 2.9). ESD estimates calculated for one million generations are the same as those calculated for one generation because time is not a factor in the ESD under the strict stasis and stasis models

83 -9 (Table 2.9). For P4 width and protoconid height, ESD estimates are 5.20 x 10 and 1.29 x

10-8, respectively, per generation and 5.20 x 10-3 and 1.29 x 10-2, respectively, per one

-9 million generations (Table 2.9). M1 length and width ESD estimates are 8.94 x 10 and

5.11 x 10-9, respectively, per generation and 8.94 x 10-3 and 5.11 x 10-3, respectively, per one million generations (Table 2.9). The M2 tooth length and width ESD estimates are

3.67 x 10-8 and 7.08 x 10-9, respectively, per generation and 3.67 x 10-2 and 7.08 x 10-3, respectively, per one million generations (Table 2.9). M3 length and width have ESD estimates of 2.16 x 10-8 and 1.53 x 10-8, respectively, per generation and 2.16 x 10-2 and

1.53 x 10-2, respectively, per one million generations (Table 2.9).

Modes and Rates of Morphological Evolution: Phenacolemur praecox –

Phenacolemur fortior

The Phenacolemur praecox – Phenacolemur fortior lineage persists through

Biohorizon A and goes extinct at the beginning of Biohorizon B. Speciation occurs at the beginning of Biohorizon A. There was no dietary shift that occurred between these omnivorous species and I predicted that the transition between these species would be marked by stasis in the tooth metrics that I observed.

The best fit modes of evolutionary phenotypic differentiation in tooth metrics for the P. praecox – P. fortior suggest that the P4 was on a different evolutionary trajectory from the molars. Over the course of the lineage, P4 height and protoconid height decreased, while length and width increased (Fig. 2.6). All molar lengths and M1 width stayed roughly the same size, while M2 and M3 widths slightly increased over the course of the lineage. The model of an unbiased random walk has the highest support for all P4

84 tooth metrics, while stasis and the strict stasis models are strongly supported for M1, M2, and M3 lengths and widths (Fig. 2.6; Table 2.10).

The model of an unbiased random walk had the highest support for all P4 tooth metrics. Visually, the data fit well to the expectation of the random walk model, with none of the observed sample means falling outside of the 95% probability interval (Fig.

2.6). The stasis model was most strongly supported for M1 length and the strict stasis model is strongly supported for M1 width and M2 and M3 length and width. The majority of the sample means fit well to the highest supported model. The sample means of the first P. fortior OSU for M1 and M2 width fall outside of the 95% probability interval and the third P. praecox OSU falls outside of this interval for M2 length.

Under the random walk model, ESD depends on the magnitude of the step variance. The step variances for P4 length, width, protoconid height, and height ranges

-9 2 -8 2 from 1.86 x 10 ln mm (P4 length) to 8.94 x 10 ln mm (P4 protoconid height; Table

2.10) per generation. For P4 length, width, protoconid height, and height, ESD estimates are 2.31 x 10-2, 5.48 x 10-9, 8.94 x 10-8, and 1.64 x 10-8, respectively, per generation and

2.31 x 104, 5.48 x 10-3, 8.94 x 10-2, and 1.64 x 10-2, respectively, per one million

-3 generations (Table 2.10). ESD estimates for M1 length and width are 0 and 1.06 x 10 , respectively, per generation and per one million generations (Table 2.10). The M2 tooth length and width ESD estimates are 5.20 x 10-4 and 4.81 x 10-4, respectively, per generation and per one million generations (Table 2.10). M3 ESD estimates are 0 for both length and width per generation and per one million generations (Table 2.10). ESD estimates calculated for one million generations are the same as those calculated for one

85 generation because elapsed time is not a factor in the ESD under the models for strict stasis and stasis (Table 2.10). Under the strict stasis model, trait means are constant and at

2 or near the optimum (. = 0 ln mm ). For M1 length and M3 length and width, the trait mean is at the optimum phenotype of 1.02 ln mm, 1.31 ln mm, and 0.723 ln mm, respectively. For M1 width, the optimum phenotype is 0.822 ln mm and the variance around the optimum is 5.31 x 10-4 ln mm2.

Modes and Rates of Morphological Evolution: Phenacolemur fortior – Phenacolemur citatus

The Phenacolemur fortior – Phenacolemur citatus lineage begins at Biohorizon A and persists beyond Biohorizon B. Speciation occurred at the beginning of Biohorizon A and the transition involved a dietary shift from an omnivorous diet to an omnivorous- frugivorous diet. I predicted that directional evolution occurred between these species in the tooth metrics I observed.

The best fit modes of evolutionary phenotypic differentiation in tooth metrics for the Phenacolemur fortior – Phenacolemur citatus suggest that all tooth metrics were experiencing similar evolutionary pressures. Over the course of the lineage, P4 height and protoconid height increased, while length and width decreased (Fig. 2.7). First and second molar lengths and M3 width decreased, while M3 length stayed roughly the same over the course of the lineage. The model of an unbiased random walk has the highest support for all tooth metrics, except for M3 width (Fig. 2.7; Table 2.11). The strict stasis model had the highest support for M3 width (Fig. 2.7; Table 2.11). Maximum-likelihood

86 parameter estimates and ESD estimates for one generation and one million generations for each model are listed in Table 2.11.

Qualitatively, the data fit well to the expectation of the random walk model, with none of the observed sample means falling outside of the 95% probability interval (Fig.

2.7). Only one data point fell outside of the 95% probability interval of the stasis model for the M3 tooth metric. Under the random walk model, ESD depends on the magnitude

' of the model parameter for the step variance, 0#$%&. The step variances for P4 length, width, protoconid height, and height, ESD estimates are 4.29 x 10-8, 3.32 x 10-8, 8.81 x

10-8, and 4.65 x 10-8, respectively, per generation and 4.29 x 10-2, 3.32 x 10-2, 8.81 x 10-2, and 4.65 x 10-2, respectively, per one million generations (Table 2.11). ESD estimates for

-9 -8 -3 M1 length and width are 5.96 x 10 and 1.39 x 10 per generation and 5.96 x 10 and

-2 1.39 x 10 , respectively, per one million generations (Table 2.11). The M2 tooth length and width ESD estimates are 5.65 x 10-9 and 7.77 x 10-9, respectively, per generation and

-9 per one million generations (Table 2.11). ESD estimates for M3 Length are 8.13 x 10 per generation and 8.13 x 10-3 per one million generations (Table 2.11). The ESD estimate for M3 width is 0 per generation and 0 per one million generations.

Modes and Rates of Morphological Evolution: Phenacolemur praecox –

Phenacolemur citatus

The Phenacolemur praecox – Phenacolemur citatus lineage persists through both

Biohorizon A and Biohorizon B. Speciation occurs at the beginning of Biohorizon A and did not involve a dietary shift from the omnivorous ancestral diet of P. praecox. I

87 predicted that the transition between these species would be marked by stasis in the tooth metrics I observed.

The best fit modes of evolutionary phenotypic differentiation in tooth metrics for the Phenacolemur praecox – Phenacolemur citatus suggest that all tooth metrics apart from M2 length were on similar evolutionary trajectories. All tooth metrics decreased from the latest P. praecox sample to the earliest P. citatus sample but increased again back towards the initial phenotype (Fig. 2.8). The model of an unbiased random walk has the highest support for all tooth metrics except for M2 length, which has the strongest support for the stasis model (Fig. 2.8; Table 2.12). Maximum-likelihood parameter estimates and ESD estimates for one generation and one million generations for each model are listed in Table 2.12.

The model of an unbiased random walk had the highest support for P4 protoconid height and crown height and P4, M1, and M3 length and width and M2 width.

Qualitatively, the data fit well with the expectation of the random walk model, as none of the observed sample means are outside of the 95% probability interval (Fig. 2.8). The stasis model was strongly supported for M2 length. Visually, M2 length sample means match well with the expectation of the 95% probability interval. The optimum value for

-3 2 M2 length is 0.973 ln mm and the variance around this optimum, ., is 1.29 x 10 ln mm per generation (Table 2.12).

Expected squared divergence for the random walk model depends on the magnitude of the step variance and scales temporally. For P4 length, width, protoconid height, and height, ESD estimates are 2.32 x 10-8, 1.05 x 10-8, 7.14 x 10-8, and 4.40 x 10-2,

88 respectively, per generation and 2.32 x 10-2, 1.05 x 10-2, 7.14 x 10-2, and 4.40 x 104, respectively, per one million generations (Table 2.12). ESD estimates for M1 length and width are 2.63 x 10-9 and 4.81 x 10-9, respectively, per generation and 2.63 x 10-3 and

4.81 x 10-3, respectively, per one million generations (Table 2.12). The ESD estimate for

-9 -3 M2 width is 3.33 x 10 per generation and 3.33 x 10 per one million generations (Table

-9 -9 2.12). ESD estimates for M3 length and width are 3.33 x 10 and 1.28 x 10 per generation and 3.33 x 10-3 and 1.28 x 10-3 per one million generations (Table 2.12). The

-3 -3 ESD estimate for M2 length is 2.58 x 10 per generation and 2.58 x 10 per one million generations (Table 2.12). The ESD estimates for traits evolving under stasis are the same whether one computes them over one million generations or one generation because elapsed time is not a factor in the ESD under the models for stasis.

Modes and Rates of Morphological Evolution: Phenacolemur simonsi –

Phenacolemur willwoodensis

The Phenacolemur simonsi – Phenacolemur willwoodensis lineage persists through Biohorizon A and Biohorizon B. Speciation occurs at the beginning of

Biohorizon B and involves a dietary shift from an omnivorous diet to an insectivorous- omnivorous diet. I predicted that directional evolution occurred between P. simonsi and

P. willwoodensis in the tooth metrics that I observed.

The best fit modes of evolutionary phenotypic differentiation in tooth metrics for the Phenacolemur simonsi – Phenacolemur willwoodensis suggest that the P4 tooth metrics were under different evolutionary pressures than the molars. All tooth metrics increased in size over the course of the lineage (Fig. 2.9). The random walk model is

89 most strongly supported for P4 length and P4 width, while an Ornstein-Uhlenbeck model is fully supported for P4 protoconid height and P4 crown height. The strict stasis model is most strongly supported for M1, M2, and M3 length and width. Estimates and ranges for population genetic and selective parameters are listed in Table 2.13 and maximum- likelihood parameter estimates and ESD estimates for one generation and one million generations for each model are listed in Table 2.14.

The model of an unbiased random walk has the highest support for P4 length and width. Visually, the data fit well with the expectation of the random walk model, as none of the observed sample means for P4 length and width fall outside of the 95% probability region (Fig. 2.9). Model fitting results for P4 protoconid height and height show that the

OU model outperforms all other models. Qualitatively, the phenotypic trajectories of P4 protoconid height and height observed could be interpreted as populations climbing an adaptive peak but having only one P. willwoodensis OSU makes it challenging to definitively say if the trend truly plateaued around a new phenotypic optimum. The expected trajectory of the OU model and observed data match well for P4 protoconid height, as none of the observed sample means fall outside the 95% probability region

(Fig. 2.9). The match between model and data fit less well for P4 height as the means of the last OSU sample of P. simonsi and the single P. willwoodensis sample fall outside of the 95% probability region (Fig. 2.9).

The model fits for P4 protoconid height and height suggest a net displacement between the initial trait value (P. simonsi OSU-1) and the optimum trait value of 1.00 to

1.67 standard deviation units (Table 2.13), respectively. The variance of the evolutionary

90 ' -8 2 transitions, 0#$%&, for the P4 protoconid height and height are 2.05 x 10 ln mm and 1.00 x 10-10 ln mm2, respectively, per generation (Table 2.14) suggesting minimal input from genetic drift. Estimates for .' suggest that the traits experienced weak stabilizing selection around the optimal phenotype, which aligns with the high estimates for the time estimated for the population to traverse half the distance to the optimum phenotype, t1/2

(517,000 – 642,000 generations; Table 2.13). The estimates for effective population sizes are comparable across P4 protoconid height and height (Table 2.13), which is expected for traits measured from the same evolving population.

The strict stasis model was strongly supported for M1, M2, and M3 lengths and widths (Fig. 2.9; Table 2.14). Visually, M2 length and width sample means for each OSU match the expectation from the stasis model better than M1 and M3 length and width, since some sample means are outside of the 95% probability region for the M1 and M3 teeth. Under the strict stasis model, trait means are constant (. = 0 ln mm2) and at or near the optimum phenotype, -. For M1 length and width, the optimum phenotypes are 0.715 ln mm and 0.426 ln mm, respectively. (Table 2.14). For M2 length and width, the optimum phenotypes are 0.691 ln mm and 0.430 ln mm and for M3 length and width, the optimum phenotype are 0.963 ln mm and 0.411 ln mm, respectively (Table 2.14).

Under the random walk model, ESD depends solely on the magnitude of the step

-9 -9 variance. ESD estimates for P4 length and width are 5.41 x 10 and 4.23 x 10 , respectively, per generation and 5.41 x 10-3 and 4.23 x 10-3, respectively, per one million generations (Table 2.14). Expected squared divergence estimates for P4 protoconid height and height are 2.04 x 10-8 and 1.00 x 10-10, respectively, per generation and 1.02 x 10-2

91 and 5.51 x 10-3, respectively, per one million generations (Table 2.14). ESD estimates calculated for M1, M2, and M3 length and width over one million generations is the same as that calculated for one generation because time is not a factor in estimates of ESD under the models for strict stasis and stasis (Table 2.14). M1 length and width have ESD estimates of 1.45 x 10-3 and 1.67 x 10-3, respectively, per generation and the same estimates per one million generations (Table 2.14). ESD estimates for M2 tooth length and width are 4.79 x 10-3 and 2.05 x 10-3, respectively, per generation and the same estimates per one million generations (Table 2.14). ESD estimates for M3 length and width are 9.24 x 10-4 and 3.22 x 10-3, respectively, per generation and the same estimates per one million generations (Table 2.14).

General overview of results for all lineages

The model of a random walk was the dominant evolutionary model supported by the data. Slightly less than half (47.83%) of all observed tooth metrics evolved under neutral processes. The Orstein-Uhlenbeck model was the best supported model for 23.2% of all observed tooth metrics. The strict stasis model received highest model support

17.39% of the time, followed by the directional (8.69%) and the stasis (2.89%) models.

Considering both strict stasis and stasis, these models received highest support 20.3% of the time. Expected squared divergence ranges from 0 to 2.31 x 10-2 for one generation and 0 to 2.31 x 104 for one million generations.

2.4 Discussion

The lower dental evolution of the paromomyid lineages under study was complex and resulted in either overall size increases or decreases and dietary shifts accompanied

92 these changes for several lineages. The I. frugivorus – I. graybullianus, P. pagei – P. praecox, P. praecox – P. fortior, and P. simonsi – P. willwoodensis lineages appear to have evolved through a process of anagenetic gradual evolution as their known taxonomic ranges in the fossil record do not overlap and in some instances, like the P. praecox – P. fortior lineage, intermediate forms between two taxa are known to have existed (Bown and Rose 1976; Silcox et al. 2008; Secord 2008). The I. fremontensis – I. frugivorus and I. frugivorus – P. pagei lineages appear to have evolved through a process of splitting cladogenesis, as the earlier species have temporal and geographic ranges that overlap with the later occurring species; however, researchers have proposed that intermediate forms between these species exist in the fossil record as well (Bown and

Rose 1976; Secord 2008). Within these overall evolutionary patterns, the analyses uncovered further complexity as discussed in the following sections.

Ignacius fremontensis – Ignacius frugivorus lineage

The dentition of the Ignacius fremontensis – Ignacius frugivorus lineage evolved anagenetically, with changes to its dentition that indicate a shift towards increased size and a more frugivorus diet. Ignacius fremontensis is the oldest known species of the genus and its lower cheek teeth exhibit greater occlusal curvature, with sharper cusps that possess greater shearing potential than later Ignacius species, including Ignacius frugivorus (López-Torres et al. 2018). Ignacius fremontensis P4 size is smaller and the molars are smaller and narrower than I. frugivorus. These observations suggest that I. fremontensis was a generalized omnivore, whereas I. frugivorus is interpreted to have

93 included a larger amount of fruit in their diet but was not completely frugivorous (López-

Torres et al. 2018) as previously hypothesized (Matthew and Granger 1921).

The results from the evolutionary mode analysis are interesting in that I found that the directional selection model gained the highest support for P4 and M1 length and width and the OU model was strongly supported for M2 length and width (Fig. 2.2). Both of these models suggest that there was a strong directional pull towards a new phenotypic optimum. Moreover, the nature of each tooth’s trait trajectory towards the optimal phenotype differs between tooth metrics that are best fit by an OU model and those best fit by the directional model. For example, the P4 length and width tooth metrics that are best fit by a directional model exhibit a sustained gradual increase in size that doesn’t plateau (Fig. 2.2). First molar length trait trajectories are best fit by the directional model; though, there was some support for the OU model for this tooth metric (Akaike weight =

0.255). The trait evolution of M1 length involved an initial steep climb to the optimum phenotype that tapered off by the end of the lineage (Fig. 2.2), which does seem to mirror an OU process. The M2 length and width are best fit by the OU model and exhibit a moderately rapid trait evolution towards the adaptive peak before reaching a plateau. It took between 433,000 and 630,000 generations out of a total of 2.6 million generations for M2 length and width to reach halfway to the optimal phenotype. In other words, between 16% and 24% of the total time had to pass before the lineage climbed halfway to the adaptive peak on the evolutionary landscape.

Estimated squared divergence (ESD) values for the M1 length and M2 length and width are higher than P4 length and width and M1 width. This at first seems

94 counterintuitive, since P4 length and width and M1 width were under directional selection; however, the higher rates for M1 length and M2 length and width are driven by the initial rapid climb to the adaptive optimum before these traits plateaued. Graphically, the trajectory of M2 length and width towards its adaptive peak has a much steeper slope than P4 length and width (Fig. 2.2), therefore it will take more time for P4 length and width to reach the adaptive optimum, thus explaining why ESD values are smaller for teeth that have strong support for directional selection than those that evolved under an

OU process.

Ignacius fremontensis appeared at the beginning of the second Torrejonian (To-2)

NALMA and persisted beyond the Torrejonian – Tiffanian boundary, before going extinct at the end of the first Tiffanian (Ti-1) NALMA. Several other mammals were contemporaneous with and had similar diets to I. fremontensis, including species of

Palaeoryctes, Picrodus, Pronothodectes, Neoplagiaulax, Paromomys, Mimetodon,

Baiotomeus, and Plesiolestes (Lofgren et al. 2004; Behrensmeyer and Turner 2013).

Ignacius frugivorus first appears in the fossil record at the Torrejonian – Tiffanian boundary. Other mammals, including other plesiadapiforms, also appeared at the

Torrejonian – Tiffanian boundary including Carpodaptes, Bisonalveus, Nannodectes,

Navajovius, Plesiadapis, and Limaconyssus (Gunnell 1989; Lofgren et al. 2004). Many of which were omnivorous or insectivorous (Lofgren et al. 2004; Behrensmeyer and Turner

2013) with similar diets to Ignacius fremontensis, which likely resulted in greater competition for food between the newly introduced species and I. fremontensis. The pressure of competing for food, may have driven the shift from the omnivorous diet of I.

95 fremontensis to the more frugivorous diet of I. frugivorus. The selective pressure to adopt a more specialized frugivorous diet may have influenced the rate and mode of evolution in the I. fremontensis – I. frugivorus lineage.

Given the findings, I cannot reject the first hypothesis that directional evolution can explain the phenotypic differences observed in tooth metrics between I. fremontensis and I. frugivorous. Directional evolution was the best fit model for P4 and M1 length and width, which supports my hypothesis. The OU model had the highest support for M2 length and width, and though the OU model has a component of stasis around the optimum, there is a brief but rapid directional trend towards the phenotypic optimum, which supports, at least in part, the first hypothesis. However, caution should be taken when interpreting the results from these model fitting analyses when only a few samples are available. If more samples are collected in the future, it would be worthwhile to run these analyses again to see if the best supported models remain the same for each tooth metric.

Ignacius frugivorus – Ignacius graybullianus lineage

The Ignacius frugivorus – Ignacius graybullianus lineage persists through

Biohorizon A and goes extinct just before Biohorizon B. There was no dietary shift that occurred between these species and I predicted that the transition would be marked by stasis in the tooth metrics that I observed.

The Ignacius frugivorus and Ignacius graybullianus represents two end members of an anagenetically evolving lineage (Bown and Rose 1976; Bloch et al. 2007). Ignacius clarkforkensis represents the middle species connecting these two end members but

96 sample size of I. clarkforkensis was too small to include this species in the analyses.

Molar cusp morphology of I. graybullianus show lower levels of curvature than I. frugivorus. As mentioned above, I. frugivorus has lower levels of curvature than I. fremontensis, which implies that Ignacius species adopted increasing levels of frugivory through time (López-Torres et al. 2018). All tooth metrics, apart from P4 protoconid height, increased in size from I. frugivorus to I. graybullianus. Overall P4 height increased while protoconid height decreased. These observations point to a talonid that became broader-based and taller relative to the height of the protoconid. These changes to the dentition from I. frugivorus to I. graybullianus indicate a shift towards increased size and an even more frugivorus diet.

The results from the evolutionary mode analysis show that the OU model was strongly supported for all tooth metrics (Fig. 2.3; Table 2.6). This model suggests that there was a brief directional pull towards a new phenotypic optimum for all tooth metrics, that once reached was maintained through stabilizing selection. Interestingly, P4 length and protoconid height have .' values that are lower than the pooled phenotypic variance across samples. This means that stabilizing selection around the optimal phenotype was strong. This, coupled with relatively small displacement values for P4 length (+0.561) and protoconid height (-1.16) was why the amount of time to reach halfway to the optimal phenotype was so short (t1/2 range: 0.441 – 1.12 generations; Table 2.5) when compared to all other tooth metrics (Displacement range: +1.14 – +3.08; t1/2 range: 685,000 –

1,370,000; Table 2.5).

97 Estimated squared divergence values for the P4 length and protoconid height are higher than all other tooth metrics (Table 2.6). This is consistent with what I would expect from a phenotype that experienced a strong pull towards the optimum and had smaller displacement values than other tooth metrics.

As discussed in the previous section, Ignacius frugivorus first appears in the fossil record at the Torrejonian – Tiffanian boundary and goes extinct by the end of Ti-5

NALMA. Before I. frugivorus disappears, two Phenacolemur species appear around Ti-4 and Ti-5, Phenacolemur archus an omnivore-insectivore and Phenacolemur pagei an omnivore (Fig. 2.1). Both of these Phenacolemur species would have been in competition for similar food sources with I. frugivorus, who was already likely in competition with several other mammals as discussed in the previous section.

Ignacius graybullianus appears in the fossil record at the beginning of the Eocene

(Wa-0 NALMA) and persists through the first biohorizon event, Biohorizon A, but goes extinct at the start of Biohorizon B (Wa-5 NALMA). Ignacius graybullianus appeared at the same time as Phenacolemur praecox and during its existence several other plesiadapiform omnivores or mixed feeding omnivores appear in the fossil record of the

Bighorn Basin, including species of Arctodontomys, and Phenacolemur (Fig. 2.1;

Gunnell 1985; Silcox et al. 2008; López-Torres et al. 2018). The beginning of the Eocene marks the appearance of omomyid and adapiform euprimates (Lofgren et al. 2004). The adapiform euprimate, Cantius, persists throughout the Wasatchian. The earliest Cantius species (Wa-1 to Wa-3), Cantius ralstoni, Cantius mckennai, Cantius trigonodus were all mixed feeding omnivores that likely incorporated some fruit in their diets (Maas and

98 O’Leary 1996; Glonek 2017) and may have competed for food with I. graybullianus. The omomyid euprimates, Teilhardina and Tetonius would have also been a potential competitor of food for I. graybullianus as both of these omomyid species were mixed feeding omnivores that included fruit and insects in their diets (Strait 2001). Though the transition from I. frugivorus to I. graybullianus didn’t involve a dietary shift, previous researchers have suggested that Ignacius incorporated increasing amounts of fruit into their diet through time (López-Torres et al. 2018). It is possible that with so many generalists around, it may have proven more advantageous for Ignacius to adopt a more specialized fruit centered diet.

My findings do not support the hypothesis that the observed phenotypic differences between I. frugivorus and I. graybullianus is marked by stasis in the tooth metrics that I observed. The OU model does suggest that stabilizing selection played a large role in the evolution of these species, but this model also indicates that a rapid brief directional change occurred in all tooth metrics.

Ignacius frugivorus – Phenacolemur pagei lineage

The transition between Ignacius frugivorus – Phenacolemur pagei occurred during the late Paleocene and included a dietary shift. I predicted that directional evolution occurred in the tooth metrics that I observed.

The Ignacius frugivorus – Phenacolemur pagei represents a genus level budding cladogenesis event (Fig. 2.1). Phenacolemur archus represents an intermediate species connecting I. frugivorus and P. pagei (Secord 2008), but sample size of P. archus was too small to include this species in the analyses. Phenacolemur pagei is larger and more

99 robust than I. frugivorus and all tooth metrics increase in size from I. frugivorus to P. pagei. Phenacolemur pagei exhibits a more bulbous P4 with more exodaenodonty of the posterior root (Secord 2008; Silcox et al. 2008) and the protoconid height of P4 is taller with respect to the talonid. The P4 of Ignacius frugivorus is shorter and narrower, relative to M1, and more squared than that observed in Phenacolemur (Silcox et al. 2008; López-

Torres et al. 2018). The dental evolution from I. frugivorus to P. pagei indicate a shift towards increased size and a dietary shift to a more omnivorous diet with less fruit intake

(Fig. 2.1).

The results from the evolutionary mode analysis show that the OU model was strongly supported for M1 and P4 length and width, and P4 protoconid height and height

(Fig. 2.4; Table 2.8) and the directional model was strongly supported for M2 length and width. The OU model suggests that there was a brief directional pull towards a new phenotypic optimum for the P4 and M1 tooth metrics. Once the phenotypic optimum of these traits was reached, stabilizing selection was the main evolutionary force. The .' values for the P4 and M1 tooth metrics are higher than the pooled phenotypic variance across samples, which suggests stabilizing selection around the optimal phenotype was weak. High displacement values for P4 and M1 (Displacement range: +1.86 - +6.81) and the large amount of time to it took for these traits to reach halfway to the optimal phenotype (t1/2 range: 715,000 – 1,410,000 generations; Table 2.7), supports the observation of a weak pull towards the optimum. It took between 26% and 43% of the total duration of the lineage (3.31 million generations) for these traits to reach midway to the optimum phenotype.

100 Second molar length and width trait trajectories are best fit by the directional model, with almost full model support. However, only the latest occurring P. pagei OSU

(Ppag-2) was included in this analysis because of small sample size for Ppag-1. It is likely that the absence of OSU Ppag-1 skewed model support results towards a best fit of directional selection, so caution should be taken when interpreting these results.

Nevertheless, it appears that some degree of directional selection acted on all tooth metrics for this lineage

Estimated squared divergence (ESD) values for the P4 and M1 tooth metrics are higher than the ESD values for M2 length and width (Table 2.8 and 2.14). As explained above for the Ignacius fremontensis – Ignacius frugivorus lineage, it is possible for ESD values to be smaller for directional evolution because ESD values under the OU model are driven by the initial rapid climb to the adaptive optimum before these traits plateaued around a stable phenotype. Graphically, the trajectory of P4 and M1 tooth metrics exhibit a much steeper slope than M2 tooth metrics (Fig. 2.4), therefore it will take more time for

M2 length and width to reach their adaptive optimums and will have slower rates than that predicted under the OU model.

As discussed in previous sections, Ignacius frugivorus first appears in the fossil record at the Torrejonian – Tiffanian boundary and goes extinct by the end of Ti-5

NALMA. Ignacius frugivorus was likely in competition with several other mammals with similar diets (Fig. 2.1). Phenacolemur pagei appears in the fossil record at the beginning of the fourth Tiffanian (Ti-4) NALMA biozone and persists until the end of the second

Clarkforkian (Cf-2) NALMA biozone. Several omnivorous mammal groups went extinct

101 during the Tiffanian including Anacodon, Baiotomeus, Krauseia, and Mesodma (Lofgren et al. 2004). The disappearance of these animals may have created available niche space for P. pagei to adopt a more omnivorous diet and may have influenced the evolution of I. frugivorus and P. pagei.

The evolution of I. frugivorus to P. pagei involved a dietary shift from an omnivore – frugivore to a stricter omnivorous diet (López-Torres et al. 2018). The third hypothesis that directional evolution can explain the phenotypic differences observed in tooth metrics between I. frugivorus and P. pagei is not supported for the evolution of the

P4 and M1 tooth metrics but is supported for the evolution of M2 length and width. The

OU model does suggest that directional selection occurred briefly in the evolution of the

P4 and M1 tooth metrics, but stasis was the predominant selective pressure acting on these teeth. The evolutionary trajectories of M2 length and width support a directional model of evolution, so I cannot reject this hypothesis for the evolution of this tooth.

Phenacolemur pagei – Phenacolemur praecox lineage

The Phenacolemur pagei – Phenacolemur praecox lineage goes extinct at the beginning of Biohorizon A. No dietary shift occurred between these species and I predicted that the transition between P. pagei and P. praecox is marked by stasis in the tooth metrics I observed.

The dentition of the Phenacolemur pagei – Phenacolemur praecox lineage evolved anagenetically, with changes to its dentition that indicate a shift towards increased size but maintaining an omnivorous diet (Fig. 2.5). Both P. pagei and P. praecox exhibit a more bulbous P4 protoconid with a developed mesiobasal expansion

102 (Silcox et al. 2008). The P4 height and protoconid height increased and there was a pronounced shift in P4 length/width ratios from P. pagei to P. praecox (Secord 2008).

This shift was driven by the decrease in width between P. pagei and P. praecox (Fig.

2.5). All other tooth metrics increased from P. pagei to P. praecox. Phenacolemur pagei and P. praecox both exhibit similar occlusal curvature and shearing potential that are indicative of an omnivorous diet (López-Torres et al. 2018).

The results from the evolutionary mode analysis are interesting in that I found that the strict stasis model gained the highest support for P4 length and height, while the unbiased random walk model was strongly supported for all other tooth metrics (Fig.

2.5). As previously explained, the strict stasis model assumes zero variance around the long-term mean with no real variation in a trait (Hunt 2006; 2008; Hunt et al. 2015), and the unbiased random walk model assumes trait increments are equally likely to be increases or decreases (Fig. 2.5; Hunt 2006; 2008; Hunt et al. 2015). Graphically, the trajectory of P4 protoconid height and width, and M1, M2, and M3 length and width fluctuate around the mean without deviating from the expectation of a random walk (Fig.

2.5). It is important to note that OSU Ppag-1 had too small of a sample for the M2 and M3 teeth to allow for its inclusion into this analysis; however, the random walk model was still strongly supported for these teeth.

As expected, I find that ESD values for P4 length and height over one million generation are generally less than ESD values for all other tooth metrics when also considered over one million generations. ESD values calculated for traits that evolved under stasis or strict stasis do not increase with elapsed time as they do for traits that

103 evolved through a random walk or directional evolution and their values reflect the total amount of divergence that is expected regardless of the amount of elapsed time. As a result, I find it best to compare ESD values over one million generations when stasis or strict stasis is supported for some but not all traits in a lineage, as the case here.

Phenacolemur pagei appears in the fossil record at the beginning of the fourth

Tiffanian (Ti-4) NALMA biozone and persists until the end of the second Clarkforkian

(Cf-2) NALMA biozone. Phenacolemur praecox first appears in the fossil record at the

Paleocene - Eocene boundary and goes extinct by the end of Wa-3 NALMA, before the onset of Biohorizon A. Several mammals were contemporaneous with P. pagei in the

Bighorn Basin including species of Acritoparamys, Apatosciuravus, Arctodontomys,

Chalicomomys, Carpolestes, Paramys, Tinimomys, P. simonsi, and I. clarkforkensis

(Biknevicius 1986; Bloch and Gingerich 1998; López-Torres et al. 2018) and though many may have competed for similar resources, the majority of these species were insectivorous (Biknevicius 1986; Bloch and Gingerich 1998). The large number of specialist insectivores in the area would have allowed the more omnivorous species to diversify and may explain why the P. pagei – P. praecox lineage maintained their omnivorous diet.

For all tooth metrics other than P4 height and length I must reject the fourth hypothesis; however, for P4 height and length I find support for the hypothesis that the observed phenotypic differences in tooth metrics between P. pagei and P. praecox is marked by stasis.

Phenacolemur praecox – Phenacolemur fortior lineage

104 The Phenacolemur praecox – Phenacolemur fortior lineage persists through

Biohorizon A and goes extinct at the beginning of Biohorizon B. Speciation occurs at the beginning of Biohorizon A. There was no dietary shift that occurred between these omnivorous species and I predicted that the transition between these species would be marked by stasis in the tooth metrics that I observed.

The dentition of the Phenacolemur praecox – Phenacolemur fortior lineage evolved anagenetically, with changes to its dentition that indicate a shift towards increased P4 and M3 size but a decrease in P4 protoconid height and height, highlighting movement away from a strictly omnivorous diet to a diet that incorporates a larger amount of fruit (Fig. 2.6). The M1 lengths and widths and M2 lengths changed very little, while M2 widths and M3 lengths and widths increase only slightly from P. praecox to P. fortior. In contrast to P. praecox, the P4 protoconids of P. fortior are short relative to its overall height, which is exaggerated by the high cristid obliqua (Silcox et al. 2008).

Phenacolemur praecox exhibits greater occlusal curvature and shearing potential than P. fortior, which further supports the transition towards a more frugivorous diet in P. fortior

(López-Torres et al. 2018).

The results from the evolutionary mode analysis are interesting, as it indicates that significant changes in the tooth metrics I observed can occur under an evolutionary mode of a random walk and that the P4 tooth metric is very important in terms of diet. I find that for all P4 tooth metrics a model of a random walk has the highest support, while for all molar tooth metrics the models of stasis and strict stasis have the highest support.

105 Similarly, I find that ESD values for all P4 tooth metrics are higher than ESD values for molar tooth metrics, when compared to rates over one million generations.

Phenacolemur praecox first appears in the fossil record at the Paleocene - Eocene boundary and goes extinct by the end of Wa-3 NALMA, before the onset of Biohorizon

A. Phenacolemur praecox is subsequently replaced at the beginning of Biohorizon A by

P. fortior. Phenacolemur fortior, an omnivore-frugivore, went extinct before Biohorizon

B. Phenacolemur simonsi, an omnivore, was contemporaneous with P. praecox and P. fortior and all three of these species likely competed for similar food sources within the

Bighorn Basin. The beginning of the Eocene marks the appearance of other plesiadapiform primates, such as I. graybullianus, as well as several omomyid and adapiform euprimates (Robinson et al. 2004). Since P. praecox was a generalized omnivore, they likely experienced competition from both adapiform and omomyid euprimates, which were mixed feeding omnivores that incorporated varying degrees of fruits and insects in their diets (Behrensmeyer and Turner 2013; Glonek 2017). Before P. praecox went extinct at Biohorizon A, an intermediate form linking P. praecox to P. fortior appeared in the southern Bighorn Basin. These intermediates, referred to as the P. praecox – P. fortior intermediates, were omnivorous but included higher amounts of fruit in their diet than P. praecox did (López-Torres et al. 2018).

It may have been that the shift from an omnivorous diet towards a diet higher in fruit was a response to the ever-increasing competition from many omnivorous mammals that were saturating the landscape at the time. If so, my results indicate that the evolutionary changes that were needed to adopt the more frugivorous diet occurred in the

106 premolar teeth and these important changes could occur under neutral evolution. The molar teeth remained relatively conserved in the P. praecox – P. fortior lineage. For all tooth metrics I must reject the fifth hypothesis that directional evolution can explain the phenotypic differences observed in tooth metrics between P. praecox and P. fortior.

Phenacolemur fortior – Phenacolemur citatus lineage

The Phenacolemur fortior – Phenacolemur citatus lineage begins at Biohorizon A and persists beyond Biohorizon B. Speciation occurred at the beginning of Biohorizon A and the transition involved a dietary shift from an omnivorous diet to an omnivorous- frugivorous diet. I predicted that directional evolution occurred between these species in the tooth metrics I observed.

The dentition of the Phenacolemur fortior – Phenacolemur citatus lineage evolved by budding cladogenesis if, in fact, P. fortior is the most recent ancestor to P. citatus. The transition from P. fortior to P. citatus involved a dietary shift, or more accurately a dietary reversal, from that of an omnivore – frugivore to a generalized omnivore. Dentally, this transition is characterized by decreases in P4, M1, M2, and M3 length and width and an increase in P4 protoconid height and height (Fig. 2.7).

Phenacolemur citatus exhibits greater occlusal curvature and shearing potential than P. fortior, which further supports the transition back towards a more omnivorous diet in P. citatus (López-Torres et al. 2018).

The results from the evolutionary mode analysis are noteworthy because I find that substantial changes in dental morphology that lead to important dietary shifts, such as that observed in the P4, can be explained by changes that fit the expectation of a

107 random walk for most tooth metrics. I find that the evolutionary trajectories of all tooth metrics, except M3 width, are best fit by a model of a random walk. Similarly, I find that

ESD values for all tooth metrics, apart from M3 width, are similar regardless of the magnitude of change that occurred in each tooth metric (Table 2.11).

Phenacolemur fortior and P. citatus both first appears in the fossil record at the

Wa-4 NALMA biozone and the onset of Biohorizon A. Phenacolemur fortior went extinct before Biohorizon B but P. citatus persisted until the end of the Wasatchian (end of Wa-7 NALMA biozone), making P. citatus the only species of Ignacius or

Phenacolemur that survived both biohorizon events. Phenacolemur fortior and early individuals of P. citatus overlapped in range with P. simonsi and I. graybullianus.

Phenacolemur citatus overlapped in range with two additional Phenacolemur species that appeared after Biohorizon B, P. willwoodensis, an insectivore-omnivore, and P. jepseni, an omnivore-insectivore. Phenacolemur fortior was contemporaneous and likely in competition with several mixed diet plesiadapiforms and euprimates including P. simonsi, P. citatus, Microsyops cardiorestes, Microsyops latidens, I. graybullianus, and

Cantius (Behrensmeyer and Turner 2013; Glonek 2017). It is possible that rapid species disappearances at Biohorizon A created available niche space for P. citatus to return to the omnivorous ancestral diet of P. pagei and P. praecox. Similar to the evolutionary transition from P. praecox to P. fortior, the greatest changes occurred in the P4, specifically P4 protoconid height and height, further highlighting their importance with respect to diet. For all tooth metrics, I must reject the sixth hypothesis that directional

108 evolution can explain the phenotypic differences observed in tooth metrics between P. fortior and P. citatus.

Phenacolemur praecox – Phenacolemur citatus lineage

The Phenacolemur praecox – Phenacolemur citatus lineage persists through both

Biohorizon A and Biohorizon B. Speciation occurs at the beginning of Biohorizon A and did not involve a dietary shift from the omnivorous ancestral diet of P. praecox. I predicted that the transition between these species would be marked by stasis in the tooth metrics that I observed.

As an alternative to the hypothesis that P. citatus was a direct descendant of P. fortior, I explore a possible ancestor – descendant relationship between P. praecox and P. citatus. The dentition of the Phenacolemur praecox – Phenacolemur citatus lineage evolved anagenetically, with fewer changes to its dentition than that which is observed between P. fortior and P. citatus. All tooth metrics demonstrate very little net change over the course of the lineage, which is expected from these two species that are not readily distinguishable except for P. praecox specimens being slightly larger, having a wider M1, and slightly taller P4 protoconids on average (Silcox et al. 2008). P. praecox and P. citatus exhibit similar occlusal curvature and shearing potential that is indicative of an omnivorous diet in both species (Fig. 2.8; López-Torres et al. 2018).

The results from the evolutionary mode analysis point towards an evolutionary mode of a random walk for all teeth, except for M2 length which exhibited an evolutionary trajectory that is best supported by a model of stasis. B Expected squared divergence estimates for all P4 tooth metrics are one order of magnitude higher than ESD

109 estimates for molar tooth metrics, indicating that the P4 was less constrained than the molar teeth.

As previously mentioned, P. praecox first appears in the fossil record at the

Paleocene - Eocene boundary and goes extinct by the end of Wa-3 NALMA, before the onset of Biohorizon A. Phenacolemur praecox is subsequently replaced at the beginning of Biohorizon A by P. citatus. Phenacolemur citatus is relatively long lived and persists through both biohorizon events. Phenacolemur simonsi was contemporaneous with P. praecox and P. citatus during at least part of their existence and all three likely competed for the same food sources within the Bighorn Basin. Other plesiadapiform, omomyid, and adapiform primates were contemporaneous with P. praecox, a generalized omnivore

(López-Torres et al. 2018). Some of these contemporaneous species include the omnivore-frugivore species I. graybullianus and the P. praecox – P. fortior intermediates, the omnivorous species P. simonsi and several more insectivorous species of Arctodontomys, Teilhardina and Tetonius. It may be that an omnivorous diet was advantageous in a landscape that comprised of several species with more specialist diets and explain why the transition from P. praecox to P. citatus did not involve a dietary shift.

My results suggest that the P. praecox – P. citatus lineage evolved under neutral or stabilizing (M2 length) processes, suggesting that their generalized omnivorous diet allowed them to compete successfully with several other species in a changing environment for millions of years. For all tooth metrics, except for M2 length, I must

110 reject the seventh hypothesis that the phenotypic differences observed between P. praecox and P. citatus is marked by stasis in the tooth metrics that I observed.

Phenacolemur simonsi – Phenacolemur willwoodensis lineage

The Phenacolemur simonsi – Phenacolemur willwoodensis lineage persists through Biohorizon A and Biohorizon B. Speciation occurs at the beginning of

Biohorizon B and involves a dietary shift from an omnivorous diet to an insectivorous- omnivorous diet. I predicted that directional evolution occurred between P. simonsi and

P. willwoodensis in the tooth metrics that I observed.

The dentition of the Phenacolemur simonsi – Phenacolemur willwoodensis lineage evolved anagenetically. Changes to its dentition indicate a slight but not statistically significant increase in tooth size and a more insectivorous diet (Fig. 2.9). The

P4 talonid of P. willwoodensis is slightly longer than that observed in P. simonsi (Silcox et al. 2008). The molar trigonids of P. willwoodensis are more expansive than that observed in P. simonsi as a result of the rounder and mesially extended paracristids.

Additionally, the molars of P. willwoodensis appear more basally inflated because the talonid cusps are less peripherally placed than in P. simonsi (Silcox et al. 2008). The cusps of P. willwoodensis are taller and sharper with greater shearing potential than P. simonsi, indicating a shift from the omnivorous diet of P. simonsi to the insectivorous – omnivorous diet of P. willwoodensis (López-Torres et al. 2018).

The results from the evolutionary mode analysis are similar to the results for the

P. praecox – P. fortior lineage. I found that neutral evolution can explain the differences observed in P4 length and width and that strict stasis can explain the differences observed

111 in the molar tooth metrics. The ESD estimates for all teeth are similar when compared over one million generations; however, I find the highest ESD estimates for P4 length, width, and M2 length and the lowest ESD estimates for M3 length. These results suggest that, similar to other lineages, the more anterior teeth are less constrained than the more posterior teeth.

Phenacolemur simonsi first appears in the fossil record at the beginning of Cf-2

NALMA and goes extinct at the end of Wa-4 NALMA, just before Biohorizon B (Fig.

2.1). Phenacolemur willwoodensis appears in the Bighorn Basin at the beginning of Wa-6

NALMA after Biohorizon B. There is no record of P. simonsi or P. willwoodensis during the Wa-5 NALMA interval. Throughout P. simonsi’s existence it was contemporaneous with several different potential competitors, including P. pagei, P. praecox, P. fortior, the

P. praecox – P. fortior intermediates, I. graybullianus, and I. clarkforkensis, and Cantius.

It is possible that intense competition between several other omnivorous species and P. simonsi influenced the dental evolution from a strictly omnivorous diet towards a diet that incorporated more insects, as that seen in P. willwoodensis.

Similar to what I have observed in the other lineages, the P4 tooth metrics are less constrained than those of the molars, and their evolution can be explained by neutral processes. The molar teeth remained relatively conserved in the P. simonsi – P. willwoodensis lineage. For all tooth metrics, I must reject the eighth hypothesis that directional evolution can explain the phenotypic differences observed in tooth metrics between P. simonsi and P. willwoodensis.

All lineages

112 The model of a random walk was the dominant evolutionary model supported by my data, followed by the Orstein-Uhlenbeck and strict stasis models. My findings are different to those of Hunt et al. (2015) who found that the majority of traits in fossil lineages fit either a stasis model (38%) or random walk model (28%). However, Hunt et al. (2015) observed several fossil lineages that were not all closely related to each other as the paromomyids under study here are, and the types of traits from each lineage varied.

Therefore, the percentages are not direct comparisons to those of Hunt et al. (2015).

I found that often the same modes of evolution were acting on different tooth metrics within a single lineage. If, for example, a random walk had the highest model support for P4 length, then more often than not, the same model would have the highest support for P4 width. This finding is similar to that observed by Hunt et al. (2015) who also noted that that modes may be shared among a few or the majority of traits within species lineages.

Hunt et al. (2015) suggests that strict stasis is less probable with increasing lineage lengths. Of the three lineages that I found high model support for strict stasis (P. pagei – P. praecox, P. praecox – P. fortior, and P. simonsi – P. willwoodensis), P. praecox – P. fortior was one million years shorter in duration than the other two lineages.

Hunt et al. (2015) also show that directional evolution is more likely in lineages of longer duration, which is supported by my observations in the M2 tooth metrics of the I. frugivorus – P. pagei lineage and if I had omitted the OU model as a candidate model, I likely would have observed this in the I. frugivorus – I. graybullianus lineage as well.

113 I find a wide range of expected squared divergence estimates. For the P4 tooth metrics I tend to see the highest ESD values in the P. pagei – P. praecox and I. frugivorus

– P. pagei, and I. frugivorus – I. graybullianus lineages. For the molar tooth metrics, I found the highest ESD values in the P. simonsi – P. willwoodensis, P. praecox – P. fortior, and P. praecox – P. citatus lineages. It is not unexpected that the highest ESD values are observed in lineages that have trait trajectories that are best fit the expectation of the OU model, as there is a very brief but rapid directional component to an OU process. Interestingly, I do find the highest ESD values among lineages who have trait trajectories that best fit the expectation of the stasis or strict stasis models. Under these circumstances, the ESD value will be the same regardless of the number of generations used to evaluate ESD. This is because time is not a factor when estimating expected squared divergence for the stasis and strict stasis models. This unfortunately results in a limitation when trying to compare ESD as a rate across lineages that have trait trajectories best fit by different evolutionary models. Comparing ESD estimates in these situations is best done with across a wide range of generational time scales.

Overall, I find that the changes in the P4 tooth metrics of the Phenacolemur lineages can be explained by neutral processes. This is interesting because this tooth often exhibits the most drastic changes between species. The changes in the molar tooth metrics of the Phenacolemur lineages can be explained by either stabilizing selection or neutral processes. The differences in tooth metrics for the Ignacius lineages can be explained by directional selection or an OU process.

114 2.5 Conclusion

This study adds to previous work on the evolution of paromomyids by analyzing rates and modes of morphological evolution among tooth metrics of the posterior lower dentition of several paromomyid lineages. The incredible preservation and temporal resolution of this sample allowed us to test several hypotheses of morphological evolution within each paromomyid lineage. The following sections summarize my findings for each lineage.

Ignacius fremontensis – Ignacius frugivorus lineage

1. Increases in all tooth metrics occurred in this lineage. The changes in the P4 and M1

tooth metrics can be explained by directional selection and changes in the M2 tooth

metrics can be explained by an Orstein-Uhlenbeck process.

2. There was a strong directional pull towards a new phenotypic optimum for all tooth

metrics.

3. Estimated squared divergence (ESD) values for the M1 length and M2 length and

width are higher than P4 length and width and M1 width.

4. Since the OU model involves a brief but rapid directional trend towards the

phenotypic optimum, I cannot reject the first hypothesis that directional evolution can

explain the phenotypic differences observed in tooth metrics between I. fremontensis

and I. frugivorous.

5. The pressure of competing for food with several animals that had similar dietary

preferences may have motivated the shift from the omnivorous diet of I. fremontensis

to the more frugivorous diet of I. frugivorus. 115 6. The selective pressure to adopt a more frugivorous diet may have influenced the rate

and mode of evolution in the I. fremontensis – I. frugivorus lineage.

7. Hunt’s (2006, 2008) methods for estimating rate and mode are less reliable when few

samples are available to include in the analysis. Therefore, caution should be taken

when interpreting results for the I. fremontensis – I. frugivorus lineage. If more

samples become available, it would be worthwhile to run these analyses again to see

if the best supported models remain the same for each tooth metric.

Ignacius frugivorus – Ignacius graybullianus lineage

1. Changes to the dentition from I. frugivorus to I. graybullianus indicate a shift towards

increased size and an even more frugivorus diet, which can be explained by an

Ornstein-Uhlenbeck process.

2. Stabilizing selection around the optimal phenotype was stronger for P4 length and

protoconid height than other tooth metrics. P4 length and protoconid height had small

displacement values and the amount of time to reach halfway to the optimal

phenotype was very short when compared to all other tooth metrics.

3. Estimated squared divergence values for the P4 length and protoconid height are

higher than all other tooth metrics, which is consistent with what I would expect from

a phenotype that experienced a strong pull towards the optimum and had smaller

displacement values than other tooth metrics.

4. It may have been more advantageous for Ignacius to adopt a more fruit centered diet

in a landscape that was saturated with generalist omnivores.

116 5. I reject the hypothesis that phenotypic differences between I. frugivorus and I.

graybullianus is marked by stasis in the tooth metrics that I observed.

Ignacius frugivorus – Phenacolemur pagei lineage

1. The dental evolution from I. frugivorus to P. pagei indicate a shift towards increased

size and a dietary shift to a more omnivorous diet with less fruit intake.

2. The OU model was strongly supported for M1 and P4 length and width, and P4

protoconid height and height. The directional model was strongly supported for M2

length and width.

3. For M1 and P4 length and width, and P4 protoconid height and height, stabilizing

selection around the optimal phenotype was weak. High displacement values for P4

and M1 and the large amount of time to it took for these traits to reach halfway to the

optimal phenotype, supports the observation of a weak pull towards the optimum.

4. The absence of OSU Ppag-1 could have skewed model support results towards a best

fit of directional selection, so caution should be taken when interpreting these results.

If sample size increases, reanalysis of this lineage would be warranted.

5. Estimated squared divergence values for the P4 and M1 tooth metrics are higher than

the ESD values for M2 length and width. See text above for how ESD estimates for an

OU model can be greater than those estimated under the directional model.

6. Competition between Ignacius frugivorus and other mammals, coupled with the

disappearance of several omnivorous mammals may have created available niche

117 space for P. pagei to adopt a more omnivorous diet and may have influenced the

evolution of I. frugivorus and P. pagei.

7. The third hypothesis that directional evolution can explain the phenotypic differences

observed in tooth metrics between I. frugivorus and P. pagei is not supported for the

evolution of the P4 and M1 tooth metrics but is supported for the evolution of M2

length and width.

Phenacolemur pagei – Phenacolemur praecox lineage

1. The dentition of the Phenacolemur pagei – Phenacolemur praecox lineage evolved

anagenetically, with changes to its dentition that indicate a shift towards increased

size but maintaining an omnivorous diet.

2. The strict stasis model gained the highest support for P4 length and height, while the

unbiased random walk model was strongly supported for all other tooth metrics. The

sample for OSU Ppag-1 was too small for the M2 and M3 teeth to allow for its

inclusion into the analysis; however, the random walk model was still strongly

supported for these teeth.

3. ESD values calculated for traits that evolved under stasis or strict stasis do not

increase with elapsed time as they do for traits that evolved through a random walk or

directional evolution and their values reflect the total amount of divergence that is

expected regardless of the amount of elapsed time.

4. ESD values for P4 length and height over one million generation are less than ESD

values for all other tooth metrics.

118 5. The large number of specialist insectivores in the area would have allowed the more

omnivorous species to diversify and may explain why the P. pagei – P. praecox

lineage maintained their omnivorous diet.

6. I reject the fourth hypothesis for all tooth metrics other than P4 height and length. For

P4 height and length, I am able to support the hypothesis that phenotypic differences

in tooth metrics between P. pagei and P. praecox is marked by stasis in the tooth

metrics that I observed.

Phenacolemur praecox – Phenacolemur fortior lineage

1. The dentition of the Phenacolemur praecox – Phenacolemur fortior lineage evolved

anagenetically, with changes to its dentition that indicate a shift towards increased P4

and M3 size but a decrease in P4 protoconid height and height, highlighting movement

away from a strictly omnivorous diet to a diet that incorporates a larger amount of

fruit.

2. For all P4 tooth metrics a model of a random walk has the highest support, while all

molar tooth metrics have the highest support for models of stasis and strict stasis.

3. Estimated squared divergence values for all P4 tooth metrics are higher than ESD

values for molar tooth metrics, when compared to rates over one million generations.

4. The evolutionary changes that were needed to adopt the more frugivorous diet

occurred in the premolar teeth and these important changes could occur under neutral

evolution. The molar teeth remained relatively conserved throughout the lineage.

119 5. The shift from an omnivorous diet towards a diet higher in fruit may reflect a

response to the ever-increasing competition from many omnivorous mammals

saturating the landscape.

6. For all tooth metrics I must reject the fifth hypothesis that directional evolution can

explain the phenotypic differences observed in tooth metrics between P. praecox and

P. fortior.

Phenacolemur fortior – Phenacolemur citatus lineage

1. The transition from P. fortior to P. citatus involved a dietary shift from that of an

omnivore-frugivore to a generalized omnivore and was characterized by decreases in

P4, M1, M2, and M3 length and width and an increase in P4 protoconid height and

height.

2. The evolutionary trajectories of all tooth metrics, except M3 width, are best fit by a

model of a random walk.

3. Substantial changes in dental morphology that lead to important dietary shifts, such as

that observed in the P4, can be explained purely by changes that fit the expectation of

a random walk.

4. Expected squared divergence values for all tooth metrics, except M3 width, are

similar regardless of the magnitude of change that occurred in each tooth metric. The

ESD value for M3 width is zero regardless of the amount of time that occurred.

5. Phenacolemur fortior was likely in competition with several mixed diet mammals

and rapid species disappearances at Biohorizon A may have created available niche

120 space for P. citatus to return to the omnivorous ancestral diet of P. pagei and P.

praecox.

6. Similar to the evolutionary transition from P. praecox to P. fortior, the greatest

changes occurred in the P4, specifically P4 protoconid height and height, highlighting

their importance with respect to diet.

7. For all tooth metrics, I must reject the sixth hypothesis that directional evolution can

explain the phenotypic differences observed in tooth metrics between P. fortior and

P. citatus.

Phenacolemur praecox – Phenacolemur citatus lineage

1. The dentition of the Phenacolemur praecox – Phenacolemur citatus lineage evolved

anagenetically with very little net change occurring in the P4, M1, M2, or M3 tooth

metrics over the course of the lineage.

2. The evolutionary trajectories of all tooth metrics, except for M2 length, are best fit by

a model of a random walk. The evolutionary trajectory of M2 length is best supported

by a model of stasis

3. Expected squared divergence estimates for all P4 tooth metrics are one order of

magnitude higher than ESD estimates for molar tooth metrics, indicating that the P4

was less constrained than the molar teeth.

4. An omnivorous diet may have been advantageous in a landscape that comprised of

several species with more specialist diets and explain why the transition from P.

praecox to P. citatus did not involve a dietary shift away from omnivory.

121 5. For P4 height and protoconid height, P4, M1, and M3 length and width, and M2 width,

I must reject the seventh hypothesis that phenotypic differences between P. praecox

and P. citatus is marked by stasis in the tooth metrics that I observed.

6. For M2 length, I am able to support the seventh hypothesis that phenotypic

differences between P. praecox and P. citatus is marked by stasis in the tooth metrics

that I observed.

Phenacolemur simonsi – Phenacolemur willwoodensis lineage

1. The dentition of the Phenacolemur simonsi – Phenacolemur willwoodensis lineage

evolved anagenetically and are characterized by slight but not statistically significant

increases in tooth size and a more insectivorous diet from that of an omnivorous diet

(Fig. 2.9).

2. Neutral evolution can explain the differences observed in P4 length and width and

strict stasis can explain the differences observed in the molar tooth metrics.

3. Expected squared divergence estimates for all teeth are similar when compared over

one million generations; however, I find the highest ESD estimates for P4 length,

width, and M2 length and the lowest ESD estimates for M3 length.

4. Similar to other lineages, the P4 tooth metrics are less constrained than the more

posterior teeth.

5. It is possible that intense competition between several other omnivorous species and

P. simonsi influenced the dental evolution from a strictly omnivorous diet towards a

diet that incorporated more insects, as that seen in P. willwoodensis.

122 6. For all tooth metrics, I must reject the eighth hypothesis that directional evolution can

explain the phenotypic differences observed in tooth metrics between P. simonsi and

P. willwoodensis.

General Conclusions

1. No one mode can characterize the Ignacius and Phenacolemur radiation. However, a

random walk was the dominant evolutionary model supported by the data, followed

by an Ornstein-Uhlenbeck process, and strict stasis.

2. The Phenacolemur evolutionary radiation have P4 tooth metrics trajectories that can

be explained largely by neutral processes.

3. The Ignacius evolutionary radiation have tooth metric trajectories that can be

explained by either an Ornstein-Uhlenbeck process or directional selection.

4. Dietary shifts were sometimes associated with directional change, but this was not

always the case.

5. Lack of a dietary shift was sometimes associated with stasis or a random walk, but

this was not always the case.

6. There was evidence for directional evolution between Ignacius and Phenacolemur.

7. Some Paromomyids had P4 teeth that were less constrained than their molar teeth,

while others show similar levels of constraint between their P4 teeth and their molar

teeth.

8. Significant differences in tooth metrics between species can often be explained by

neutral evolutionary processes.

123 9. Hunt’s (2006, 2008) method for estimating rates is more reliable when there are a

greater number of samples available.

10. Expected squared divergence as a metric for measuring rates of evolution are limited

in their usefulness when ESD values are estimated from different models of best fit.

11. A range of generational time scales should be used when comparing ESD estimates

from different models of best fit.

12. In general, the early primate tooth metrics observed in this study likely experienced

mostly brief periods of directional selection in between longer periods of stabilizing

selection.

2.6 Figures

* * jepseni P. P. P. citatus P. Ln p4 length willwoodensis P. 50.3 intermediates 51.3 Wa 7

52.3 fortior P. -

53.3 Wa 6 *

Wa 5 simsoni P. P. fortior P. 54.3 I. graybullianus Biohorizon B H2 Wa 4 praecox P. ETM2 P. praecox P. Biohorizon A 55.3 Wa 3 Biohorizon B Wa 2 Wa 0-1 * P. pagei P. 56.3 Cf 3 I. clarkforkensis Cf 2 Anagenesis

Ma ? 57.3 Cf 1 Budding cladogenesis P. archus P.

Ti 6 I. frugivorus Dietary shift MAT 58.3 Ti 5 Biohorizon A Phenacolemur Taxa excluded from study due Ti 4 * to insufficient data 59.3 Ti 3

Ti 2 I. fremontensis Omnivore 60.3 Ti 1

61.3 To 3 PETMOmnivore - frugivore

To 2 62.3 Ignacius Omnivore - insectivore 63.3 To 1 Insectivore - omnivore Fig. 2.1 Temporal ranges of North American species of Ignacius and Phenacolemur. Proposed relationships between species of Ignacius and Phenacolemur that were included in this study are indicated by arrows. Patterns indicate dietary niches (López-Torres et al. 2018).

124

2 - 2 - ck Ifrug Ifrug Uhlenbe - 1 1 - - width are plotted plotted are width Ifrug Ifrug Ornstein length and length 1 1 1 and M and - -

4 P Ifrem Ifrem . s u 2 2 - - Ifrug Ifrug Ignacius frugivor Ignacius

to 1 1 - - Ifrug Ifrug and width are plotted with the expectation from the the from are expectation width plotted and with length length

2 Ignacius fremontensis fremontensis Ignacius 1 1 - - Ifrem Ifrem from from

3 ,and M 2 2 2 , M - - 1 Ifrug Ifrug , M 4

cs for cs P for 1 1 - - Ifrug Ifrug Trends in tooth metri tooth in Trends 1 1

- - Ifrem Ifrem Fig. 2.2 Fig. model M and the evolution from with the directional expectation interval). probability (95% model

125 2 - 2 - Ig Ig 1 - Ig 1 - Ig 2 2 and how OSU geologic age age geologic OSU how and - - Ifrug Ifrug 1 - 1 - plotted with plotted the the from with expectation Ifrug Ifrug I. graybullianus I. graybullianus 2 2 - - 2 Ig Ig - Ig 1 - 1 1 - - Ig Ig Ig Ignacius graybullianus graybullianus Ignacius to ll samples for later occurring occurring later for ll samples 2 2 2 - - - Ifrug Ifrug Ifrug Ignacius frugivorus frugivorus Ignacius 1 1 1 - - - Ifrug from from Ifrug Ifrug

3 sma of result a As , , and M

2 2. - 2 , M - 2 1 Ig - 2 Ig - Ig , M 4 1 1 1 - - - Ig Ig Ig or or P f 2 2 2 - - - Ifrug Ifrug Ifrug 1 - Uhlenbeck model (95% probability interval). interval). probability (95% model Uhlenbeck Trends in Trends tooth metrics - 1 - 1

- Ifrug Ifrug Ifrug stein as averaged, Biohorizon A occurs after Ig after A occurs Biohorizon as averaged, Fig. Fig. 2.3 Orn w

126 - 2 2 - - Ifrug Ppag Ppag ength ength and (OSU codes: codes: (OSU 2 - 2 - Ifrug Ifrug 1 1 protoconid protoconid height, height, l length length and width are plotted the with - -

4 2 Ignacius frugivorus frugivorus Ignacius Ifrug Ifrug P are are

). 2 - model model and M 2 2

2 - - - Ppag Ppag Ppag 1 and Ppag and 1 Phenacolemur pagei. Phenacolemur - Uhlenbeck - 1 to to - 1 - 1 - Ppag Ppag Ppag Ppag Ornstein ). The two samples first OSU 2 - 2 2 Ifrug - - us us frugivorus Ifrug Ifrug (OSU codes: codes: (OSU

from from the

Ignaci 1 - 1 1 - - Ifrug Ifrug Ifrug from from

3 , , and M 2 Phenacolemur pagei Phenacolemur 2 2 - - 2 - , M 1 Ppag Ppag Ppag , M 4 olution model (95% probability interval model probability (95% olution samples are are are plotted with the expectation 1 1

- -

1 - U Ppag Ppag Ppag 2 - 2 2 - - Ifrug Ifrug Ifrug length length and width

1 1 1 1 - ) and the last two OS last two the and ) - - Trends Trends in tooth metrics for P 2

- Ifrug Ifrug Ifrug

Fig. 2.4 width, and M ev the directional from expectation 1, Ifrug 127 4 4 - - Ppra Ppra 3 3 - - 2 - Ppra Ppra 2 - Ppra Ppra 1 1 - - Ppra Ppra ) and the last four four the last and ) 2 - 2 2 Ppag - -

id height and length, and and length, and height id Ppag Ppag and 1 - protocon

4 4 4 Ppag - - P . Ppra Ppra 3 3 - - 2 - 2 Ppra - Ppra Ppra Ppra 1 - 1 - (OSU codes: codes: (OSU Ppra Ppra height and length are plotted with the expectation from from expectation the with plotted are length and height

4

ur pagei ur pagei ). 4 - Phenacolemur praecox Phenacolemur 2 2 - - to to Ppag Ppag model. P model.

3, Ppra 3, - Phenacolem 4 4 - - 3 4 - - 3 Ppra Ppra - 2, Ppra 2, 3 - Ppra Ppra 2 2 - - - Ppra 2 - Ppra Ppra Ppra 1 1 - 1 - - Ppra Ppra Ppra Ppra Phenacolemur pagei pagei Phenacolemur 1,Ppra - 2 - 2 2 - - Ppag Ppag Ppag from from Ppra

3 expectation of the random walk random of the expectation

and M and

, 1 - 2 1 1 - - Ppag Ppag Ppag , M (OSU codes: codes: (OSU 1

, M 4 4 4 - - 4 3 - - 3 Ppra 3 Ppra - ity interval). The first two OSU samples are are samples OSU two first The interval). ity - Ppra Ppra 2 2 - - Ppra are plotted with the with are plotted Ppra 2

- 1 Ppra Ppra 1 - 1 - - Ppra Ppra Ppra Ppra 2 2 2 - - - Ppag Ppag Ppag Phenacolemur praecox Phenacolemur

(95% probabil (95% length and width and length

2 Trends in tooth metrics for P for metrics tooth in Trends

1 1 1 - - - Ppag Ppag Ppag and M

1

2.5 Fig. M model the stasis OSU samples are 128 2 - 2 - - Pfor Pfor 1 1 - -

Pfor Pfor

A Bio A Bio Ppra 1, - 4 4 Ppra - - are plotted with with plotted are

Ppra Ppra 3 3 - - Ppra Ppra 2 1 - 2 - - 1 - nd width Ppra Ppra Ppra Ppra (OSU codes: (OSU toconid height, height, length, length, height, height, toconid length a length pro

3 4 P

. ). 2 2 - - 2 - Pfor Pfor 1 1 , and M , and - - 2

Pfor Pfor

A Bio A Bio , M 1 1, Pfor 1, - Phenacolemur praecox praecox Phenacolemur Pfor 4 - 4 - Ppra Ppra 3 3 - - Phenacolemur fortior Phenacolemur Ppra 2 Ppra - 2 to to 1 -

- 1 - Ppra Ppra Ppra Ppra (OSU codes: codes: (OSU

OSU OSU samples are 2 - 2 2 - - Pfor 1 - Pfor Pfor 1 1 - - Pfor Pfor Pfor

model (95% probability interval). M interval). probability (95% model

A Bio A Bio A Bio Phenacolemur praecox Phenacolemur Phenacolemur fortior Phenacolemur 4 - from from

4 - 3 4 Ppra - Ppra Ppra 3 3 3 - - - 2 - Ppra Ppra 2 Ppra 2 - - , and M , and 2 Ppra 1 1 1 - - - Ppra Ppra M of the random walk random the of Ppra Ppra Ppra ,

1 n , M 4 2 2 - - 2 - Pfor Pfor Pfor model (95% probability interval). The first four The four first interval). (95% model probability 1 1 1

- - -

Pfor Pfor Pfor

A Bio A Bio A Bio ) and the last two OSU samples are are samples OSU two last the and ) 4 - 4 - 4 4 - Ppra -

Ppra Ppra Ppra nd 3 3 - tion of the the stasis tion of - a 3 - 2 Ppra - Ppra Trends in tooth metrics for P for metrics tooth in Trends 3, 2 - Ppra

- 2 1 - 1 1 - Ppra - - Ppra Ppra Ppra Ppra Ppra

2.6Fig. expectatio the with are plotted and width the expecta 2,Ppra 129

5 5 - - Pcit Pcit 4 4 - - Pcit Pcit width, 3

3 - - 3 Pcit Pcit 2 - 2 - 1 - Pcit Pcit Pcit

Phenacolemur Phenacolemur 1

-

Bio B Bio Bio B Bio Pcit he expectation of expectation he , except M e are are e l 2 2 - - Pfor Pfor 1 - 1 - P. citatus Pfor Pfor – All metrics All tooth t five OSU samp OSU five t . 5 5 - - P. fortior fortior P. Pcit Pcit 4 4 - - Pcit Pcit 3 3 - - Pcit Pcit 2 ) and the las the and ) 2 - - 2 Pcit - Pcit 1 width tooth metric is plotted with t with plotted is metric tooth width 1 - -

3 Bio B Bio Pcit B Bio Bio B and is bounded by dotted lines. dotted by bounded is and B Bio Pcit 1, Pfor 1, - Phenacolemur citatus Phenacolemur

The The M 2 - to 2

- Pfor Pfor Pfor 1 1 - - Pfor Pfor (OSU codes: codes: (OSU 5 5 5 - - - Pcit Pcit Pcit 4 4 - - 4 - Pcit Pcit 3 Pcit 3 - - 3 - Phenacolemur fortior Phenacolemur Pcit Pcit Pcit 2 2 - - 2 - Pcit Pcit Biohorizon B event is indicated as indicated is event B Biohorizon 1 1 Pcit - 1

from from - -

).

Pcit 3 Pcit Bio B Bio Bio B Bio Pcit B Bio 5 - model (95% probability interval). interval). probability (95% model

enacolemur fortior enacolemur 2 - Ph 2 , , and M - 4, 4, Pcit 2 2 Pfor - - Pfor Pfor 1 1 1 - - - , M 1 Pfor Pfor Pfor 3, Pcit , M - 4 5 5 2, Pcit 2, - 5 - - - Pcit Pcit Pcit 4 - 4 - 4 Pcit - Pcit 3 Pcit 3 3 - - - 1, Pcit - Pcit Pcit Pcit 2 2 - - 2 - Pcit Pcit Pcit Pcit 1

1 - 1

-

-

Bio B Bio B Bio Bio B Bio are samples OSU two first The Pcit in in tooth metrics for P Pcit Pcit h the expectation of the random walk random the of expectation the h t 2 - Trends Trends 2 2 - -

Pfor (OSU code: code: (OSU

Pfor Pfor 1 1 1 - - - Pfor Pfor Pfor Fig. Fig. 2.7 wi are plotted model. stasis the citatus

130 length are length

2 model (95% model

) and the last five OSU OSU five last the and ) 4 - Ppra

and 3, 3, - All teeth metrics except M except metrics teeth All . atus t 2, Ppra 2, - ents ents are indicated as Bio A and Bio B and are 1, Ppra 1, - Ppra Phenacolemur ci Phenacolemur Biohorizon ev Biohorizon

length is plotted with the expectation of the the stasis of expectation the with plotted is length

). to to 2

5 - (OSU codes: codes: (OSU 4, 4, Pcit - y interval). M interval). y 3, Pcit - emur praecox praecox emur l 2, Pcit Phenacolemur praecox Phenacolemur - from from

3 1, Pcit - Phenaco cit P model (95% probabilit (95% model

, and M and , 2 , M 1 , M 4 (OSU (OSU codes:

s trics for P for trics

Phenacolemur citatu Phenacolemur Trends in tooth me tooth in Trends

2.8 Fig. walk random the of expectation the with plotted are samples OSU four first The interval). probability samples are lines. dotted by bounded 131 1 1 - -

Pwil Pwil

B Bio B Bio model. model.

4 4 - -

Psim Psim

A Bio A Bio y dotted lines. dotted y 3 - 3 2 - - ) and the last OSU OSU the last ) and 1 - Psim 1 4 2 - - Psim Psim - Psim protoconid height and height height and height protoconid Psim Psim

4 P Psim . and ctation of the random walk the random of ctation 3, e - 1 1 - -

Pwil Pwil

B Bio B Bio 2, Psim 2, - 4 4 - -

Psim Psim

A Bio A Bio 1, 1, Psim - Psim 3 3 - - Phenacolemur willwoodensis Phenacolemur Psim Psim 2 2 - to to es: es: - 1

1 - - d Psim Psim del. All plots include the 95% probability interval for their their for interval probability the 95% include plots All del. Psim Psim o m

(OSU co (OSU 1 1 - - length and width are plotted with the exp the with are plotted width and length

Pwil

Pwil 4

B Bio P B Bio

iohorizon events are indicated as Bio A and Bio B and are bounded b bounded are and B Bio and A Bio as are indicated events iohorizon Phenacolemur simonsi Phenacolemur B

4 - 4 ). - 1 Psim

-

Psim

A Bio A Bio from

3 Pwil Phenacolemur simonsi simonsi Phenacolemur 3 - 3 - Uhlenbeck model. Uhlenbeck - Psim 2 , and M ,and 2 - Psim - 2 1 1 - - Psim Psim Psim , M Psim 1 (OSU code: code: (OSU

, M 4 he Ornstein he 1 - 1 -

Pwil

Pwil

B Bio B Bio 4 4 - -

Psim Psim

A Bio A Bio length and width are plotted with the expectation of the the stasis of expectation the with are plotted width and length

3 3 - Phenacolemur willwoodensis Phenacolemur 3 2 - - Trends in tooth metrics for P for metrics tooth in Trends 2 Psim -

1 1 , and M ,and - - Psim 2 Psim Psim ctive models. The first four OSU samples are samples OSU four The first models. ctive Psim Psim , M 1

2.9 Fig. t of the expectation with are plotted M respe is sample 132 2.7 Tables

Table 2.1

Number of Individual Species OSU code Mean age (Ma) specimens (n)

P. willwoodensis Pwil-1 8 53.69

P. simonsi Psim-4 13 54.73

P. simonsi Psim-3 24 55.75

P. simonsi Psim-2 22 55.83

P. simonsi Psim-1 23 55.92

P. citatus Pcit-5 32 53.41

P. citatus Pcit-4 40 53.59

P. citatus Pcit-3 25 53.72

P. citatus Pcit-2 23 53.89

P. citatus Pcit-1 42 54.06

P. fortior Pfor-2 16 54.54

P. fortior Pfor-1 32 54.94

P. praecox Ppra-4 48 55.42

P. praecox Ppra-3 32 55.69

P. praecox Ppra-2 61 55.74

P. praecox Ppra-1 49 55.86

P. pagei Ppag-2 13 56.47

P. pagei Ppag-1 15 57.64

I. graybullianus Ig-2 32 55.56

I. graybullianus Ig-1 18 56.11

I. frugivorus Ifrug-2 9 58.70

133 Table 2.1 Continued

I. frugivorus Ifrug-1 59 59.78

I. fremontensis Ifrem-1 8 61.3

Table 2.1 List of Operational Stratigraphic Units (OSUs) and their sample sizes and mean estimated age for each species of Ignacius and Phenacolemur included in the study.

Table 2.2

Evolutionary Expected squared Mean ∆= Variance ∆= model divergence, ESD

Stasis/Strict stasis > − =8 ? 2?

: : Random walk 0 A2#"9/ A2#"9t

: : : Directional B2#"9t A2#"9/ B2#"9/ + A2#"9/

Ornstein- : A2#"9 2 [1 − #F"(−G/)](> − =() (1 − #F"[−2G/]) (Mean ∆=) + Variance ∆= Uhlenbeck 2G

Table 2.2 Evolutionary divergence for three models of evolution. For each evolutionary model, changes from ancestor to descendant (∆B) over t generations will be normally distributed with means and variance provided in the second and third columns. Column four provides the expression for expected squared divergence (ESD), a measure of expected evolutionary change. For the stasis model, the ESD integrates over the distribution of ancestral states (B ). Table modified from Hunt (2012). &

134

Table 2.3

: : Trait Displacement A 9 Ne ? t1/2

M2 length +4.75 0.00489 4,890,000 – 34,200,000 445 – 3110 630,000

M2 width +4.45 0.00563 5,630,000 – 39,400,000 352 – 2460 433,000

Table 2.3 Estimates and ranges for population genetic parameters computed from the maximum-likelihood parameter estimates of the Ornstein-Uhlenbeck model for M2 length and width in the Ignacius fremontensis – Ignacius frugivorus lineage. Displacement is the difference between the initial trait value and the optimal trait value of the lineage in standard deviation units (calculated from the pooled phenotypic ' variance across samples, C (). Effective population size ranges were calculated with an assumed trait heritability range between 0.1 and 0.7 and reported ranges reflect calculations using these two end-member heritability values. The last column, t1/2, is the time in generations for the population to reach the halfway point to the phenotypic optimum.

Table 2.4 ESD Akaike ESD Trait Model LogL AIC Parameter estimates (1 x 106 C weight (1 gen.) gens.)

P4 length Strict Stasis -1.55 9.09 0.000 >=0.501

> = 0.474 Stasis 1.46 Inf 0.000 ? = 0.0172

: -8 Random Walk 2.17 Inf 0.000 A2#"9 = 2.83x10

-7 I;<=> = 1.60 x 10 -14 -8 Directional 5.55 -29.10 0.937 ? 5.13 x 10 5.13 x 10 J;<=> = 0.000 : -10 Ornstein- A2#"9 = 1x 10 Uhlenbeck 5.85 -23.70 0.063 > = 6.42x10-1 G = 7.82 x 10-7

P4 width Strict Stasis -3.76 13.52 0.000 >=0.0892

> = 0.0683 Stasis 1.98 Inf 0.000 ? = 0.0133

: -8 Random Walk 2.94 Inf 0.000 A2#"9 = 1.91 x 10

135 Table 2.4 Continued -7 I;<=> = 1.31 x 10 -14 -8 Directional 6.66 -31.33 0.948 ? 3.44 x 10 3.44 x 10 J;<=> = 0.000

A: = 1x 10-10 Ornstein- 2#"9 6.76 -25.52 0.052 > = 1.99 x 10-1 Uhlenbeck -7 G = 8.23 x 10

M1 length Strict Stasis -15.97 37.95 0.000 > = 0.709

> = 0.640 Stasis 2.43 Inf 0.000 ? = 0.0107

: -8 Random Walk 3.08 Inf 0.000 A2#"9 = 2.29 x 10

-8 I;<=> = 7.31 x 10 -8 -2 Directional 3.38 -24.76 0.745 ? -8 1.68 x 10 1.68 x 10 J;<=> = 1.68 x 10 : -8 Ornstein- A2#"9 = 5.59 x 10 Uhlenbeck 5.31 -22.62 0.255 > = 0.671 G = 9.10 x 10-6

M1 width Strict Stasis -5.53 17.06 0.000 > = 0.436

> = 0.414 Stasis 2.39 Inf 0.000 ? = 0.0105

: -8 Random Walk 3.48 Inf 0.000 A2#"9 = 1.45 x 10

-7 I;<=> = 1.16 x 10 -14 -8 Directional 7.30 -32.60 0.942 ? 2.69 x 10 2.69 x 10 J;<=> = 0.000

A: = 1x10-10 Ornstein- 2#"9 7.52 -27.04 0.058 > = 0.527 Uhlenbeck -7 G = 8.29 x 10

M2 length Strict Stasis -16.17 38.34 0.000 > = 0.682

> = 0.630 Stasis 1.60 Inf 0.000 ? = 0.0189

: -8 Random Walk 2.90 Inf 0.000 A2#"9 = 2.36 x 10

-7 B2#"9 = 1.32 x 10 Directional 4.76 -27.52 0.478 : -9 A2#"9 = 3.06 x 10 J? = 1x10-10 Ornstein- ;<=> 7.86 -27.72 0.526 1.00 x 10-10 4.91 x 10-2 Uhlenbeck K = 0.759 L = 1.10 x 10-6

M2 width Strict Stasis -15.61 37.21 0.000 > = 0.516

> = 0.453 Stasis 1.45 Inf 0.000 ? = 0.0208

: -8 Random Walk 2.64 Inf 0.000 A2#"9= 2.86 x 10

136 Table 2.4 Continued

-7 B2#"9 = 1.32 x 10 Directional 3.83 -25.68 0.249 : -9 A2#"9 = 8.15 x 10

J? = 1x10-10 Ornstein- ;<=> 7.94 -27.89 0.751 K = 0.570 1.00 x 10-10 7.11 x 10-2 Uhlenbeck -6 L = 1.60 x 10

Table 2.4 Evolutionary model-fitting results for the Ignacius fremontensis – Ignacius frugivorus lineage using Hunt’s (2008) joint parameterization method. For each trait, the best-supported model is in bold. Expected squared divergence (ESD) is reported for one generation and one million generations. AICC, Akaike information criterion; LogL, Log-likelihood. There was no data on P4 tooth height or protoconid height, so these tooth metrics were excluded from the analysis. The M3 tooth had insufficient data to include in the analysis.

Table 2.5

: : Trait Displacement A 9 Ne ? t1/2

P4 length +0.561 0.0139 13,940,000 – 97,100,000 -0.0130 – -0.00768 0.441

P4 width +1.14 0.126 126,000,000 – 879,000,000 1560 –10900 1,220,000 P protoconid 4 -1.16 0.0294 29,400,000 – 206,000,000 -0.0246 – 0.00395 1.12 height

P4 height +1.14 0.0158 15,860,000 – 110,000,000 1560 – 10900 685,000

M1 length +1.68 0.00423 50,800 – 356,000 834 – 5840 1,370,000

M1 width +3.08 0.00540 68,400 – 479,000 655 – 4580 840,000

M2 length +2.79 0.00380 1,320,000 – 9,270,000 565 – 3960 1,030,000

M2 width +2.15 0.00518 885,000 – 6,200,000 983 – 6880 1,320,000

Table 2.5 Estimates and ranges for population genetic parameters computed from the maximum-likelihood parameter estimates of the Ornstein-Uhlenbeck model for P4, M1, and M2 tooth metrics in the Ignacius frugivorus – Ignacius graybullianus lineage. Displacement is the difference between the initial trait value and the optimal trait value of the lineage in standard deviation units (calculated from the pooled phenotypic variance across ' samples, C (). Effective population size ranges were calculated with an assumed trait heritability range between 0.1 and 0.7 and reported ranges reflect calculations using these two end-member heritability values. The last column, t1/2, is the time in generations for the population to reach the halfway point to the phenotypic optimum.

137 Table 2.6 ESD Akaike ESD 6 Model LogL AICC Parameter estimates (1 x 10 Trait weight (1 gen.) gens.)

P4 length Strict Stasis 6.67 -9.33 0.000 D=0.557

D = 0.557 Stasis 6.67 2.67 0.000 E = 0.000

' -10 Random Walk 6.11 3.79 0.000 C)*+( = 5.55x10

-8 F)*+( = 1.57 x 10 Directional 6.98 Inf 0.000 ' C)*+( = 0.000

G0 = 1x 10-10 Ornstein- ,-./ 7.45 -46.91 1.000 2.77 x 10-3 4.42 x 10-3 Uhlenbeck H = 0.590 I = 1.57

P4 width Strict Stasis -8.54 21.08 0.000 D=0.237

D = 0.280 Stasis 2.26 11.48 0.000 E = 0.0162

' -8 Random Walk 4.45 7.10 0.000 C)*+( = 1.13 x 10

-8 F)*+( = 7.79 x 10 Directional 7.91 Inf 0.000 ' C)*+( = 0.000

G0 = 1x 10-10 Ornstein- ,-./ 7.54 -47.08 1.000 H = 0.427 1.00 x 10-10 1.93 x 10-2 Uhlenbeck -7 I = 5.66 x 10 P4 protoconid Strict Stasis 2.71 -1.41 0.000 D= -0.138 height D = -0.169 Stasis 3.19 9.63 0.000 E = 0.00531

-9 Random Walk 3.55 8.89 0.000 C)*+( = 8.66 x 10

F = -5.79 x 10-8 Directional 5.23 Inf 0.000 )*+( C)*+( = 0.000 G = 1 x 10-10 Ornstein- ,-./ 5.49 -42.99 1.000 8.44 x 10-3 3.98 x 10-2 Uhlenbeck H = -0.255 I = 0.617

P4 height Strict Stasis 4.44 -4.87 0.000 D = 0.510

D = 0.526 Stasis 4.58 6.84 0.000 E = 0.00165

-9 Random Walk 4.68 6.64 0.000 C)*+( = 3.59 x 10

138 Table 2.6 Continued F = 3.61 x 10-8 Directional 6.22 Inf 0.000 )*+( C)*+( = 0.000 G = 1 x 10-10 Ornstein- ,-./ 6.46 -44.91 1.000 H = 0.601 1.00 x 10-10 8.30 x 10-3 Uhlenbeck -6 I = 1.01 x 10

M1 length Strict Stasis -11.62 27.24 0.000 D = 0.790

D = 0.796 Stasis 4.03 7.94 0.000 E = 0.00688

-9 Random Walk 5.90 4.20 0.000 C)*+( = 7.18 x 10

-8 F)*+( = 2.78 x 10 Directional 6.15 Inf 0.000 -9 C)*+( = 5.26 x 10 G = 8.32 x 10-9 Ornstein- ,-./ 6.54 -45.08 1.000 H = 0.856 8.32 x 10-9 7.11 x 10-3 Uhlenbeck -7 I = 5.06 x 10

M1 width Strict Stasis -51.60 107.20 0.000 D = 0.562

D = 0.603 Stasis 2.68 10.65 0.000 E = 0.0147

-8 Random Walk 5.11 5.77 0.000 C)*+( = 1.27 x 10

-8 F)*+( = 5.84 x 10 Directional 5.85 Inf 0.000 -9 C)*+( = 5.73 x 10 G = 7.90 x 10-9 Ornstein- ,-./ 6.85 -45.69 1.000 H = 0.674 7.90 x 10-9 2.00 x 10-2 Uhlenbeck -7 I = 8.25 x 10

M2 length Strict Stasis -28.39 60.79 0.000 D = 0.772

D = 0.805 Stasis 4.15 7.70 0.000 E = 0.00685

-9 Random Walk 6.68 2.64 0.000 C)*+( = 4.62 x 10

F = 4.45 x 10-8 Directional 9.63 Inf 0.000 )*+( C)*+( = 0.000 G = 2.87 x 10-10 Ornstein- ,-./ 9.39 -50.78 1.000 H = 0.865 2.87 x 10-10 7.21 x 10-3 Uhlenbeck -7 I = 6.72 x 10

M2 width Strict Stasis -13.85 31.71 0.000 D = 0.606

139 Table 2.6 Continued D = 0.632 Stasis 4.33 7.34 0.000 E = 0.00601

-9 Random Walk 6.76 2.49 0.000 C)*+( = 3.65 x 10

F = 3.98 x 10-8 Directional 10.00 Inf 0.000 )*+( C)*+( = 0.000 G = 5.85 x 10-10 Ornstein- ,-./ 8.68 -49.36 1.000 H = 0.695 5.85 x 10-10 4.41 x 10-3 Uhlenbeck -7 I = 5.27 x 10 Table 2.6 Evolutionary model-fitting results for the Ignacius frugivorus – Ignacius graybullianus lineage using Hunt’s (2008) joint parameterization method. For each trait, the best-supported model is in bold. Expected squared divergence (ESD) is reported for one generation and one million generations. AICC, Akaike information criterion; LogL, Log- likelihood. The M3 tooth had insufficient data to include in the analysis.

Table 2.7

' ' Trait Displacement C ( Ne . t1/2

P4 length +5.02 0.0118 23,400 – 165,000 1470 – 10300 863,000

P4 width +6.81 0.00693 5,970 – 41,800 715 – 5010 715,000

P4 protoconid height +3.10 0.0198 28,600 – 200,000 3490 – 24500 1,220,000

P4 height +4.83 0.0182 29,300 – 205,000 2340 – 16400 892,000

M1 length +1.86 0.00382 54,800 – 384,000 775 – 5420 1,410,000

M1 width +3.89 0.00393 257,000 – 1,800,000 491 – 3430 865,000

Table 2.7 Estimates and ranges for population genetic parameters computed from the maximum-likelihood parameter estimates of the Ornstein-Uhlenbeck model for P4 and M1 tooth metrics in the Ignacius frugivorus – Phenacolemur pagei lineage. Displacement is the difference between the initial trait value and the optimal trait value of the lineage in standard deviation units (calculated from the pooled phenotypic variance across ' samples, C (). Effective population size ranges were calculated with an assumed trait heritability range between 0.1 and 0.7 and reported ranges reflect calculations using these two end-member heritability values. The last column, t1/2, is the time in generations for the population to reach the halfway point to the phenotypic optimum.

140 Table 2.8 ESD Akaike ESD Trait Model LogL AIC Parameter estimates (1 x 106 C weight (1 gen.) gens.)

P4 length Strict Stasis -92.73 189.45 0.000 >=0.895

> = 0.839 Stasis -0.364 16.73 0.000 ? = 0.0684 Random 1.79 12.42 0.000 A: = 7.85 x 10-8 Walk 2#"9

-7 B2#"9 = 1.66 x 10 Directional 2.55 Inf 0.000 : -8 A2#"9 = 4.27 x 10 Ornstein- J? = 5.06 x 10-8 ;<=> 5.06 x 1.16 x 10- Uhlenbeck 3.33 -38.67 1.000 K = 1.07 10-8 1 L = 8.03 x 10-7 - P4 width Strict Stasis 428.00 0.000 >=0.518 212.00

> = 0.449 Stasis -0.869 17.74 0.000 ? = 0.0893 Random 1.43 13.14 0.000 A: = 1.23 x 10-7 Walk 2#"9

-7 B2#"9 = 1.72 x 10 Directional 1.90 Inf 0.000 : -8 A2#"9 = 8.76 x 10 Ornstein- J? = 1.16 x 10-7 ;<=> 1.16 x 1.75 x 10- Uhlenbeck 2.78 -37.55 1.000 K = 0.674 10-7 1 L = 9.69 x 10-7 P protoconid 4 Strict Stasis -28.30 60.60 0.000 >= 0.183 height

- > = 0.122 Stasis 16.17 0.000 0.0826 ? = 0.0559 Random 1.39 13.22 0.000 A: = 7.57 x 10-8 Walk 2#"9

-7 B2#"9 = 1.33 x 10 Directional 1.87 Inf 0.000 : -8 A2#"9 = 4.35 x 10 Ornstein- J? = 6.96 x 10-8 ;<=> 1.16 x 1.05 x 10- Uhlenbeck 2.20 -36.40 1.000 K = 0.381 10-7 1 L = 5.69 x 10-7

P4 height Strict Stasis -77.89 159.79 0.000 > = 0.872

> = 0.832 Stasis -1.04 18.07 0.000 ? = 0.0952 Random 1.10 13.79 0.000 A: = 1.06 x 10-7 Walk 2#"9

-7 B2#"9 = 1.99 x 10 Directional 1.94 Inf 0.000 : -8 A2#"9 = 5.28 x 10

141 Table 2.8 Continued Ornstein- J? = 6.22 x 10-8 ;<=> 6.22 x 1.56 x 10- Uhlenbeck 2.69 -37.38 1.000 K = 1.11 10-8 1 L = 7.77 x 10-7

M1 length Strict Stasis -4.04 12.07 0.000 > = 0.776

> = 0.780 Stasis 4.79 6.42 0.000 ? = 0.00443 Random 6.02 3.96 0.000 A: = 6.68 x 10-9 Walk 2#"9

-8 B2#"9 = 3.47 x 10 Directional 6.38 Inf 0.000 : -9 A2#"9 = 3.95 x 10 Ornstein- J? =6.97 x 10-9 ;<=> 6.97 x 6.44 x 10- Uhlenbeck 6.62 -45.25 1.000 K = 0.862 10-9 3 L = 4.93 x 10-7

M1 width Strict Stasis -47.29 98.58 0.000 > = 0.539

> = 0.591 Stasis 3.20 9.61 0.000 ? = 0.0113 Random 5.60 4.80 0.000 A: = 1.10 x 10-8 Walk 2#"9

-8 B2#"9 = 7.74 x 10 Directional 7.10 Inf 0.000 : -9 A2#"9 = 2.14 x 10 Ornstein- J? = 1.53 x 10-9 ;<=> 1.53 x 1.89 x 10- Uhlenbeck 8.05 -48.10 1.000 K = 0.692 10-9 2 L = 8.01 x 10-7

M2 length Strict Stasis 1.44 3.11 0.000 > = 0.723

> = 0.753 Stasis 4.36 Inf 0.000 ? = 0.00234 Random 5.59 Inf 0.000 A: = 3.29 x 10-9 Walk 2#"9

-8 - I;<=> = 4.48 x 10 4.01 x 4.01 x 10 Directional 8.11 -34.21 0.950 ? -15 9 J;<=>= 0.000 10 : -10 Ornstein- A2#"9 = 1 x 10 Uhlenbeck 8.17 -28.33 0.050 > = 0.839 G = 6.21 x 10-7

M2 width Strict Stasis 3.84 -1.67 0.000 > = 0.560

> = 0.581 Stasis 4.53 Inf 0.000 ? = 0.00151 Random 5.71 Inf 0.000 A: = 2.21 x 10-9 Walk 2#"9

-8 - I;<=> = 3.78 x 10 2.85 x 2.85 x 10 Directional 7.95 -33.90 0.970 ? -15 9 J;<=>= 0.000 10

142 Table 2.8 Continued

: -10 Ornstein- A2#"9 = 1x10 Uhlenbeck 7.49 -26.97 0.030 > = 0.673 G = 4.18 x 10-7 Table 2.8 Evolutionary model-fitting results for the Ignacius frugivorus – Phenacolemur pagei lineage using Hunt’s (2008) joint parameterization method. For each trait, the best-supported model is in bold. Expected squared divergence (ESD) is reported for one generation and one million generations. AICC, Akaike information criterion; LogL, Log-likelihood. The M3 tooth had insufficient data to include in the analysis.

Table 2.9 ESD Akaike ESD Trait Model LogL AIC Parameter estimates (1 x 106 C weight (1 gen.) gens.)

Strict -3 -3 P4 length 10.87 -18.74 0.747 K=1.14 1.12 x 10 1.12 x 10 Stasis

> = 1.14 Stasis 11.63 -15.26 0.131 ? = 5.62 x 10-4 Random 11.54 -15.08 0.120 A: = 1.96 x 10-9 Walk 2#"9

-8 B2#"9 = 1.30 x 10 Directional 12.04 -6.08 0.001 : A2#"9 = 0.000

A: = 2.34 x 10-9 Ornstein- 2#"9 11.94 24.12 0.000 > = 1.17 Uhlenbeck -7 G = 6.46 x 10

P4 width Strict Stasis 7.32 -11.65 0.160 >= 0.751

> = 0.750 Stasis 10.55 -13.10 0.331 ? = 0.00120 Random 10.98 -13.95 0.506 J? = 5.20 x 10-9 5.20 x 10-9 5.20 x 10-3 Walk ;<=>

-8 B2#"9 = -1.95 x 10 Directional 10.98 -3.94 0.003 : -9 A2#"9 = 5.39 x 10

A: = 7.83 x 10-9 Ornstein- 2#"9 11.69 24.63 0.000 > = 0.772 Uhlenbeck -6 G = 1.66 x 10 P4 protoconid Strict Stasis 1.45 0.0907 0.012 >= 0.439 height > = 0.449 Stasis 6.74 -5.48 0.201 ? = 0.00466 Random 8.09 -8.18 0.779 J? = 1.29 x 10-8 1.29 x 10-8 1.29 x 10-2 Walk ;<=>

143 Table 2.9 Continued -8 B2#"9 = 5.52 x 10 Directional 8.37 1.25 0.007 : -9 A2#"9 = 8.62 x 10

A: = 2.28 x 10-8 Ornstein- 2#"9 9.41 29.18 0.000 > = 0.425 Uhlenbeck -6 G = 3.23 x 10

Strict -3 -3 P4 height 7.41 -11.81 0.545 K = 1.19 3.32 x 10 3.32 x 10 Stasis

> = 1.19 Stasis 8.91 -9.81 0.200 ? = 0.00166 Random 9.14 -10.28 0.253 A: = 5.87 x 10-9 Walk 2#"9

-8 B2#"9 = 2.34 x 10 Directional 9.24 -0.494 0.002 : -9 A2#"9 = 4.74 x 10

A: = 1.87 x 10-8 Ornstein- 2#"9 10.05 27.91 0.000 > = 1.20 Uhlenbeck -6 G = 4.28 x 10

M1 length Strict Stasis -30.94 64.89 0.000 > = 0.977

> = 0.962 Stasis 6.52 -5.03 0.019 ? = 0.00622 Random 10.44 -12.89 0.958 J? = 8.94 x 10-9 8.94 x 10-9 8.94 x 10-3 Walk ;<=>

-8 B2#"9 = 8.59 x 10 Directional 11.71 -5.42 0.023 : -9 A2#"9 = 4.04 x 10

A: = 6.73 x 10-9 Ornstein- 2#"9 11.59 24.83 0.000 > = 1.02 Uhlenbeck -7 G = 6.94 x 10

M1 width Strict Stasis -2.72 8.44 0.000 > = 0.785

> = 0.774 Stasis 8.89 -9.79 0.117 ? = 0.00254 Random 10.90 -13.79 0.869 J? = 5.11 x 10-9 5.11 x 10-9 5.11 x 10-3 Walk ;<=>

-8 B2#"9 = 5.41 x 10 Directional 11.77 -5.53 0.014 : -9 A2#"9 = 2.27 x 10

A: = 4.10 x 10-9 Ornstein- 2#"9 11.73 24.54 0.000 > = 0.819 Uhlenbeck -7 G = 6.44 x 10

M2 length Strict Stasis -2.59 8.51 0.003 > = 1.00

> = 0.971 Stasis 5.93 -1.86 0.491 ? = 0.00455

144 Table 2.9 Continued Random 5.96 -1.92 0.506 J? = 3.67 x 10-8 3.67 x 10-8 3.67 x 10-2 Walk ;<=>

-7 B2#"9 = 1.87 x 10 Directional 6.58 16.84 0.000 : -8 A2#"9 = 1.54 x 10

A: = 9.07 x 10-8 Ornstein- 2#"9 8.91 Inf 0.000 > = 1.03 Uhlenbeck -5 G = 3.60 x 10

M2 width Strict Stasis -4.56 12.45 0.000 > = 0.799

> = 0.780 Stasis 7.68 -5.34 0.073 ? = 0.00235 Random 10.22 -10.44 0.926 J? = 7.08 x 10-9 7.08 x 10-9 7.08 x 10-3 Walk ;<=>

-7 B2#"9 = 1.48 x 10 Directional 12.83 4.34 0.001 : -9 A2#"9= 1.06 x 10

A: = 1.00 x 10-10 Ornstein- 2#"9 16.16 Inf 0.000 > = 0.823 Uhlenbeck -6 G = 2.88 x 10

M3 length Strict Stasis -22.38 48.10 0.000 > = 1.29

> = 1.26 Stasis 5.06 -0.118 0.048 ? = 0.00718 Random 8.05 -6.10 0.952 J? = 2.16 x 10-8 2.16 x 10-8 2.16 x 10-2 Walk ;<=>

-7 B2#"9 = 1.98 x 10 Directional 9.13 11.73 0.000 : -8 A2#"9 = 1.16 x 10

A: = 7.68 x 10-9 Ornstein- 2#"9 11.99 Inf 0.000 > = 1.28 Uhlenbeck -6 G = 7.33 x 10

M3 width Strict Stasis -5.10 13.54 0.000 > = 0.700

> = 0.680 Stasis 5.81 -1.62 0.067 ? = 0.000495 Random 8.44 -6.88 0.933 J? = 1.53 x 10-8 1.53 x 10-8 1.53 x 10-2 Walk ;<=>

-7 B2#"9 = 1.94 x 10 Directional 9.86 10.29 0.000 : -9 A2#"9 = 6.11 x 10

A: = 1.00 x 10-10 Ornstein- 2#"9 14.76 Inf 0.000 Uhlenbeck > = 0.717 G = 0.00383 Table 2.9 Evolutionary model-fitting results for the Phenacolemur pagei – Phenacolemur praecox lineage using Hunt’s (2008) joint parameterization method. Expected squared divergence (ESD) is reported for one generation and one million generations. For each trait, the best-supported model is in bold. AICC, Akaike information criterion; LogL, Log-likelihood. 145

Table 2.10 ESD Akaike ESD Trait Model LogL AIC Parameter estimates (1 x 106 C weight (1 gen.) gens.) Strict P4 length 9.50 -16.00 0.138 >=1.19 Stasis

> = 1.18 Stasis 11.73 -15.45 0.105 ? = 7.00 x 10-4 Random 13.61 -19.22 0.689 J? = 1.86 x 10-9 2.31 x 10-2 2.31 x 104 Walk ;<=>

-8 B2#"9 = 6.17 x 10 Directional 16.31 -14.61 0.069 : A2#"9 = 0.000 : -9 Ornstein- A2#"9 =1.01 x 10 Uhlenbeck 14.44 19.12 0.000 > = 1.22 G = 1.15 x 10-6 Strict P width -7.52 18.04 0.000 >=0.801 4 Stasis

> = 0.793 Stasis 8.59 -9.18 0.022 ? = 0.00290 Random 12.19 -16.38 0.803 J? = 5.48 x 10-9 5.48 x 10-9 5.48 x 10-3 Walk ;<=>

-7 B2#"9 = 1.04 x 10 Directional 15.67 -13.33 0.175 : A2#"9 = 0.000 : -9 Ornstein- A2#"9 = 2.67 x10 Uhlenbeck 13.80 20.40 0.000 > = 0.860 G = 1.45 x 10-6 P 4 Strict protoconid -166.98 336.96 0.000 >= 0.275 Stasis height > = 0.307 Stasis -0.790 9.58 0.002 ? = 0.0748 Random 5.51 -3.01 0.909 A: = 8.94 x 10-8 8.94 x 10-8 8.94 x 10-2 Walk 2#"9

-7 B2#"9 = -4.62 x 10 Directional 8.18 1.63 0.0.089 : -8 A2#"9= 2.35 x 10 : -8 Ornstein- A2#"9 = 5.67 x 10 Uhlenbeck 7.04 33.91 0.000 > = -0.105 G = 9.52 x 10-7 Strict P height -31.57 66.15 0.000 > = 1.15 4 Stasis

> = 1.17 Stasis 5.65 -3.30 0.019 ? = 0.00827 Random 9.57 -11.13 0.969 J? = 1.64 x 10-8 1.64 x 10-8 1.64 x 10-2 Walk ;<=>

-7 B2#"9 = -1.23 x 10 Directional 10.15 -2.30 0.012 : -8 A2#"9 = 1.09 x 10

146 Table 2.10 Continued

: -8 Ornstein- A2#"9 = 1.65 x 10 Uhlenbeck 10.25 27.50 0.000 > = 1.06 G = 1.19 x 10-6 Strict M1 length 16.79 -30.58 0.900 K = 1.02 0 0 Stasis

> = 1.02 Stasis 16.79 -25.58 0.074 ? = 0.000 Random 15.73 -23.45 0.026 A: = 2.30 x 10-10 Walk 2#"9

-8 B2#"9 = 1.75 x 10 Directional 16.88 -15.75 0.001 : A2#"9 = 0.000 : -10 Ornstein- A2#"9 = 2.34 x 10 Uhlenbeck 15.72 16.55 0.000 > = 1.00 G = 1.00 x 10-8 Strict M1 width 9.26 -15.52 0.167 > = 0.824 Stasis

K = 0.822 Stasis 13.03 -18.05 0.591 1.06 x 10-3 1.06 x 10-3 M = 5.31 x 10-4 Random 12.13 -16.25 0.240 A: = 4.54 x 10-9 Walk 2#"9

-8 B2#"9 = 1.12 x 10 Directional 12.14 -6.27 0.002 : -9 A2#"9 = 4.28 x 10 : -7 Ornstein- A2#"9 = 4.04 x 10 Uhlenbeck 13.08 21.84 0.000 > = 0.805 G = 1.93 x 10-4 Strict M length 11.62 -20.24 0.853 K = 1.02 5.20 x 10-4 5.20 x 10-4 2 Stasis

> = 1.01 Stasis 11.71 -15.41 0.076 ? = 2.60 x 10-4 Random 11.62 -15.24 0.070 A: = 0.000 Walk 2#"9

-9 B2#"9 = 8.01 x 10 Directional 11.73 -5.46 0.001 : A2#"9 = 0.000 : -10 Ornstein- A2#"9 = 1 x 10 Uhlenbeck 11.40 25.20 0.000 > = 0.986 G = 1.00 x 10-8 Strict M width 13.34 -23.69 0.491 K = 0.815 4.81 x 10-4 4.81 x 10-4 2 Stasis

> = 0.816 Stasis 14.41 -20.81 0.117 ? = 2.41 x 10-4 Random 15.51 -23.02 0.352 A: = 1.19 x 10-9 Walk 2#"9

-8 B2#"9 = 4.20 x 10 Directional 18.37 -18.73 0.041 : A2#"9 = 0.000

147 Table 2.10 Continued

: -10 Ornstein- A2#"9 = 1x10 Uhlenbeck 18.09 11.81 0.000 > = 0.829 G = 4.04 x 10-6 Strict M3 length 15.15 -27.31 0.914 K = 1.31 0 0 Stasis

> = 1.31 Stasis 15.15 -22.31 0.075 ? = 0.000 Random 13.18 -18.37 0.010 A: = 1.14 x 10-9 Walk 2#"9

-8 B2#"9 = 1.94 x 10 Directional 14.96 -11.91 0.000 : A2#"9 = 0.000 : -9 Ornstein- A2#"9 = 8.41 x 10 Uhlenbeck 14.42 19.16 0.000 > = 1.30 G = 3.06 x 10-5 Strict M3 width 17.03 -31.06 0.879 K = 0.723 0 0 Stasis

> = 0.723 Stasis 17.03 -26.07 0.072 ? = 0.000 Random 16.61 -25.23 0.047 A: = 2.60 x 10-10 Walk 2#"9

-8 B2#"9 = 2.28 x 10 Directional 18.03 -18.07 0.001 : A2#"9 = 0.000 : -10 Ornstein- A2#"9 = 1.00 x 10 Uhlenbeck 17.78 12.43 0.000 > = 0.740 G = 2.10 x 10-6 Table 2.10 Evolutionary model-fitting results for the Phenacolemur praecox – Phenacolemur fortior lineage using Hunt’s (2008) joint parameterization method. Expected squared divergence (ESD) is reported for one generation and one million generations. For each trait, the best-supported model is in bold. AICC, Akaike information criterion; LogL, Log-likelihood.

148 Table 2.11 ESD Akaike ESD 6 Trait Model LogL AICC Parameter estimates (1 x 10 weight (1 gen.) gens.) Strict P4 length -65.31 133.41 0.000 D = 1.09 Stasis D = 1.09 Stasis 5.78 -4.55 0.046 E = 0.0107 Random 8.76 -10.54 0.924 G0 = 4.29 x 10-8 4.29 x 10-8 4.29 x 10-2 Walk ,-./ -8 F)*+( = -5.46 x 10 Directional 8.81 -3.63 0.029 ' -8 C)*+( = 4.21 x 10

C' = 5.11 x 10-8 Ornstein- )*+( 9.31 9.39 0.000 D = 1.17 Uhlenbeck -6 J = 1.71 x 10 Strict P4 width -62.04 126.88 0.000 D= 0.710 Stasis D = 0.708 Stasis 5.45 -3.90 0.019 E = 0.0118 Random 9.35 -11.71 0.941 G0 = 3.32 x 10-8 3.32 x 10-8 3.32 x 10-2 Walk ,-./ -7 F)*+( = -1.30 x 10 Directional 9.70 -5.40 0.040 ' -8 C)*+( = 2.85 x 10 C' = 3.49 x 10-8 Ornstein- )*+( 10.74 6.52 0.000 D = 0.721 Uhlenbeck -6 J = 2.88 x 10 P4 Strict protoconid -67.05 136.89 0.000 D= 0.129 Stasis height D = 0.177 Stasis 1.59 3.83 0.014 E = 0.0355 Random 5.75 -4.51 0.871 G0 = 8.81 x 10-8 8.81 x 10-8 8.81 x 10-2 Walk ,-./ -7 F)*+( = 3.74 x 10 Directional 7.24 -0.472 0.116 ' -8 C)*+( = 3.54 x 10 ' -8 C)*+( = 6.57 x 10 Ornstein- 6.88 14.24 0.000 D = 0.445 Uhlenbeck J = 9.95 x 10-7 Strict P4 height -22.45 47.70 0.000 D = 1.04 Stasis D = 1.06 Stasis 7.91 -8.82 0.396 E = 5.56 x 10-3 Random 8.29 -9.58 0.580 G0 = 4.65 x 10-8 4.65 x 10-8 4.65 x 10-2 Walk ,-./

149 Table 2.11 Continued

-7 F)*+( = 1.38 x 10 Directional 8.57 -3.15 0.023 ' -8 C)*+( = 4.12 x 10

C' = 4.95 x 10-8 Ornstein- )*+( 8.80 10.40 0.000 D = 1.22 Uhlenbeck -6 J = 1.05 x 10 Strict M1 length 0.476 1.85 0.000 D = 0.976 Stasis D = 0.975 Stasis 12.46 -17.92 0.127 E = 1.39 x 10-3 Random 14.35 -21.70 0.846 G0 = 5.96 x 10-9 5.96 x 10-9 5.96 x 10-3 Walk ,-./ -8 F)*+( = -3.82 x 10 Directional 14.38 -14.75 0.026 ' -9 C)*+( = 6.03 x 10

C' = 7.85 x 10-9 Ornstein- )*+( 14.89 -1.79 0.000 D = 1.00 Uhlenbeck -6 J = 1.97 x 10 Strict M1 width -54.31 111.42 0.000 D = 0.737 Stasis D = 0.746 Stasis 9.06 -11.13 0.037 E = 4.19 x 10-3 Random 12.27 -17.54 0.920 G0 = 1.39 x 10-8 1.39 x 10-8 1.39 x 10-2 Walk ,-./ -7 F)*+( = -1.03 x 10 Directional 12.69 -11.39 0.042 ' -8 C)*+( = 1.18 x 10 ' -8 C)*+( = 1.28 x 10 Ornstein- 14.79 -1.58 0.000 D = 0.748 Uhlenbeck J = 4.54 x 10-6 Strict M2 length 4.93 -7.07 0.000 D = 0.965 Stasis D = 0.967 Stasis 13.24 -19.48 0.223 E = 1.06 x 10-3 Random 14.44 -21.88 0.742 G0 = 5.65 x 10-9 5.65 x 10-9 5.65 x 10-3 Walk ,-./ -8 F)*+( = -5.88 x 10 Directional 14.87 -15.73 0.034 ' -9 C)*+( = 4.33 x 10

C' = 5.44 x 10-9 Ornstein- )*+( 16.84 -5.67 0.000 D = 0.975 Uhlenbeck -6 J = 5.56 x 10 Strict M2 width -21.11 45.02 0.000 D = 0.741 Stasis D = 0.754 Stasis 9.92 -12.84 0.019 E = 3.15 x 10-3 150 Table 2.11 Continued

Random 13.81 -20.62 0.932 G0 = 7.77 x 10-9 7.77 x 10-9 7.77 x 10-3 Walk ,-./ -8 F)*+( = -8.40 x 10 Directional 14.35 -14.71 0.049 ' -9 C)*+( = 6.09 x 10

C' = 7.32 x 10-9 Ornstein- )*+( 15.56 -3.12 0.000 D = 0.758 Uhlenbeck -6 J = 3.03 x 10 Strict M3 length 9.48 -16.17 0.163 D = 1.28 Stasis D = 1.28 Stasis 12.49 -17.97 0.401 E = 1.08 x 10-3 Random 12.54 -18.08 0.423 G0 = 8.13 x 10-9 8.13 x 10-9 8.13 x 10-3 Walk ,-./ -9 F)*+( = -9.48 x 10 Directional 12.55 -11.09 0.013 ' -9 C)*+( = 8.00 x 10

C' = 9.59 x 10-9 Ornstein- )*+( 12.76 2.48 0.000 D = 1.34 Uhlenbeck -7 J = 7.97 x 10 Strict M3 width 11.06 -19.33 0.389 H = 0.683 0 0 Stasis D = 0.686 Stasis 12.60 -18.20 0.221 E = 8.74 x 10-4 Random 13.13 -19.26 0.377 C' = 4.73 x 10-9 Walk )*+( -8 F)*+( = -4.54 x 10 Directional 13.30 -12.61 0.014 ' -9 C)*+( = 4.22 x 10

C' = 6.45 x 10-9 Ornstein- )*+( 14.40 -0.792 0.000 D = 0.693 Uhlenbeck -6 J = 4.11 x 10 Table 2.11 Evolutionary model-fitting results for the Phenacolemur fortior – Phenacolemur citatus lineage using Hunt’s (2008) joint parameterization method. Expected squared divergence (ESD) is reported for one generation and one million generations. For each trait, the best-supported model is in bold. AICC, Akaike information criterion; LogL, Log-likelihood.

151 Table 2.12 ESD Akaike ESD 6 Trait Model LogL AICC Parameter estimates (1 x 10 weight (1 gen.) gens.) Strict P4 length -44.01 90.59 0.000 D=1.09 Stasis D = 1.09 Stasis 9.75 -13.50 0.046 E = 0.00624 Random 12.70 -19.39 0.871 G0 = 2.32 x 10-8 2.32 x 10-8 2.32 x 10-2 Walk ,-./ -9 F)*+( = -4.29 x 10 Directional 12.70 -14.59 0.079 ' -8 C)*+( = 2.32 x 10

C' = 2.78 x 10-8 Ornstein- )*+( 13.26 -8.51 0.004 D = 1.17 Uhlenbeck -6 J = 1.06 x 10 Strict P4 width -10.64 23.84 0.000 D= 0.689 Stasis D = 0.691 Stasis 11.70 -17.40 0.046 E = 0.00375 Random 14.64 -23.28 0.869 G0 = 1.05 x 10-8 1.05 x 10-8 1.05 x 10-2 Walk ,-./ -8 F)*+( = -1.42 x 10 Directional 14.66 -18.53 0.081 ' -8 C)*+( = 1.03 x 10 C' = 1.41 x 10-8 Ornstein- )*+( 15.39 -12.78 0.005 D = 0.721 Uhlenbeck -6 J = 1.46x 10 P4 Strict protoconid -61.64 125.86 0.000 D= 0.348 Stasis height D = 0.378 Stasis 4.55 -3.10 0.055 E = 0.0200 Random 7.30 -8.60 0.862 G0 = 7.14 x 10-8 7.14 x 10-8 7.14 x 10-2 Walk ,-./ -8 F)*+( = -3.02 x 10 Directional 7.31 -3.81 0.079 ' -8 C)*+( = 7.11 x 10 ' -8 C)*+( = 8.93 x 10 Ornstein- 7.88 2.24 0.004 D = 0.445 Uhlenbeck J = 1.17 x 10-6 Strict - P4 height 206.14 0.000 D = 1.12 Stasis 101.79 D = 1.14 Stasis 7.25 -8.49 0.046 E = 0.0112 Random 10.18 -14.36 0.872 G0 = 4.40 x 10-8 1.03 x 10-3 4.30 x 10-2 Walk ,-./

152 Table 2.12 Continued

-10 F)*+( = -6.30 x 10 Directional 10.17 -9.56 0.078 ' -8 C)*+( = 4.44 x 10

C' = 5.33 x 10-8 Ornstein- )*+( 10.72 -3.44 0.004 D = 1.22 Uhlenbeck -6 J = 1.08 x 10 Strict M1 length 3.41 -4.25 0.000 D = 0.981 Stasis D = 0.983 Stasis 16.58 -27.17 0.021 E = 0.00117 Random 20.34 -34.68 0.897 G0 = 2.63 x 10-9 2.63 x 10-9 2.63 x 10-3 Walk ,-./ -9 F)*+( = -7.38 x 10 Directional 20.31 -29.83 0.079 ' -9 C)*+( = 2.63 x 10

C' = 3.30 x 10-9 Ornstein- )*+( 20.73 -23.47 0.003 D = 1.00 Uhlenbeck -7 J = 8.53 x 10 Strict M1 width -34.49 71.55 0.000 D = 0.747 Stasis D = 0.753 Stasis 13.30 -20.60 0.009 E = 0.00280 Random 17.92 -29.84 0.885 G0 = 4.81 x 10-9 4.81 x 10-9 4.81 x 10-3 Walk ,-./ -8 F)*+( = -2.91 x 10 Directional 18.14 -25.47 0.100 ' -9 C)*+( = 4.11 x 10 ' -9 C)*+( = 5.89 x 10 Ornstein- 18.90 -19.80 0.006 D = 0.748 Uhlenbeck J = 1.46 x 10-6 Strict M2 length 0.695 1.18 0.000 D = 0.978 Stasis H = 0.973 Stasis 16.27 -26.54 0.541 2.58 x 10-3 2.58 x 10-3 K = 1.29 x 10-3 Random 15.98 -25.97 0.407 C' = 2.06 x 10-9 Walk )*+( -8 F)*+( = -2.13 x 10 Directional 16.28 -21.76 0.050 ' -9 C)*+( = 1.19 x 10

C' = 4.06 x 10-9 Ornstein- )*+( 17.04 -16.09 0.003 D = 0.975 Uhlenbeck -6 J = 2.12 x 10 Strict M2 width -34.47 71.51 0.000 D = 0.757 Stasis D = 0.757 Stasis 15.00 -24.00 0.006 E = 1.93 x 10-3 153 Table 2.12 Continued

Random 20.10 -34.21 0.905 G0 = 3.33 x 10-9 3.33 x 10-9 3.33 x 10-3 Walk ,-./ -8 F)*+( = -1.76 x 10 Directional 20.14 -29.48 0.085 ' -9 C)*+( = 3.27 x 10

C' = 4.13 x 10-9 Ornstein- )*+( 20.74 -23.48 0.004 D = 0.758 Uhlenbeck -6 J = 1.13 x 10 Strict M3 length -34.47 71.51 0.000 D = 0.757 Stasis D = 0.757 Stasis 15.00 -24.00 0.006 E = 0.00193 Random 20.10 -34.21 0.905 G0 = 3.33 x 10-9 3.33 x 10-9 3.33 x 10-3 Walk ,-./ -8 F)*+( = -1.76 x 10 Directional 20.14 -29.48 0.085 ' -9 C)*+( = 3.27 x 10

C' = 4.13 x 10-9 Ornstein- )*+( 20.74 -23.48 0.004 D = 0.758 Uhlenbeck -6 J = 1.13 x 10 Strict M3 width 16.86 -31.14 0.183 D = 0.688 Stasis D = 0.688 Stasis 18.19 -30.38 0.125 E = 4.96 x 10-4 Random 19.70 -33.39 0.564 G0 = 1.28 x 10-9 1.28 x 10-9 1.28 x 10-3 Walk ,-./ -8 F)*+( = -1.89 x 10 Directional 20.59 -30.39 0.126 ' C)*+( = 0.000

C' = 1.82 x 10-9 Ornstein- )*+( 20.35 -22.70 0.003 D = 0.693 Uhlenbeck -6 J = 1.33 x 10 Table 2.12 Evolutionary model-fitting results for the Phenacolemur praecox – Phenacolemur citatus lineage using Hunt’s (2008) joint parameterization method. Expected squared divergence (ESD) is reported for one generation and one million generations. For each trait, the best-supported model is in bold. AICC, Akaike information criterion; LogL, Log-likelihood.

154

Table 2.13

' ' Trait Displacement C ( Ne E t1/2

P4 protoconid height +1.00 0.00572 27,900 – 195,000 427 – 2990 517,000

P4 height +1.67 0.00448 21,800 – 153,000 415 – 2900 642,000

Table 2.13 Estimates and ranges for population genetic parameters computed from the maximum-likelihood parameter estimates of the Ornstein-Uhlenbeck model for P4 tooth metric in the Phenacolemur simonsi – Phenacolemur willwoodensis lineage. Displacement is the difference between the initial trait value and the optimal trait value of the lineage in standard deviation units (calculated from the pooled phenotypic variance across samples, (C' ). Effective population size ranges were calculated with an assumed trait heritability ( range between 0.1 and 0.7 and reported ranges reflect calculations using these two end-member heritability values. The last column, t1/2, is the time in generations for the population to reach the halfway point to the phenotypic optimum.

Table 2.14 ESD Akaike Parameter ESD 6 Trait Model LogL AICC (1 x 10 weight estimates (1 gen.) gens.) Strict P4 length 4.43 -5.53 0.386 D = 0.647 stasis D = 0.646, E = Stasis 6.56 -3.12 0.116 0.00279 Random G = 5.41 x 10- 8.02 -6.03 0.498 ,-./ 5.41 x 10-9 5.41 x 10-3 walk 9 - F)*+( = 6.75 x 10 Directional 10.20 9.60 0.000 8 C)*+( = 0.000 - C)*+( = 1.49 x 10 Ornstein- 9 Uhlenbeck 8.83 Inf 0.000 D = 0.771 J = 4.69 x 10-7 Strict P4 width 2.16 -0.985 0.055 D = 0.278 stasis D = 0.278 Stasis 6.66 -3.31 0.177 E = 0.00311 Random G = 4.23 x 10- 8.12 -6.24 0.767 ,-./ 4.23 x 10-9 4.23 x 10-3 walk 9 F = 6.70 x 10- Directional 11.12 7.76 0.001 )*+( 8 155 Table 2.14 Continued

C)*+( = 0.000

-10 Ornstein- C)*+( = 1x10 Uhlenbeck 10.69 Inf 0.000 D = 0.393 J = 7.62 x 10-7

Strict -3 -3 M1 length 8.23 -13.14 0.833 H = 0.715 1.45 x 10 1.45 x 10 stasis D = 0.718 Stasis 8.63 -7.26 0.044 E = 7.25 x 10-4 Random C = 2.66 x 10- 9.66 -9.31 0.123 )*+( walk 9 - F)*+( = 4.68 x 10 Directional 11.83 6.33 0.000 8 C)*+( = 0.000 -10 Ornstein- C)*+( = 1x10 Uhlenbeck 11.37 Inf 0.000 D = 0.806 J = 5.82 x 10-7

Strict -3 -3 M1 width 7.90 -12.47 0.803 H = 0.426 1.67 x 10 1.67 x 10 stasis D = 0.428 Stasis 8.28 -6.55 0.042 E = 8.36 x 10-4 Random C = 2.26 x 10- 9.59 -9.19 0.156 )*+( walk 9 - F)*+( = 4.14 x 10 Directional 11.45 7.09 0.000 8 C)*+( = 0.000 -10 Ornstein- C)*+( = 1x10 Uhlenbeck 10.99 Inf 0.000 D = 0.519 J = 5.18 x 10-7

Strict -3 -3 M2 length 5.39 -7.45 0.783 H = 0.691 4.79 x 10 4.79 x 10 stasis D = 0.690 Stasis 6.45 -2.90 0.081 E = 2.40 x 10-3 Random 6.98 -3.95 0.137 C = 4.45 x 10-9 walk )*+( - F)*+( = 6.05 x 10 Directional 8.91 12.19 0.000 8 C)*+( = 0.000 -10 Ornstein- C)*+( = 1.0 x 10 Uhlenbeck 8.21 Inf 0.000 D = 0.802 J = 6.70 x 10-7

Strict -3 -3 M2 width 7.54 -11.75 0.832 H = 0.430 2.05 x 10 2.05 x 10 stasis D = 0.428 Stasis 8.20 -6.40 0.057 E = 1.03 x 10-3

156 Table 2.14 Continued Random C = 1.65 x 10- 8.86 -7.72 0.111 )*+( walk 9 - F)*+( = 4.34 x 10 Directional 10.99 8.02 0.000 8 C)*+( = 0.000 -10 Ornstein- C)*+( = 1.0 x 10 Uhlenbeck 10.82 Inf 0.000 D = 0.524 J = 5.39 x 10-7

Strict -4 -4 M3 length 8.71 -14.09 0.952 H = 0.963 9.24 x 10 9.24 x 10 stasis D = 0.965 Stasis 8.87 -7.74 0.040 E = 4.62 x 10-4 Random C = 7.91 x 10- 7.24 -4.48 0.008 )*+( walk 9 - F)*+( = 3.44 x 10 Directional 10.21 9.57 0.000 8 C)*+( = 0.000 C = 2.14 x 10- Ornstein- )*+( 9 Uhlenbeck 9.63 Inf 0.000 = 1.03 D J = 5.64 x 10-6

Strict -3 -3 M3 width 6.48 -9.63 0.925 H=0.411 3.22 x 10 3.22 x 10 stasis D = 0.412 Stasis 7.24 -4.48 0.071 E = 1.61 x 10-3 Random 4.52 0.958 0.005 C = 4.52 x 10-8 walk )*+( -8 F)*+(= 6.32 x 10 Directional 4.62 20.76 0.000 -8 C)*+(= 4.12 x 10 -10 Ornstein- C)*+(=1.0 x 10 Uhlenbeck 10.71 Inf 0.000 D=0.440 J= 3.78 x 10-3 Table 2.14 Evolutionary model-fitting results for the Phenacolemur simonsi – Phenacolemur willwoodensis lineage using Hunt’s (2008) joint parameterization method. Expected squared divergence (ESD) is reported for one generation and one million generations. For each trait, the best-supported model is in bold. AICC, Akaike information criterion; LogL, Log-likelihood. Analyses for P4 protoconid height and height are excluded because of lack of data for P. willwoodensis.

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172

Chapter 3. The Role of Climate Change on the Dental Evolution of Late Paleocene and

Early Eocene Paromomyids

3.1 Introduction

The Bighorn Basin is an approximately 100-mile-wide intermontane basin located in northwest Wyoming in the United States. It is surrounded by four mountain ranges, the

Bighorn Mountains to the east, the Absaroka Mountains to the west, and the Owl Creek and Bridger Mountains to the south. The basin is open on its northern end. During the

Paleocene and early Eocene, alluvial sediments accumulated in the Bighorn Basin forming the Fort Union and Willwood formations (Neasham and Vondra 1972; Bown

1980; Bown and Kraus 1981, 1993). The main source of sediments creating these formations were the surrounding mountain ranges formed during the Laramide orogeny

(Omar et al. 1994).

Over a century of collecting from the 770-meter Willwood formation in the

Bighorn Basin has provided a large fossil record of Wasatchian mammals (early Eocene

North American Land Mammal Age, NALMA) with a detailed record of their stratigraphic ranges (Bown 1979; Gingerich 1980a; Schankler 1980; Bown and Kraus

1993; Bown et al. 1994b), ranging from Wasatchian zone 0 (Wa-0) (earliest

Sandcouleean subage) to Wasatchian zone Wa-7 (earliest Lostcabinian subage; Robinson et al. 2004). The base of the Willwood formation corresponds to approximately 55.8 ±

0.2 million years ago (Secord et al. 2006; Gradstein et al. 2012), near the Paleocene-

173 Eocene boundary, and the top of the formation to 52.6 million years ago (Smith et al.

2004). This time period is important as it includes several mammal radiations, faunal turnover events, and gradual and rapid climate change (Schankler 1980; Bown and Kihm

1981; Rose 1981; Bown and Kraus 1981; Stucky 1984; Rea et al. 1990; Wing 1998;

Wing et al. 1991, 2000, 2005; Robinson et al. 2004; Lourens et al. 2005; Chew 2005,

2009; Zack 2011).

Two major turnover events of vertebrate fauna occurred in the early Eocene and involved high rates of species appearance and disappearance. The first turnover event is termed Biohorizon A and it occurred at the beginning of the Eocene (Wa-0, NALMA) and lasted approximates 300,000 years (55.1-54.8 Ma, 180-219 m above the base of the

Willwood Formation). Biohorizon A was directly related to global warming at the

Paleocene-Eocene (P/E) boundary (Schankler 1980; Gingerich 1989, 2001, 2003; Clyde and Gingerich 1998; Clyde 2001; Strait 2001; Bowen et al. 2004; Wing et al. 2005; Chew

2006, 2009) and included the widespread appearance and dispersal of artiodactyls, perisodactyls, and euprimates in the Northern Hemisphere (Robinson et al. 2004). A second major turnover event, termed Biohorizon B, occurred at the beginning of the fourth Wasatchian NALMA (Wa-4) and lasted approximately 200,000 years (54.2-54.0

Ma, 380-419 m above the base of the Willwood Formation; Chew 2006, 2009; Silcox et al. 2008). Biohorizon B represents a time of increased migration, marked by a higher proportion of generic appearances into the Bighorn Basin, including the genera

Copelemur (adapiform primate), Absarokius and Steinius (omomyid primates; Chew

2009).

174 Paleoclimatic conditions during the late Paleocene and Eocene in the Bighorn

Basin have been reconstructed using leaf margins (e.g., Wing et al. 2000; Wing and

Harrington 2001), oxygen isotope ratios of hematitic soil nodules, and fossil dental enamel (Koch et al. 1995; Fricke et al. 1998; Wing 1998; Bao et al. 1999; Koch and

Morril 2000; Wing et al. 1991, 2000, 2005; Chew 2009). Mean Annual Temperature

(MAT) increased at the beginning of the Eocene, reaching as high as 19oC by approximately 55.56 Ma, before the beginning of Biohorizon A (55.1 Ma). Temperatures then decreased abruptly until 54.38 Ma, before the beginning of Biohorizon B (54.2 Ma), reaching a minimum mean annual temperature of approximately 11oC. Temperatures then began to increase dramatically again reaching a peak at the end of the early Eocene, termed the early Eocene climatic optimum. Hence, Biohorizon A occurs at the beginning of the early Eocene cooling interval and Biohorizon B occurs during the phase of rapid temperature increase (Koch et al. 1995; Fricke et al. 1998; Wing 1998; Bao et al. 1999;

Koch and Morril 2000; Wing et al. 1991, 2000, 2005; Silcox et al. 2008; Chew 2009).

The detailed fossil record of the Bighorn Basin, coupled with the two biostratigraphic zones and their establishment among the Bighorn Basin’s Willwood mammals (Schankler 1980; Chew 2009), and the extensive paleosol and paleomagnetic work done on the Willwood Formation, offers researchers an accurate measure of

Wasatchian time in the Bighorn Basin (Van Houten 1944; Neasham and Vondra 1972;

Bown 1979; Bown and Kraus 1981; Butler et al. 1981, 1987; Rapp et al 1983; Flynn

1986; Bown and Kraus 1993; Clyle et al. 1994). These records make the Willwood

Formation in the Bighorn Basin an important part of the discussion on the general

175 evolutionary patterns, or modes, of early Eocene mammal evolution and the potential influence of climate on the macroevolutionary patterns of mammalian evolution.

This chapter focuses on the role of climate change in the radiation of the Ignacius and Phenacolemur parmomomyid primates and addresses whether the observed morphological changes in the lower dentition of the Ignacius frugivorus – Phenacolemur citatus lineage were influenced by paleoclimate. The I. frugivorus – P. citatus lineage evolved in the Bighorn Basin during the late Paleocene and early Eocene and showcases an evolutionary transition from the genus Ignacius to the genus Phenacolemur with several species level transitions occurring between the earliest and latest individuals. The species of this lineage include Ignacius frugivorus, Phenacolemur pagei, Phenacolemur praecox, Phenacolemur fortior, and Phenacolemur citatus. Many of these species were relatively common and, therefore, a decent fossil record documenting their dental evolution exists.

The genus level transition between I. frugivorus and P. pagei, occurs during the late Paleocene, with a possible intermediate type species, P. archus, bridging the two species (Secord 2008). Phenacolemur pagei is replaced by P. praecox (Rose 1981;

Secord 2008), a species that goes extinct at the beginning of Biohorizon A.

Phenacolemur praecox was replaced by P. fortior at the beginning of Biohorizon A. This evolutionary transition is evidenced by intermediate forms referred to as the P. praecox –

P. fortior intermediates (Silcox et al. 2008). There are currently two hypotheses relating

P. citatus to earlier occurring Phenacolemur. The first is that P. citatus descended from

P. fortior through budding cladogenesis within the Bighorn Basin (Silcox et al. 2008;

176 López-Torres et al. 2018). The second hypothesis proposes that P. citatus descended from P. praecox by means of allopatric speciation that possibly occurred outside of the

Bighorn Basin and then P. citatus migrated back into the Bighorn Basin around the beginning of Biohorizon A (Fig. 3.1; Silcox et al. 2008). For the purposes of the research presented here, I treat all species previously mentioned as one evolving lineage with P. citatus descending from P. fortior.

This lineages’ dental evolution is complex in that it reveals several dietary shifts, as well as changes in their lower posterior teeth (P4, M1, M2, and M3). Overall, I see shifts back and forth between an omnivorous-frugivorous diet and a stricter omnivorous diet and shifting patterns in tooth metrics (P4, M1, M2, and M3 length and width, and P4 protoconid height and height) between that of increasing and decreasing through time

(Figs. 3.1 and 3.2). Several of these changes appear to coincide with the biohorizon events and periods of climate cooling and warming. Specifically, during the cooling period between Biohorizon A and Biohorizon B, there is a general decrease in the tooth metrics of the lower dentition from the previous warming period before Biohorizon A.

When temperatures begin to cool after Biohorizon B there is a general increase in these same tooth metrics. These observations reflect some of the trends I observed in Chapter 1 of this dissertation between MAT and tooth length and width in the Tetonius –

Pseudotetonius dentition. In that study, I found that P3 length was inversely correlated to temperature before Biohorizon A and then after Biohorizon A during the cooling period,

P3 length had a positive correlation to MAT. Overall, I found the P4 to be more responsive to changes in temperature than the molar teeth.

177 Increases or decreases in tooth size, particularly molar tooth size, are reflective of changes in primate body size (Kay 1975; Gingerich 1977, 1981; Gingerich et al. 1980,

1982; Kay and Simons 1980; Gingerich and Smith 1985; Conroy 1987; Dagosto and

Terranova 1992). The observation that tooth size in this paromomyid lineage appears to have a direct relationship with MAT, opposes Bergmann’s Rule. Bergmann’s Rule predicts that closely related endothermic species or populations within a species are generally larger bodied at cooler climates and smaller bodied at warmer climates (Mayr

1963). In mammals, this phenomenon has been explained by larger sizes offering heat- conserving effects as a result of the lower ratio of surface area relative to volume

(Blackburn et al. 1999; Blackburn and Hawkins 2004); however, this explanation is likely inadequate as cold temperatures and large size are correlated among several poikilothermic taxa as well (Strauch 1968; Partridge and Coyne 1997; Blackburn et al.

1999; Huey et al. 2000; Ashton and Feldman 2003; Olalla-Tarraga and Rodrigues 2007, among others).

The analyses of this chapter attempt to determine if there was significant correlation, or lack of correlation, between changes in tooth metrics of these paromomyid’s lower dentitions, and climate variation, specifically Mean Annual

Temperature, in the Bighorn Basin. If significant correlations are found, it may imply that there were causal relationships between environmental change and paromomyid dental evolution in the Bighorn Basin. If significant correlations are not found, this may suggest that other controls were responsible for the evolutionary patterns observed in the dentitions of paromomyids from the Bighorn Basin. Based on my observations from the

178 fossil record, I test the following hypotheses: (1) the Ignacius frugivorus – Phenacolemur citatus lineage responded with increasing tooth sizes during intervals of climate warming;

(2) the Ignacius frugivorus – Phenacolemur citatus lineage responded with decreasing tooth sizes during the interval of climate cooling.

3.2 Materials and Methods

The Sample

The sample includes individuals of the paromomyid species Ignacius frugivorus,

Ignacius graybullianus, Phenacolemur praecox, Phenacolemur fortior, and

Phenacolemur citatus from the Willwood Formation of the southern Bighorn Basin,

Wyoming. Individuals of Ignacius frugivorus, and Phenacolemur pagei are from the Fort

Union Formation of the northern Bighorn Basin. All specimens included in this study have known stratigraphic levels within the Fort Union Formation (Tiffanian, Ti-1 through

Ti-6 and Clarkforkian, Cf-1 through Cf-3 NALMA; Rose 1981; Gingerich 1975, 1976) and the Willwood Formation (Wasatchian, Wa-0 through Wa-7 NALMA; Bown et al.,

1994b). Fossils were either excavated, surface collected, or screenwashed from the

Bighorn Basin by expeditions from Yale (Y), University of Wyoming (UW), United

States Geological Survey (USGS), and Johns Hopkins University (JHU) between 1960 and the mid-1990s (Silcox et al. 2008).

Ancestor – descendant relationships of Ignacius and Phenacolemur

As discussed in Chapter 2 of this dissertation, several researchers have proposed ancestor-descendant relationships within and between species of Ignacius and

Phenacolemur based on their observations of similar dental and postcranial morphology,

179 and geographic and stratigraphic occurrence (Bown and Rose 1976; Rose and Gingerich

1976; Szalay and Delson 1979; Rose 1981; Bloch et al. 2007; Secord 2008; Silcox et al.

2008). From these previous hypotheses, I compiled a proposed phylogeny of Ignacius and Phenacolemur species. The lineage of longest duration in this phylogeny begins with

I. fremontensis and ends with P. citatus. Since this study compares MAT estimates of the

Bighorn Basin to the fossil dental records of paromomyids, only individuals collected from the Bighorn Basin were included. As a result, Ignacius fremontensis and some individuals of I. frugivorus were excluded from this study (as opposed to their inclusion in the study presented in Chapter 2 of this dissertation) due to their samples being collected from outside of the Bighorn Basin. The species included in this lineage are I. frugivorus, P. pagei, P. praecox, P. fortior, and P. citatus. Fig. 2.1 from Chapter 2 has been modified to highlight the particular lineage of interest to this study and is shown in

Fig. 3.1.

The Data

Maximum length and maximum width measurements of the P4, M1, M2, and M3 teeth, as well as P4 height and protoconid height of 496 individuals were obtained from the primary literature. Tooth measurement data for 487 individuals of I. graybullianus, P. praecox, P. fortior and P. citatus were provided by Mary Silcox, University of Toronto who reported in Silcox et al. (2008) that measurements were made to the nearest 0.05 mm using digital calipers and followed the guidelines provided by Bloch and Gingerich

(1998: fig. 1). I measured nine individuals of Ignacius frugivorus and 28 individuals of P. pagei that are housed in the University of Michigan Museum of Paleontology in the same

180 manner as that reported by Silcox (2008). Measurements of upper tooth positions or the anterior teeth of the lower dentition were excluded from the study due to small sample size.

Stratigraphy

The specimens included in this study have known locality information that includes a meter level within the southern or northern parts of the Bighorn Basin.

Sediment accumulation rates and maximum and minimum meter levels for middle

Paleocene to early Eocene North American Land Mammal Ages were provided to the authors by William Clyde and were based on works by several authors (Butler et al.

1981; Bown and Rose 1987; Bown et al. 1994b; Tauxe et al. 1994; Hamzi 2003;

Gradstein et al. 2012).

Geologic Age and Biohorizon Events

To estimate the relationships between MAT estimates from within the Bighorn Basin and tooth metrics, a geologic age for each individual had to be determined. The same methods reported in Chapter 2 were used here to derive age estimates. Meter level for each locality was provided in the dataset from Silcox et al. (2008). Meter level or locality information was indicated on the specimen tags that I measured at the University of

Michigan Museum of Paleontology. An individual’s geologic age was calculated using equation one.

!"#$%&#' )#*+*)%$ ,)# = *+.#!/ ,)# *0 1%*2*'# 1*3'.,45 (7,) −

!"#"$ &"'"& () &(*+&,#- (!)0&(1"2# &"'"& () 3,(4(5" 3(657+$- (!) : ! ; (1) 2"7,!"5#+#,(5 $+#" ( ) "#

181 The zonation of Biohorizon A and Biohorizon B was obtained from Schankler

(1980) and Chew (2009).

Data analysis

To address the hypotheses, I divided the interval into three period: an early period of warming (59.8 – 55.56 Ma), a middle period of cooling (55.55 – 54.38 Ma), and a late period of warming (54.37 -53.21 Ma). These periods were chosen without reference to changes in tooth metrics and individuals were binned in each period based on their geologic age even if this resulted in individuals of the same species being binned in different periods. I performed Shapiro-Wilk test of normality on each tooth metric for each period and differences between tooth metrics for each period was evaluated using a

Kruskal-Wallis H test.

For each period, patterns of tooth metrics throughout the lineage segment were compared to changes in MAT. I used Spearman’s Rho rank correlation tests to compare changes in tooth metrics to changes in MAT for the early warming, middle cooling, and late warming periods. I chose to use the Spearman’s Rho test because it is more appropriate when there is less certainty about the reliability of close ranks (Sokal and

Rohlf 1995). Mean Annual Temperature estimates were obtained from previous studies using leaf margin analysis in the Bighorn Basin throughout the late Paleocene and early

Eocene Wing et al. (1991, 2000, 2005).

Lastly, patterns of tooth metrics throughout the entire lineage were compared to changes in MAT. I used the non-parametric Spearman’s Rho rank correlation tests to compare changes in tooth metrics to changes in MAT. I also look at the evolutionary

182 changes that occurred in this lineage at a finer scale, the change in tooth metric size from an ancestor to a descendant population. For this approach, I use the OSUs established in

Chapter 2, Table 2.2, as ancestor and descendant units of this lineage (Table 3.1). I tested the relationships between each evolutionary step (between adjacent OSUs) and temperature by using a weighted least-squares regression (Bowerman and O’Connell

1990) of each tooth metric size increment against the changes in paleotemperature.

Lastly, I assigned each evolutionary step to one of the periods in accordance with the age of the descendant population and performed t-tests to evaluate whether there were general increases or decreases in tooth metric size in each period.

All statistical analyses were performed in RStudio v. 1.2.1335 (RStudio Team

2018).

3.3 Results

Descriptive statistics of log transformed measurements for all teeth for each period can be found in Table 3.2. Box plots for log transformed measurements for each period are provided in Fig. 3.6. The P4 height, and P4, M1, M2, and M3 length and width tooth metrics show that their largest average sizes occurred during the early and middle periods, while P4 protoconid height exhibited their largest average sizes during the early period (Table 3.2). However, largest average sizes were only significantly different from an adjacent period in some tooth metrics (see Fig. 3.6, and results from Kruskal Wallis H test in the following paragraph). Shapiro-Wilk tests of normality indicate that several tooth metrics in each period do not follow a normal distribution. These results are provided in Table 3.3.

183 Trajectories for P4 protoconid height and height and P4, M1, M2 and M3 length and width for the early, middle, and late period are shown in Figs. 3.3, 3.4, and 3.5, respectively. During the early period, species included I. frugivorus, P. pagei, and P. praecox. The P4 height, length and width, and M1 and M2 length tooth metrics appears to be increasing through time (Fig. 3.3). There is a larger shift between I. frugivorus and both Phenacolemur species in tooth metrics that have I. frugivorus samples available.

The width of M2 appears to have a decreasing trend; however, sample size for this tooth is smaller and this trend may be an artifact of small sample size (Fig. 3.3). The sample sizes for the M3 tooth metrics are also small and trends may not be reliably accounted for

(Fig 3.3). During the middle period, species included P. praecox and P. fortior. The P4 protoconid height and height tooth metrics show a decreasing trend through time, whereas P4 and M1 length and width show increasing trends through time (Fig 3.4). The

M2 and M3 tooth metrics do not show any clear trends and M3 has a small sample size

(Fig 3.4). During the latest period, P4 protoconid height and height, P4, M1, M2 and M3 length and width show increasing trends through time (Fig 3.5). Trends in width of all teeth are less apparent but there does appear to be a tendency towards larger width sizes

(Fig 3.5).

A Kruskal-Wallis H test was carried out to compare differences between each tooth metric for each period. I found significant differences in P4 length and width between the different periods, χ2(2) = 48.108, p < 0.001, χ2(2) = 60.108, p < 0.001, respectively. Dunn-Bonferroni post hoc tests showed that during the middle period P4 length and width were greater than during the early or late period (p < 0.001) and that

184 during the late period P4 length and width was less than during the early and middle periods (p < 0.001; Fig. 3.6). There was a statistically significant difference in P4 protoconid heights between the different periods, χ2(2) = 35.476, p < 0.001. Post hoc tests for P4 protoconid height showed that during the early period P4 protoconid height was greater than during both the middle and late periods (p < 0.001) but that P4 protoconid height was similar between the middle and late periods (p = 0.440; Fig. 3.3).

There was a significant difference in P4 heights between the different periods, χ2(2) =

17.651, p < 0.001. Dunn-Bonferroni post hoc tests for P4 height showed that P4 height was greater during the early period than during the late period (p < 0.001) but P4 height during the middle period was similar to P4 height during the early period (p = 0.144) and the late period (p = 0.190).

There was a significant difference in M1 lengths between the different periods,

χ2(2) = 19.661, p < 0.001. Post hoc tests show that M1 length was greater during the middle period than during the early period (p < 0.001) and the late period (p < 0.001) but that M1 length was similar during the early and late periods (p =1.00). There was a significant difference in M1 widths between the different periods, χ2(2) = 58.077, p <

0.001. Post hoc tests showed that M1 width was greater during the early and middle periods than during the late period (p < 0.001), but M1 width was similar during the early and middle periods (p = 0.059).

There was a significant difference in M2 lengths between the different periods,

χ2(2) = 13.605, p < 0.001. A post hoc test showed that M2 length was greater during the early and middle periods than during the late period (p < 0.001) but that during the early

185 and middle periods M2 lengths were similar (p = 0.234). There was a significant difference in M2 widths between the different periods, χ2(2) = 63.489, p < 0.001. Post hoc tests revealed that during the early and middle periods M2 widths were greater than during the late period (p < 0.001) but M2 widths were similar during the early and middle periods (p = 0.891).

There was a significant difference in M3 lengths between the different periods,

χ2(2) = 6.421, p < 0.05. However, post hoc tests showed that M3 lengths between the early and late periods (p = 0.154), the middle and late periods (p = 0.090), and the early and middle periods (p=1.00). There was a significant difference in M3 widths between the different periods, χ2(2) = 8.355, p < 0.05. Dunn-Bonferroni post hoc tests showed that M3 width during the middle period was greater than during the late period (p < 0.05) but similar in size during the early and middle periods (p = 0.599) and the early and late periods (p = 0.216).

The comparison of the changes with information on paleoclimate and Biohorizon

A and Biohorizon B for each period and the entire lineage is shown in Figs. 3.3, 3.4, 3.5, and 3.2, respectively. Visual appraisal of the leaf-margin paleotemperature curve plotted against the temporal records of tooth metrics for the early period of temperature warming reveals possible correlations between MAT and P4 protoconid height, height, and M1 and

M2 length. Spearman’s Rho correlation test supports my observation with a significant positive correlation found within the early interval between MAT and P4 protoconid height (&#= 0.415, p < 0.01), height (&#= 0.473, p <0.01), M1 length (&#= 0.708, p < 0.01) and M2 length (&#= 0.482, p <0.01, Table 3.4, Fig. 3.7).

186 Visually, the paleotemperature curve plotted against the temporal records of tooth metrics for the middle period of temperature cooling reveals possible correlations between P4 protoconid height, height, length and width. Spearman’s Rho correlation test supports my observation with a significant positive correlation found within the middle interval between MAT and P4 protoconid height (&#= 0.691, p < 0.01) and height (&#=

0.642, p <0.01), and significant negative correlations between MAT and P4 length (&#= -

0.319, p < 0.05) and width (&#= -0.519, p < 0.01, Table 3.4, Fig. 3.8).

The paleotemperature curves plotted against the temporal records of tooth metrics for the late period of temperature warming show possible correlations between P4 protoconid height, height, length and width, M1 length and width, and M2 and M3 length.

Spearman’s Rho correlation test supports most of my observations with a significant positive correlation found within the late interval between MAT and P4 protoconid height

(&#= 0.782, p < 0.01), height (&#= 0.765, p <0.01), length (&#= 0.571, p <0.01), and width

(&#= 0.431, p <0.01), M1 length (&#= 0.433, p <0.01) and width (&#= 0.247, p <0.05), and

M2 length (&#= 0.338, p <0.05, Table 3.4, Fig. 3.9).

Similarly, to the observations within individual periods, I also see a possible correlation between MAT and tooth metrics in the plots of the paleotemperature curves plotted against the temporal records of each tooth metric for the entire lineage.

Spearman’s Rho correlation test supports these observations with a significant positive correlation found between MAT and P4 protoconid height (&#= 0.314, p < 0.01), height

(&#= 0.606, p <0.01), length (&#= 0.381, p <0.01), and width (&#= 0.255, p <0.01), M1 length (&#= 0.526, p <0.01) and width (&#= 0.452, p <0.01), and M2 length (&#= 0.535, p

187 <0.01) and width (&#= 0.296, p <0.01), M3 length (&#= 0.303, p <0.01) and width (&#=

0.284, p <0.01, Table 3.4, Fig. 3.10).

Despite the significant correlations found between tooth metric size and MAT at the larger scale, evidence for a relationship between changes in tooth metric size and

MAT is not found at the scale of evolutionary steps between ancestor-descendant populations (Fig. 3.11). The relationships between tooth metric size and MAT are not statistically significant in any cases (P4 length: t = 0.262, p = 0.917; P4 width: t = -0.302, p = 0.768; P4 protoconid height: t = 1.423, p = 0.182; P4 height: t = 1.10, p = 0.295; M1 length: t = 1.294, p = 0.222; M1 width: t = 0.897, p = 0.389; M2 length: t = 1.048, p =

0.322; M2 width: t = 0.848, p = 0.418; M3 length: t = 1.753, p = 0.114; M3 width: t =

1.075, p = 0.311).

When changes between tooth metric size and MAT are divided into the three temporal windows, the mean change is positive for P4 length, width and height, M1, M2, and M3 length and width, and negative for P4 protoconid height during the early period.

During the middle period, the mean change is positive for P4 and M2 length and width, and M1 and M3 width and negative for P4 protoconid height and height, and M1 and M3 and length. During the late interval, the mean change is positive for P4 protoconid height and height and M3 length and negative for P4, M1, and M2 length and width, and M3 width. However, none of the mean changes during any period or for any tooth position are statistically different from zero (Table 3.5, Fig. 3.12).

188 3.4 Discussion

The fossil record from the Bighorn Basin reveals a picture over a 5.5 million year period, spanning the late Paleocene and early Eocene, in which the I. frugivorus – P. citatus lineage shows a general pattern of lower tooth metrics first increasing before

Biohorizon A, then decreasing until just before Biohorizon B, followed by a general tendency towards increasing sizes after Biohorizon B. The research presented in this study, documents trends in lower tooth metrics of the I. frugivorus – P. citatus lineage and their relationship to climate change in the Bighorn Basin during the late Paleocene and early Eocene.

Overall, I find evidence to suggest that there is a correlation between tooth metrics and MAT. When I look at the patterns of tooth metrics between individuals of species during each period, I find positive correlations in the early and late warming periods and both positive and negative correlations during the middle cooling period for several tooth metrics (Table 3.4, Figs. 3.7, 3.8, and 3.9). When I look at these same patterns over the entire lineage, I find significant positive correlations in all tooth metrics

(Table 3.4 and Fig. 3.10). Interestingly, the negative correlations during the cooling period were associated with P4 length and width, which both show significant positive correlations in the early and late warming periods. This continued increasing trend during each period, suggests that this tooth’s length and width metrics may have been under an evolutionary pressure to increase in size for reasons other than changing temperatures. It is likely that this increase in size was diet related as several other changes were occurring if the protoconid height and height of this tooth that I will explore below.

189 The inclusion of I. frugivorus and P. pagei in the early period sample and in the entire lineage likely influenced the results of the correlation analyses, as all of the I. frugivorus and some of the P. pagei specimens were outliers to the rest of the sample

(Fig. 3.6). However, I felt their inclusion in this study was important as they represented the start of the radiation in this sample. Other factors that may have influenced the results are smaller sample sizes for the individual periods. Small sample size likely influenced the non-significant outcomes of some tooth metrics for the analyses of individual periods.

In the future, if more fossils are collected and measured these analyses can be retested for significance. Regardless, I was able to identify significant correlations between tooth metrics and MAT throughout the individual periods and the entire lineage.

When I look at changes within OSUs and paleotemperature, the relationships between tooth metric size and MAT break down. This is likely the result of small sample size in many cases, particularly for P4 protoconid height and P4 crown height, and M1,

M2, and M3 length and width. Though significant correlations were not found for these teeth, there are still patterns that emerge that suggest a possible direct correlation between changing tooth metrics and MAT for each evolutionary step (Fig 3.11). For example, there are more positive changes in tooth metrics associated with positive changes in MAT for an evolutionary step and likewise more negative changes in tooth metric associate with negative changes in MAT (Fix 3.11). Though these relationships between tooth metrics and MAT are not supported when viewed at the level of changes between evolutionary steps (OSUs), I do see patterns emerging that may prove significant if sample sizes increase.

190 Given the overall trends I observed in the fossil record when compared to the paleotemperature curve, I was not surprised to find significant correlations. From the observations, I expected to find that many tooth metrics experienced systematic average increases during the warming periods and systematic average decreases during the cooling period. Surprisingly, I found the opposite for several tooth metrics (Table 3.5;

Figs. 3.6, 3.12). The early period most closely matched my expectation with all tooth metrics having experienced increases, with the exception of P4 protoconid height. The middle and late periods departed from my expectation by showing a mixture of increases and decreases.

During the early period, the overall mean change that I observed in P4 protoconid height, measured relative to the talonid, is negative. However, this negative change was driven by the large decrease in protoconid height from I. frugivorus to P. pagei at the very first evolutionary transition in the lineage. At the same time that the protoconid height decreased between these two early species, the overall height of the P4 increased as well as the talonid. This is interesting because these tooth metrics are particularly important with respect to diet, as they are involved in the initial division and deformation of food during puncture-crushing (Seligsohn 1977). Given their importance to mastication and diet, the P4 protoconid height and height are arguably more sensitive to changing climates than the lengths and widths of the molars. I found P4 protoconid height and height had a significant positive correlation with MAT during both warming periods and the cooling period, while the lengths and widths of this tooth were on a sustained trajectory of increasing in size (Table 3.4; Figs 3.7, 3.8, 3.9). The early period included I.

191 frugivorus, P. pagei, and P. praecox and from I. frugivorus to P. pagei a shift from an omnivorous-frugivorous diet to a stricter omnivorous diet with less fruit intake occurred and was maintained in P. praecox. Temperatures reached as high as 19oC during the early period (Wing et al. 1991, 2000, 2005) and warmer temperatures could potentially increase the availability of food resources important to primates, including fruits and insects. An abundance and variety of food sources available could have been responsible for the shift to a more omnivorous diet and one that relied less on fruit, and thus resulted in higher crowned P4 teeth (López-Torrez et al. 2018). As I see later in the lineage, during the middle cooling period the P4 protoconid height and height began to decrease and there was a shift back to an omnivorous-frugivorous diet (López-Torrez et al. 2018). The increased area of the tooth at this point would have likely been more advantageous for masticating fruit like substances (Rosenberger and Kinzey 1976, Ungar 2015).

The irregularity of the average increases during the warming periods and average decreases during the cooling period, resulted in values that were often largest during the early warming and middle cooling periods and were often smallest during the late warming period (Table 3.5, figs. 3.6, 3,12). At first these results seemed to contradict my findings of positive correlations between most tooth metrics and MAT. Given the results from the correlation tests, one might expect to find tooth metrics to be largest in the early and late periods and smallest during the middle period. There are a couple of explanations that could explain these general patterns I see in average tooth metric size.

First, the early warming period is the longest of the three periods and most tooth metrics increase fairly consistently with increasing temperatures during this time. The middle

192 cooling period follows the long early period of warming and the transition from warm to cool happens fairly rapidly and is much shorter in duration than the previous period. It appears that in several teeth, the tooth metric size continued to increase for a time after the warming period ended, before starting to decrease (Fig. 3.2). If direct correlations between these tooth metrics and MAT are real, then this observation could be explained by a lag response of morphological characters to temperatures changing towards a different trajectory. Alternatively, decreases in tooth size could have been influenced by the introduction of species at Biohorizon A and may not have been a direct result of the climate cooling but instead the result of interspecies interactions. Several species introduced at Biohorizon A were of equal or greater size to Phenacolemur, including

Prolimnocyon nivalis, Arctodontomys, and Microsyops (all considered scansorial insectivores, Behrensmeyer and Turner 2013), and may have been competitors with

Phenacolemur. The presence of species of equal or greater size in the same area competing for similar resources may have influenced a shift towards smaller sizes and greater frugivory. This latter scenario would suggest that increasing sizes may not have been solely influenced by MAT during the early period and could explain both the continued trend of increasing sizes when temperature first began to drop before

Biohorizon A and the decreasing trend that occurred afterwards. If tooth size increases were not strongly influenced by MAT, then Cope’s Rule of increasing body sizes in evolving lineages (Cope 1887, 1896; Alroy 1998) may provide an alternative or additional explanation to the sustained increase in most tooth metrics during the early warming period and the very beginning of the middle cooling period.

193 This same logic could be applied to the smaller average sizes I see in the late warming period. Though the overall pattern is of an increasing trend in tooth metric size, there is a short time were tooth metrics continue to decrease directly following the change in temperature before Biohorizon B (Fig 3.2). If I assume that the significant correlations between temperature and tooth metrics are real, then the continued decrease I see in most tooth metrics (except for P4 protoconid height; Fig. 3.2) directly after temperatures begin to warm again may also represent a brief lag in the response of these morphological characters to changing temperatures. Similar to the scenario described above, Biohorizon

B occurred just after temperatures shifted back onto an increasing trend. Several new species were introduced into the Bighorn Basin at Biohorizon B, including similarly sized primate species of Absarokius (scansorial insectivore; Behrensmeyer and Turner 2013) and Steinius (scansorial insectivore-faunivore, Strait 2001), which potentially introduced new competitors for food resources. The introduction of similarly sized species with more specialized diets may have influenced the transition towards a more generalized omnivorous diet and smaller tooth sizes. This scenario would suggest that tooth metric size was not solely influenced by MAT and perhaps explains both the continued trend of decreasing sizes when temperature first began to drop before Biohorizon A and the increasing trend that occurred thereafter.

The results suggest that MAT played a role in the evolution of the I. frugivorus –

P. citatus lineage. Though it may be impossible to discern the relative contributions of

MAT and the biohorizon events towards tooth metric changes in this lineage, I do find compelling evidence that suggests there was a relationship between tooth metrics of the

194 lower dentition and MAT. Given that my findings support a scenario of increasing tooth metric sizes during intervals of climate warming and decreasing tooth metric sizes during intervals of climate cooling, I cannot reject hypothesis one or two.

3.5 Conclusions

In the Bighorn Basin the I. frugivorus – P. citatus lineage show patterns of increasing and decreasing size trends that reflect similar changes shown in paleotemperature proxies. During periods of warming, the majority of lower posterior tooth metrics show significant direct relationships with temperature. During the cooling period, P4 protoconid height and crown height have a significant direct relationship with temperature and P4 length and width have a significant inverse relationship with temperature. This inverse relationship with temperature during the cooling period suggests that the P4 was under a stronger selective pressure than that created by changing temperatures to increase in size. The inverse relationships during the cooling period are muted when relationships are considered over the entire lineage and instead all tooth metrics show significant direct relationships with MAT over the entire lineage. This highlights the important insights that can be gained by analyzing trends during periods of cooling, warming, or no change separately.

At this time, sample sizes are too low to be able to resolve any significant relationships between changing tooth metrics and changing temperatures between evolutionary steps (OSUs). However, I was able to see some patterns emerging that appear to reflect the patterns I saw at larger scales.

195 3.6 Figures

* jepseni P. P. citatus Ln p4 length P. willwoodensis 50.3 intermediates 51.3 Wa 7

52.3 P. fortior -

53.3 Wa 6

Wa 5 P. simsoni P. fortior 54.3 I. graybullianus Biohorizon B H2 Wa 4 P. praecox ETM2 P. praecox Biohorizon A 55.3 Wa 3 Biohorizon B Wa 2 Wa 0-1 * P. pagei 56.3 Cf 3 I. clarkforkensis Cf 2 Anagenesis Ma 57.3 Cf 1 * Budding cladogenesis P. archus

Ti 6 I. frugivorus Dietary shift MAT 58.3 Ti 5 Biohorizon A Phenacolemur Taxa excluded from study due Ti 4 * to lack of data, or sample from the 59.3 Ti 3 Bighorn Basin

Ti 2 I. fremontensis

60.3 Ti 1 Omnivore

61.3 To 3 PETM Omnivore - frugivore To 2 62.3 Ignacius Omnivore - insectivore 63.3 To 1 Insectivore - omnivore Fig. 3.1 Temporal ranges of North American species of Ignacius and Phenacolemur. Proposed relationships between species included in this study are indicated by arrows. Patterns indicate dietary niches (López-Torres et al. 2018).

196 B A B A ) C o MAT ( MAT 54.8 Ma and Biohorizon Biohorizon and Ma 54.8

– B A B A lineage. lineage. Also plotted are the Mean Annual

) C o MAT ( MAT Phenacolemur citatus Phenacolemur Phenacolemur fortior Phenacolemur praecox Phenacolemur pagei Phenacolemur frugivorus Ignacius X O + Phenacolemur citatus Phenacolemur

– B A B A B A Ignacius frugivorus Ignacius ) C o MAT ( MAT t al. (1999, 2000, 2005). Biohorizon A spans the time period between 55.1 55.1 between period time the spans A Biohorizon 2005). 2000, (1999, al. t

54.0 Ma. 54.0 Ma.

– B A B A B A ) C o MAT ( MAT Scatterplots Scatterplots of log tooth transformed metrics for the

Fig. 3.2 e Wing from obtained curves (MAT) Temperature 54.2 between period time the B spans 197

and ) C o MAT ( MAT acolemur acolemur pagei, d are the Mean Annual Temperature (MAT) Phenacolemur Phenacolemur praecox, Phen ) C o MAT ( MAT Phenacolemur praecox Phenacolemur pagei Phenacolemur frugivorus Ignacius X + ) C o MAT ( MAT ) C o

. MAT ( MAT erplots erplots of log transformed tooth metrics for the early period of climate warming. Also plotte Scatt

Fig. 3.3 curves obtained from Wing et al. (1999, 2000, 2005). Species present during this frugivorus Ignacius time period are 198 . A A (C) o MAT MAT Phenacolemur fortior Phenacolemur

and

A A Phenacolemur Phenacolemur praecox ) C o MAT ( MAT Phenacolemur fortior Phenacolemur praecox Phenacolemur + A A A

) C o MAT ( MAT 54.8 Ma. 54.8

– rics for the middle period of climate cooling. Also plotted are the Mean Annual Temperature (MAT) (MAT) Temperature Annual the Mean are plotted cooling. Also climate of period middle the for rics A A A ) C o pans the time period between 55.1 55.1 between period time the pans MAT ( MAT Scatterplots of log transformed tooth met tooth transformed log of Scatterplots Fig. 3.4 3.4 Fig. curves obtained from Wing et al. (1999, 2000, 2005). Species present during this time period are s A Biohorizon

199 B B ature ature (MAT) ) C o MAT ( MAT . Biohorizon B the spans time B B ) C o Phenacolemur citatus Phenacolemur MAT ( MAT Phenacolemur citatus Phenacolemur O B B B esent during esent this during time period are ) C o MAT ( MAT B B B

) 54.0 Ma. 54.0 Ma.

C o – m m Wing et al. (1999, 2000, 2005). pr Species MAT ( MAT Scatterplots Scatterplots of log tooth metrics transformed for the late period of climate warming. are Also plotted the Annual Mean Temper

Fig. Fig. 3.5 curves fro obtained 54.2 period between 200 d d with

s. s. Orange box plots represents periods associate Box Box plots of log transformed tooth metrics for the early, middle, and late period Fig. 3.6 cooling. climate with associated period the plot represents box blue the and warming climate

201

ius for the early period of climate warming. warming. climate of period early the for ius 55.56 55.56 Ma

– Early 59.8 Climate of Warming: Period Scatterplots of log tooth metrics versus mean annual temperature (MAT) measured in degrees Cels degrees in measured (MAT) temperature annual mean versus metrics tooth log of Scatterplots

3.7

Fig. coefficient. regression the of error the standard represent line the around bands grey and added line Regression 202

54.38 Ma 54.38

– Middle Middle Period 55.55 Climate of Cooling: versus mean annual temperature (MAT) measured in degrees Celsius for the middle period of climate cooling. cooling. climate of period middle the for Celsius degrees in measured (MAT) temperature annual mean versus Scatterplots of log tooth metrics metrics tooth log of Scatterplots 8 3.

Fig. coefficient. regression the of error the standard represent line the around bands grey and added line Regression

203 mate warming. warming. mate

53.21 53.21

– ession coefficient. coefficient. ession 4.37 4.37 represent the standard error of the regr the of error the standard represent

Late Period Late 5 Climate of Warming: Scatterplots of log tooth metrics versus mean annual temperature (MAT) measured in degrees Celsius for the late period of cli of period late the for Celsius degrees in measured (MAT) temperature annual mean versus metrics tooth log of Scatterplots 9 3.

Fig. line the around bands grey and added line Regression 204 gression line gression

53.21 53.21

– Entire 59.8 Lineage: andard error of the regression coefficient. coefficient. the regression of error andard Scatterplots of log tooth metrics versus mean annual temperature (MAT) measured in degrees Celsius for the entire lineage. Re lineage. entire the for Celsius degrees in measured (MAT) temperature annual mean versus metrics tooth log of Scatterplots 10 10 3.

Fig. the st line represent the around bands grey and added 205

MAT and MAT dotted and s and periods. Dotted vertical lines represent no change in in change no lines represent vertical s periods. and Dotted

tterplot tterplot of evolutionary size increments versus Mean Annual Temperature (MAT), measured in degrees Celsius. Circles represent Sca 11 3.

Fig. all across specie population ancestral a changes an to from descendant metric size. tooth in change no represent lines horizontal 206 hree hree respect respect to the age of the length length and width with

3 , , and M 2 tooth tooth metric size. Vertical dotted lines delimited the t , M 1 , M 4 protoconid protoconid height, height, P

4

range range circles evolutionary steps represent associated with climate warming and blue circles evolutionary represent Evolutionary Evolutionary changes in tooth metrics (P 12 12 3.

.

Fig descendant (OSU). population O steps associated with climate warming. Horizontal dashed lines indicate no change in left). to right decreases time (*note periods 207 3.7 Tables

Table 3.1

Number of Individual Species OSU code Mean age (Ma) specimens (n)

P. citatus Pcit-5 32 53.41

P. citatus Pcit-4 40 53.59

P. citatus Pcit-3 25 53.72

P. citatus Pcit-2 23 53.89

P. citatus Pcit-1 42 54.06

P. fortior Pfor-2 16 54.54

P. fortior Pfor-1 32 54.94

P. praecox Ppra-4 48 55.42

P. praecox Ppra-3 32 55.69

P. praecox Ppra-2 61 55.74

P. praecox Ppra-1 49 55.86

P. pagei Ppag-2 13 56.47

P. pagei Ppag-1 15 57.64

I. frugivorus Ifrug-2 9 58.70

Table 3.1 List of Operational Stratigraphic Units (OSUs) and their sample sizes and mean estimated age for each species of Ignacius and Phenacolemur included in the study.

208 Table 3.2 Tooth metric Early period Middle Late period ln ln ln Tooth metric s s2 s s2 s s2 mean mean mean

P4 length 1.11 0.138 0.0190 1.20 0.0702 0.00492 1.04 0.104 0.0108

P4 width 0.72 0.141 0.0198 0.84 0.0837 0.00700 0.65 0.0943 0.00889

P4 protoconid height 0.45 0.154 0.0238 0.10 0.264 0.0699 0.23 0.164 0.0271

P4 height 1.15 0.174 0.0303 1.09 0.101 0.0102 1.04 0.113 0.0127

M1 length 0.93 0.143 0.0204 1.03 0.0609 0.00371 0.96 0.0555 0.00308

M1 width 0.81 0.133 0.0176 0.83 0.0458 0.00209 0.70 0.0555 0.00309

M2 length 0.93 0.176 0.0308 1.02 0.0731 0.00535 0.95 0.0476 0.00226

M2 width 0.88 0.199 0.0395 0.84 0.0460 0.00212 0.72 0.0494 0.00244

M3 length 1.29 0.0805 0.00648 1.32 0.0624 0.00390 1.27 0.0611 0.00373

M3 width 0.70 0.0673 0.00452 0.74 0.0318 0.00101 0.67 0.0643 0.00414

Table 3.2 Descriptive statistics for lengths and widths of individual teeth and protoconid heights and height of the P4 teeth for the early, middle, and late periods. Means and standard deviations are measured in ln mm. Abbreviations: s, standard deviation; s2, sample variance

Table 3.3 Earliest period Middle period Latest period Entire lineage Tooth metric Shapiro-Wilk Shapiro-Wilk Shapiro-Wilk Shapiro-Wilk result result result result

P4 length W(48)=0.841** W(37)=0.964 W(65)=0.949* W(152)=0.923**

P4 width W(49)=0.820** W(37)=0.938* W(66)=0.978 W(154)=0.959**

P4 protoconid height W(39)=0.966 W(26)=0.849** W(34)=0.0.927* W(162)=0.969*

P4 height W(40)=0.879** W(26)=0.958 W(34)=0.945 W(102)=0.971*

M1 length W(41)=0.775** W(30)=0.944 W(59)=0.968 W(132)=0.832**

M1 width W(43)=0.845** W(28)=0.901* W(63)=0.958* W(136)=0.892**

M2 length W(44)=0.803** W(21)=0.955 W(58)=0.937* W(124)=0.805**

M2 width W(46)=0.671** W(19)=0.958 W(57)=0.964 W(123)=0.695**

M3 length W(22)=0.831** W(10)=0.874 W(30)=0.970 W(63)=0.953*

M3 width W(22)=0.826** W(9)=0.814* W(33)= 0.917* W(66)=0.898** Table 3.3 Results from a Shapiro-Wilk test for each tooth metric for the early, middle, and late periods and the entire lineage. Significant results are indicated by asterisks at P<0.05 (*) and P<0.01 (**).

209 Table 3.4 Early period Middle period Late period Entire lineage Tooth metric 4) | n 4) | n 4) | n 4) | n P4 length MAT 0.210 | 49 -0.319* | 38 0.571** | 66 0.381** | 153

P4 width MAT 0.0483 | 50 -0.519** | 38 0.431** | 67 0.255** | 155

P4 protoconid height MAT 0.415** | 40 0.691** | 27 0.782** | 35 0.314** | 163

P4 height MAT 0.473** | 41 0.642** | 27 0.765** | 35 0.606** | 103

M1 length MAT 0.708** | 42 0.146 | 31 0.433** | 60 0.526** | 133

M1 width MAT 0.285 | 44 -0.0323 | 29 0.247* | 64 0.452** | 137

M2 length MAT 0.482** | 45 0.225 | 22 0.338* | 58 0.535** | 125

M2 width MAT -0.221 | 47 0.102 | 20 0.191 | 57 0.296** | 124

M3 length MAT 0.223 | 22 0.101 | 11 0.528 | 31 0.303* | 64

M3 width MAT 0.205 | 23 0.140 | 10 0.324 | 34 0.284* | 67

Table 3.4 Results from a Spearman’s Rho (4)) correlation test for each tooth metric and mean annual temperature (MAT) for the early, middle, and late periods and the entire lineage. Values listed to the left of bars are correlation coefficients, 4) and to the right of bars are sample sizes for each test. Significant results are indicated by asterisks at P≤0.05 (*) and P≤.01 (**). Abbreviations: n, sample size

Table 3.5 Early period Middle period Late period Tooth metric mean ∆ | t | p mean ∆ | t | p mean ∆ | t | p

P4 length 0.104 | 1.04 | 0.359 0.0252 | 1.15 | 0.369 -0.0109 | -0.179 | 0.867

P4 width 0.112 | 0.871 | 0.433 0.0345 | 0.866 | 0.478 -0.0278 | 0.866 | 0.478

P4 protoconid height -0.0570 | -0.511 | 0.637 -0. 214 | -1.65 | 0.239 0.110 | 2.09 | 0.105

P4 height 0.140 | 1.26 | 0.275 -0.0740 | -1.30 | 0.324 0.0318 | 0.599 | 0.581

M1 length 0.0709 | 2.11 | 0.103 -0.00712 | -0.390 | 0.734 -0.0111 | -0.0111 | 0.992

M1 width 0.0524 | 1.33 | 0.254 0.00537 | 0.138 | 0.903 -0.0112 | -0.377 | 0.725

M2 length 0.0314 | 0.386 | 0.737 0.0199 | 0.427 | 0.711 -0.00225 | -0.143 | 0.893

M2 width 0.0406 | 1.02 | 0.416 0.0115 | 0.566 | 0.629 -0.0140 | -0.552 | 0.610

M3 length 0.0794 | 1.26 | 0.335 -0.00749 | -0.252 | 0.825 0.00872 | 0.336 | 0.754

M3 width 0.0672 | 1.08 | 0.394 0.00641 | 0.476 | 0.681 -0.00976 | -0.314 | 0.769 Table 3.5 Body size changes during the early, middle, and late periods.

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Chapter 4. Conclusions

4.1 Conclusions

This dissertation explores the radiation of Primates during the Paleogene, through two case studies that address questions surrounding the general patterns, or modes, of dental evolution, evolutionary rates, and the potential influence of abiotic and biotic drivers.

In Chapter 1, I found that as the Tetonius – Pseudoteonius lineage evolved, correlations between P3 and the molars diminished, whereas correlations between P4 and the molars increased. I found evidence of varying degrees of stabilizing selection in the lengths and widths of all cheek teeth and evidence of neutral evolution in the width of P4.

My results support a trend towards P4 becoming integrated into the molar morphogenetic field, and demonstrates that morphological rates of evolution, and consequently the degree of selective pressures, vary through time and between teeth.

The second and third chapters of this dissertation focus on the radiation of the family Paromomyidae during the late Paleocene and early Eocene. Two paromomyid genera Ignacius and Phenacolemur, provide a series of long-lived lineages that experienced episodes of biotic turnover and dietary shifts. Several species level transitions occurred, including an evolutionary transition linking the two genera.

219 The second chapter provides an exploration of the evolutionary modes and rates that produced the observed changes to lower dental morphology of the Ignacius and

Phenacolemur lineages, and the potential influence of the biotic turnover events. The paromomyid radiation can be explained by several models; however, a random walk was the dominant evolutionary model, followed by an Ornstein-Uhlenbeck process and strict stasis. Often, significant differences in tooth metrics between species can be explained by neutral evolutionary processes. Dietary shifts did not always produce directional modes of evolution and stasis was not always the best fit model when no dietary shift occurred.

The third chapter focuses on the longest continuous lineage of Phenacolemur and

Ignacius species from the Bighorn Basin, the Ignacius frugivorus – Phenacolemur citatus lineage. The goal of this chapter was to assess whether morphological changes in the dentition could be explained by changes in paleotemperature. I found a significant positive correlation with temperature when the entire lineage was analyzed. When the lineage was divided between species present only during the early warming period, the middle cooling period, and the late warming period, the data revealed positive correlations between tooth metrics and paleotemperature during both warming periods.

During the cooling period, P4 protoconid height and crown height had a significant positive correlation with temperature and P4 length and width had a significant negative correlation with temperature. This inverse relationship with temperature during the cooling period, suggests that the P4 was under a stronger selective pressure than that created by changing temperatures to increase in size. The inverse relationships during the cooling period are muted when relationships are considered over the entire lineage and

220 instead show significant positive correlations with MAT, thus highlighting the important insights that can be gained by analyzing trends during periods of cooling, warming, or no change separately from the entire lineage.

The dental evolution of euprimates and plesiadapiforms was complex. Lineages within these two groups show a diverse array of dental adaptations, some of which are observed to have made seemingly drastic changes while others appear to have changed little. One of the overarching themes of this dissertation is that seemingly large changes can occur by neutral evolutionary processes. Additionally, stasis and an Ornstein-

Uhlenbeck process are commonly observed evolutionary modes in fossil euprimates and plesiadapiforms.

The biohorizon events of the early Eocene played a clear role in the evolution of euprimates and plesiadapiforms from the Bighorn Basin. My study of the Tetonius –

Pseudoteonius lineage shows that Biohorizon A was associated with a release of stabilizing selection, which allowed significant morphological changes to occur. I also show that the diminishing correlations between the P3 and the molars as the lineage progressed, may have been associated with Biohorizon A. The Ignacius and

Phenacolemur lineages that I explore in Chapters 2 and 3, do not reveal any clear indication that evolutionary mode was influenced by the biohorizon events. In both the euprimate and plesiadapiform case studies, there is evidence supporting relationships between changes in paleotemperature and tooth metrics. These findings provide compelling evidence that paleotemperature was an important factor in shaping primate dentitions.

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248 Appendix A: Locality Information for Each Lineage Segment of the Tetonius –

Pseudotetonius Lineage

Table A.1

Meter Approximate age of OTU Mean OTU Basin Included localities level locality Age (my)

A Big Horn 64 V-73016b 55.71 55.52

Big Horn 97 V-73020a 55.57

Big Horn 110 Y-343 55.51

Big Horn 119 V-73055, V-73084 55.47

Clark’s 240 UM SC-87, UM SC-213 55.41 Fork

Big Horn 140 Y-104 55.37

Big Horn 150 Y-109 55.33

B Big Horn 160 Unknown 55.28 55.20

Clark’s 320 UM SC-225 55.28 Fork Clark’s 330 UM SC-34, UM SC-192 55.26 Fork

Big Horn 170 Y-389 55.24

D-1224, D-1225, V-73125, Y-82, Big Horn 180 55.19 Y-87, Y-144, Y-363, D-1816

Big Horn 190 Y-214, Y-363 55.15

Clark’s 395 UM SC-114 55.15 Fork Clark’s C 450 UM SC-64, D-1077 55.06 54.89 Fork

Big Horn 212 Unknown 55.05

249 Table A.1 Continued

Clark’s 485 UM SC-111 55.00 Fork Clark’s 500 UM SC-112 54.97 Fork

Big Horn 240 Unknown 54.92

Big Horn 250 Unknown 54.88

Clark’s UM SC-113, UM SC-255, UM 530 54.85 Fork SC-148

Big Horn 262 D-1297 54.83

Big Horn 264 Unknown 54.82

Big Horn 270 Y-286 54.79

Clark’s 545 UM SC-147 54.78 Fork

Big Horn 282 Unknown 54.74

V-73012, Y-296, Y-297, Y-350, D Big Horn 290 54.70 54.56 Y-287 Clark’s UM SC-299, UM SC-253, UM 575 54.65 Fork SC-265

Big Horn 336 Y-157, D-1288 54.49

Big Horn 344 D-1241, D-1201 54.46

Big Horn 348 Unknown 54.44

Big Horn 370 D-1635, Y-277, Y-334 54.34

Big Horn 374 Unknown 54.32

Table A.1 Locality information for each lineage segment. Lineage segments are labeled according to OTUs A, B, C, and D. Locality designation number, basin, meter level, and the approximate age calculated for each locality is shown. Calculated mean age for each OTU is also included.

250 Appendix B: Sample size, Sample Means and Variances, and Sample Ages for Ignacius

and Phenacolemur Lineage Segments

Table B.1 Sample Sample size Sample Sample age Tooth Species OSU code variances (n) mean (mm) (Ma) (mm2)

P4 length P. willwoodensis Pwil-1 4 2.16 0.00567 53.69

P. simonsi Psim-4 3 1.87 0.0233 54.73

P. simonsi Psim-3 4 1.80 0.00667 55.75

P. simonsi Psim-2 5 1.86 0.0480 55.83

P. simonsi Psim-1 3 1.87 0.00333 55.92

P. citatus Pcit-5 14 3.21 0.0349 53.41

P. citatus Pcit-4 16 2.92 0.0643 53.59

P. citatus Pcit-3 10 2.58 0.0268 53.72

P. citatus Pcit-2 9 2.72 0.0394 53.89

P. citatus Pcit-1 17 2.72 0.0474 54.06

P. fortior Pfor-2 8 3.39 0.0727 54.54

P. fortior Pfor-1 17 3.42 0.0653 54.94

P. praecox Ppra-4 15 3.21 0.0194 55.42

P. praecox Ppra-3 5 3.14 0.0268 55.69

P. praecox Ppra-2 7 3.14 0.0662 55.74

P. praecox Ppra-1 12 3.22 0.0524 55.86

P. pagei Ppag-2 10 2.92 0.0744 56.47

P. pagei Ppag-1 11 3.08 0.146 57.64

251 Table B.1 Continued I. graybullianus Ig-2 3 1.73 0.0133 55.56

I. graybullianus Ig-1 5 1.82 0.0858 56.11

I. frugivorus Ifrug-2 2 1.87 0.0098 58.70

I. frugivorus Ifrug-1 10 1.69 0.0338 59.78

I. fremontensis Ifrem-1 2 1.3 0.000 61.3

P4 width P. willwoodensis Pwil-1 4 1.46 0.00229 53.69

P. simonsi Psim-4 3 1.37 0.0333 54.73

P. simonsi Psim-3 4 1.23 0.00250 55.75

P. simonsi Psim-2 5 1.31 0.0155 55.83

P. simonsi Psim-1 3 1.25 0.00250 55.92

P. citatus Pcit-5 15 2.06 0.0160 53.41

P. citatus Pcit-4 17 1.94 0.0593 53.59

P. citatus Pcit-3 10 1.77 0.00956 53.72

P. citatus Pcit-2 8 1.89 0.0117 53.89

P. citatus Pcit-1 17 1.87 0.0187 54.06

P. fortior Pfor-2 8 2.36 0.0377 54.54

P. fortior Pfor-1 17 2.42 0.0272 54.94

P. praecox Ppra-4 15 2.16 0.00981 55.42

P. praecox Ppra-3 5 2.13 0.0245 55.69

P. praecox Ppra-2 8 2.09 0.00460 55.74

P. praecox Ppra-1 12 2.10 0.0388 55.86

P. pagei Ppag-2 10 1.96 0.0158 56.47

P. pagei Ppag-1 11 2.25 0.0566 57.64

I. graybullianus Ig-2 3 1.53 0.0233 55.56

I. graybullianus Ig-1 5 1.49 0.0718 56.11

I. frugivorus Ifrug-2 2 1.22 0.0072 58.70

252 Table B.1 Continued

I. frugivorus Ifrug-1 10 1.11 0.00646 59.78

I. fremontensis Ifrem-1 2 0.9 0.000 61.3

P4 protoconid P. willwoodensis Pwil-1 0 - - 53.69 height

P. simonsi Psim-4 2 1.15 0.00500 54.73

P. simonsi Psim-3 4 1.00 0.00500 55.75

P. simonsi Psim-2 5 1.00 0.00375 55.83

P. simonsi Psim-1 3 1.07 0.0133 55.92

P. citatus Pcit-5 5 1.56 0.0530 53.41

P. citatus Pcit-4 5 1.38 0.042 53.59

P. citatus Pcit-3 8 1.29 0.0213 53.72

P. citatus Pcit-2 4 1.38 0.0158 53.89

P. citatus Pcit-1 13 1.08 0.00359 54.06

P. fortior Pfor-2 6 0.90 0.000 54.54

P. fortior Pfor-1 12 0.95 0.0118 54.94

P. praecox Ppra-4 10 1.53 0.0312 55.42

P. praecox Ppra-3 4 1.71 0.0106 55.69

P. praecox Ppra-2 7 1.71 0.0148 55.74

P. praecox Ppra-1 8 1.65 0.0371 55.86

P. pagei Ppag-2 10 1.46 0.0272 56.47

P. pagei Ppag-1 8 1.39 0.0168 57.64

I. graybullianus Ig-2 2 0.80 0.000 55.56

I. graybullianus Ig-1 3 0.73 0.0108 56.11

I. frugivorus Ifrug-2 2 0.815 0.0181 58.70

I. frugivorus Ifrug-1 10 0.946 0.0313 59.78

I. fremontensis Ifrem-1 0 - - 61.3

253 Table B.1 Continued

P4 height P. willwoodensis Pwil-1 0 - - 53.69

P. simonsi Psim-4 2 2.20 0.0200 54.73

P. simonsi Psim-3 4 1.94 0.0123 55.75

P. simonsi Psim-2 5 1.98 0.00825 55.83

P. simonsi Psim-1 3 1.97 0.0433 55.92

P. citatus Pcit-5 5 3.38 0.057 53.41

P. citatus Pcit-4 5 2.96 0.058 53.59

P. citatus Pcit-3 8 2.79 0.00500 53.72

P. citatus Pcit-2 4 2.98 0.0292 53.89

P. citatus Pcit-1 13 2.56 0.0176 54.06

P. fortior Pfor-2 6 2.88 0.0257 54.54

P. fortior Pfor-1 12 2.80 0.0432 54.94

P. praecox Ppra-4 10 3.32 0.0267 55.42

P. praecox Ppra-3 4 3.60 0.0133 55.69

P. praecox Ppra-2 7 3.50 0.0267 55.74

P. praecox Ppra-1 8 3.35 0.100 55.86

P. pagei Ppag-2 10 3.04 0.134 56.47

P. pagei Ppag-1 8 3.20 0.217 57.64

I. graybullianus Ig-2 2 1.93 0.00125 55.56

I. graybullianus Ig-1 3 1.72 0.0158 56.11

I. frugivorus Ifrug-2 2 1.79 0.00245 58.70

I. frugivorus Ifrug-1 10 1.58 0.0536 59.78

I. fremontensis Ifrem-1 0 - - 61.3

M1 length P. willwoodensis Pwil-1 5 2.24 0.0130 53.69

P. simonsi Psim-4 5 2.03 0.00450 54.73

P. simonsi Psim-3 6 2.03 0.00375 55.75

254 Table B.1 Continued P. simonsi Psim-2 4 2.01 0.0440 55.83

P. simonsi Psim-1 10 1.99 0.0445 55.92

P. citatus Pcit-5 10 2.73 0.0196 53.41

P. citatus Pcit-4 17 2.63 0.0163 53.59

P. citatus Pcit-3 13 2.60 0.0185 53.72

P. citatus Pcit-2 12 2.57 0.0138 53.89

P. citatus Pcit-1 8 2.49 0.0220 54.06

P. fortior Pfor-2 7 2.73 0.0257 54.54

P. fortior Pfor-1 13 2.84 0.0292 54.94

P. praecox Ppra-4 16 2.77 0.0240 55.42

P. praecox Ppra-3 4 2.79 0.000625 55.69

P. praecox Ppra-2 6 2.78 0.00267 55.74

P. praecox Ppra-1 12 2.74 0.0158 55.86

P. pagei Ppag-2 7 2.37 0.0127 56.47

P. pagei Ppag-1 5 2.30 0.0413 57.64

I. graybullianus Ig-2 7 2.35 0.0300 55.56

I. graybullianus Ig-1 7 2.46 0.0337 56.11

I. frugivorus Ifrug-2 3 1.96 0.00503 58.70

I. frugivorus Ifrug-1 20 2.11 0.0166 59.78

I. fremontensis Ifrem-1 3 1.63 0.0133 61.3

M1 width P. willwoodensis Pwil-1 5 1.68 0.00700 53.69

P. simonsi Psim-4 5 1.54 0.00300 54.73

P. simonsi Psim-3 6 1.48 0.00775 55.75

P. simonsi Psim-2 4 1.49 0.0156 55.83

P. simonsi Psim-1 9 1.51 0.0297 55.92

P. citatus Pcit-5 11 2.11 0.0100 53.41

255 Table B.1 Continued

P. citatus Pcit-4 18 2.02 0.0112 53.59

P. citatus Pcit-3 15 1.96 0.00852 53.72

P. citatus Pcit-2 12 2.06 0.00915 53.89

P. citatus Pcit-1 8 2.01 0.016 54.06

P. fortior Pfor-2 7 2.24 0.0106 54.54

P. fortior Pfor-1 11 2.40 0.00100 54.94

P. praecox Ppra-4 16 2.27 0.00996 55.42

P. praecox Ppra-3 5 2.20 0.0300 55.69

P. praecox Ppra-2 6 2.28 0.00867 55.74

P. praecox Ppra-1 13 2.28 0.00867 55.86

P. pagei Ppag-2 7 2.00 0.0246 56.47

P. pagei Ppag-1 5 2.01 0.0201 57.64

I. graybullianus Ig-2 7 1.96 0.0355 55.56

I. graybullianus Ig-1 8 2.14 0.0417 56.11

I. frugivorus Ifrug-2 3 1.69 0.00223 58.70

I. frugivorus Ifrug-1 20 1.57 0.00815 59.78

I. fremontensis Ifrem-1 3 1.30 0.0300 61.3

M2 length P. willwoodensis Pwil-1 5 2.23 0.0120 53.69

P. simonsi Psim-4 4 1.95 0.00333 54.73

P. simonsi Psim-3 3 1.87 0.0233 55.75

P. simonsi Psim-2 5 2.04 0.0518 55.83

P. simonsi Psim-1 6 1.88 0.0678 55.92

P. citatus Pcit-5 10 2.65 0.00722 53.41

P. citatus Pcit-4 16 2.61 0.0255 53.59

P. citatus Pcit-3 12 2.53 0.00970 53.72

P. citatus Pcit-2 13 2.58 0.0160 53.89

256 Table B.1 Continued

P. citatus Pcit-1 7 2.54 0.00226 54.06

P. fortior Pfor-2 5 2.68 0.0470 54.54

P. fortior Pfor-1 9 2.84 0.0474 54.94

P. praecox Ppra-4 13 2.80 0.0273 55.42

P. praecox Ppra-3 4 2.53 0.00250 55.69

P. praecox Ppra-2 17 2.79 0.0359 55.74

P. praecox Ppra-1 9 2.76 0.0228 55.86

P. pagei Ppag-2 3 2.30 0.0357 56.47

P. pagei Ppag-1 0 - - 57.64

I. graybullianus Ig-2 12 2.38 0.0166 55.56

I. graybullianus Ig-1 4 2.49 0.00729 56.11

I. frugivorus Ifrug-2 7 2.14 0.0118 58.70

I. frugivorus Ifrug-1 20 2.00 0.0204 59.78

I. fremontensis Ifrem-1 3 1.53 0.0233 61.3

M2 width P. willwoodensis Pwil-1 5 1.64 0.00300 53.69

P. simonsi Psim-4 4 1.56 0.00229 54.73

P. simonsi Psim-3 3 1.43 0.00333 55.75

P. simonsi Psim-2 5 1.55 0.0300 55.83

P. simonsi Psim-1 5 1.47 0.0120 55.92

P. citatus Pcit-5 10 2.14 0.00725 53.41

P. citatus Pcit-4 15 2.04 0.00900 53.59

P. citatus Pcit-3 11 1.99 0.00591 53.72

P. citatus Pcit-2 13 2.05 0.0123 53.89

P. citatus Pcit-1 8 2.07 0.00853 54.06

P. fortior Pfor-2 5 2.29 0.0143 54.54

P. fortior Pfor-1 7 2.36 0.0120 54.94

257 Table B.1 Continued

P. praecox Ppra-4 13 2.28 0.00651 55.42

P. praecox Ppra-3 4 2.21 0.00396 55.69

P. praecox Ppra-2 18 2.24 0.00625 55.74

P. praecox Ppra-1 9 2.21 0.00778 55.86

P. pagei Ppag-2 3 1.96 0.00750 56.47

P. pagei Ppag-1 0 - - 57.64

I. graybullianus Ig-2 12 2.00 0.0170 55.56

I. graybullianus Ig-1 4 2.09 0.0106 56.11

I. frugivorus Ifrug-2 7 1.77 0.0102 58.70

I. frugivorus Ifrug-1 20 1.72 0.0199 59.78

I. fremontensis Ifrem-1 3 1.27 0.00333 61.3

M3 length P. willwoodensis Pwil-1 2 2.80 0.000 53.69

P. simonsi Psim-4 3 2.63 0.0233 54.73

P. simonsi Psim-3 4 2.60 0.0183 55.75

P. simonsi Psim-2 3 2.72 0.00583 55.83

P. simonsi Psim-1 4 2.48 0.0492 55.92

P. citatus Pcit-5 5 3.83 0.0295 53.41

P. citatus Pcit-4 11 3.53 0.0401 53.59

P. citatus Pcit-3 5 3.58 0.0108 53.72

P. citatus Pcit-2 4 3.5 0.0333 53.89

P. citatus Pcit-1 6 3.4 0.0400 54.06

P. fortior Pfor-2 3 3.67 0.0233 54.54

P. fortior Pfor-1 6 3.79 0.0884 54.94

P. praecox Ppra-4 3 3.60 0.0300 55.42

P. praecox Ppra-3 4 3.75 0.00300 55.69

P. praecox Ppra-2 9 3.74 0.0149 55.74

258 Table B.1 Continued

P. praecox Ppra-1 4 3.63 0.00917 55.86

P. pagei Ppag-2 2 2.96 0.00125 56.47

P. pagei Ppag-1 0 - - 57.64

I. graybullianus Ig-2 6 3.52 0.0447 55.56

I. graybullianus Ig-1 1 3.40 - 56.11

I. frugivorus Ifrug-2 1 2.64 - 58.70

I. frugivorus Ifrug-1 11 2.65 0.0273 59.78

I. fremontensis Ifrem-1 0 - - 61.3

M3 width P. willwoodensis Pwil-1 3 1.57 0.00333 53.69

P. simonsi Psim-4 3 1.52 0.000833 54.73

P. simonsi Psim-3 4 1.53 0.00917 55.75

P. simonsi Psim-2 4 1.60 0.0217 55.83

P. simonsi Psim-1 4 1.36 0.0256 55.92

P. citatus Pcit-5 6 2.00 0.00700 53.41

P. citatus Pcit-4 13 1.97 0.0123 53.59

P. citatus Pcit-3 5 1.96 0.00425 53.72

P. citatus Pcit-2 4 1.96 0.0190 53.89

P. citatus Pcit-1 6 1.85 0.0310 54.06

P. fortior Pfor-2 3 2.10 0.000 54.54

P. fortior Pfor-1 5 2.10 0.0100 54.94

P. praecox Ppra-4 3 2.03 0.0133 55.42

P. praecox Ppra-3 5 2.06 0.00800 55.69

P. praecox Ppra-2 9 2.05 0.00500 55.74

P. praecox Ppra-1 5 2.04 0.00800 55.86

P. pagei Ppag-2 2 1.69 0.00605 56.47

P. pagei Ppag-1 0 - - 57.64

259 Supplementary Table B.1 Continued

Table B.1 Continued

I. graybullianus Ig-2 7 1.89 0.0237 55.56

I. graybullianus Ig-1 1 1.80 - 56.11

I. frugivorus Ifrug-2 1 1.59 - 58.70

I. frugivorus Ifrug-1 11 1.41 0.0106 59.78

I. fremontensis Ifrem-1 0 - - 61.3

Table B.1 Sample size, sample means and variances, and sample ages for each tooth loci.

260

Appendix C: Estimating Body Weight and Generation Time in Fossil Primates

C.1 Introduction

The evolutionary rate analysis used in this study requires an approximation of generation time, which is impossible to obtain directly from fossil remains and must be estimated. Several authors have demonstrated that generation time, specifically age at first reproduction, in mammals is strongly correlated with body size (Western 1979;

Millar and Zammuto 1983; Calder 1984) and body size is highly correlated to tooth size in mammals (Pilbeam and Gould 1974; Gould 1975; Kay 1975; Gingerich 1977, 1981;

Gingerich et al. 1980, 1982; Kay and Simons 1980; Gingerich and Smith 1985; Conroy

1987; Copes and Schwartz 2010). Previous researchers have experimented with using

1 2 tooth length, width, or area of either the M1, M , M2, and M teeth to derive regression equations for estimating body mass in primates ( Kay 1975; Gingerich 1977, 1981;

Gingerich et al. 1980, 1982; Kay and Simons 1980; Gingerich and Smith 1985; Conroy

1987; Dagosto and Terranova 1992). Several of these authors have found especially high correlations between primate body size and M1 area (Gingerich 1981; Gingerich et al.

1980, 1982; Gingerich and Smith 1985; Conroy 1987). Fortunately, the sample of paromomyid M1 teeth is robust and can be used to estimate body mass. From an estimate of body mass, I then can estimate generation time.

261 Several authors have proposed predictive equations relating dental size and body size in fossil primates (Gingerich 1977, 1981; Gingerich et al. 1980, 1982; Kay and

Simons 1980; Gingerich and Smith 1985; Smith 1985; Conroy 1987; Dagosto and

Terranova 1992). Of these authors, fewer derived regression equations based on forms of similar evolutionary grade (Gingerich 1981; Gingerich et al. 1982; Conroy 1987;

Gingerich and Smith 1985; Dagosto and Terranova 1992) or similar size (Smith 1985).

However, evidence suggests that body size is correlated with phylogenetic history

(Stearns 1980; 1983; Harvey and Clutton-Brock 1985; Wootton 1987; Dagosto and

Terranova 1992; Copes and Schwartz 2010) and authors have urged researchers to consider phylogeny in any cross-species comparative analyses (Conroy 1987; Cheverud et al. 1985; Dagosto and Terranova 1992; Copes and Schwartz 2010).

The paromomyid taxa under study here are considered some of the earliest prosimian primates acknowledged in the fossil record (Simpson 1955, Szalay 1968).

Consequently, in terms of finding a suitable extant model group to estimate body weight and generation time, I turn to the extant prosimians. Conroy (1987) derived a least squares regression equation to estimate body size from M1 size from a sample of 22 extant male prosimians and provided body-weight estimates for most non-hominid primate species in the fossil record including P. pagei, P. simsoni, and P. praecox. Here, I improve upon previous efforts by increasing the number of prosimian species included and include both male and female individuals. I provide a regression equation that can be used to estimate body size from M1 tooth size in prosimian grade extant and fossil species.

262 C.2 Materials and Methods

I sampled 46 prosimian grade extant primate species of lemurs, lorises, and tarsiers and includes 156 male, female, and unknown sex individuals. First molar tooth size was the product of caliper measured maximum mesiodistal length and maximum buccolingual breadth. Of the 156 M1 tooth size measurements, 93 were obtained from

Boyer (2008) who reported the same method for measuring tooth size. I measured 63 additional specimens. These data were collected from specimens housed at the University of Michigan Museum of Zoology, Ann Arbor, Michigan (UMMZ), the United States

National Museum, Washington, D.C. (USNM), and the American Museum of Natural

History, New York (AMNH). To estimate intraobserver error and to increase the accuracy of the tooth size calculation, each tooth dimension of the 63 additional specimens was measured in triplicate. I performed Shapiro-Wilk test of normality on each set of measurements and intraobserver error was evaluated using a Friedman’s two- way ANOVA for related samples. Interobserver error was not calculated because there were not enough of the same specimens measured by Doug Boyer and me.

Body weight and generation length data for extant prosimian primates was obtained from the following sources: Hill (1953), Charles-Dominique (1977), Nowak and

Paradiso (1983), Nash and Harcourt (1986), Harvey et al. (1987), Izard & Nash 1988,

Izard et al. (1988), Nash (1993), Weisenseel et al. (1998), Nowak (1999), Singapore

Zoological Gardens Docents (2001), Kappeler and Pereira (2003), Smith et al. (2003),

Nekaris & Bearder (2007), Randrianambinina et al. (2007), Barrickman et al. (2008),

Génin (2008), Mumby and Vinicius (2008), Shekelle & Nietsch (2008), Barrickman and

263 Lin (2010), Kamilar et al. (2010), Pacifici et al. (2013), Zehr et al. (2014), Zimmermann and Radespiel (2014), and Jones et al. (2009).

Body weight, generation length, and M1 tooth size data were converted to natural logarithms and two simple linear regressions were performed and least-squares regression equations were calculated in RStudio v. 1.2.1335 (RStudio Team 2018). The first a regression of body weight on first molar area (Table C.1 and Fig. C.1) and the second a regression of generation time on body weight (Table C.2 and Fig. C.2). Statistics from the corresponding analysis of variance for both regression analyses can be found in Table

C.3.

I performed Shapiro-Wilk test of normality followed by a paired-samples t-test to compare body weight estimates derived from my regression equations to those obtained from the regression equations provided by Conroy (1987) and Millar and Zammuto

(1983) using RStudio v. 1.2.1335 (RStudio Team 2018) software. To test the precision of the body weight and generation time estimates from my regression equations, I excluded one individual (an Arctocebus calabarensis specimen) from the analysis and then used their known M1 size and body weight to see if estimates are close to the true values.

C.3 Results

Estimating Body Weight and Generation Time in Fossil Primates

Shapiro-Wilk tests of normality indicates that each of the three sets of M1 length measurements that I made do not follow a normal distribution, set 1 D(63)=0.905, p<0.001; set 2 D(63)=0.902, p<0.001; set 3 D(63)=0.900, p<0.001. Shapiro-Wilk tests of normality indicates that the first and the third sets of M1 width measurements that I made

264 do not follow a normal distribution; however, the second set does follow a normal distribution, set 1 D(62)=0.960, p=0.043; set 2 D(62) = 0.962, p = 0.050; set 3 D(62) =

0.959, p = 0.036. A Friedman test was carried out to compare M1 length for the three sets of measurements. There was no significant difference found between sets of M1 length

' measurements, J (2) = 4.442, p=0.106. A Friedman test to compare M1 width for the

' three sets of measurements indicated that M1 width measures were different, J (2) =

9.573, p=0.008. Dunn-Bonferroni post hoc tests were carried out and there were significant differences between the first and the third set of M1 width measurements (p =

0.014) after Bonferroni adjustments. There were no significant differences between any other sets of measurements. As a result of these findings, the third set of M1 width measurements were not included and only the first and second sets were used. For consistency, the third set of M1 length measurements were also excluded.

Shapiro-Wilk tests of normality indicates that the body weights derived from

Conroy’s (1987) regression equation and from my regression equation follow a normal distribution, D(8) = 0.965, p = 0.849; D(8) = 0.965, p = 0.849, respectively. There was no significant difference in the body weights derived from my regression equation (M =

174.25 g, SD = 75.37 g) and those estimated from the regression equation provided by

Conroy (1987) (M = 178.56 g, SD = 79.27 g); t(15.96) = -0.118, p = 0.907. A simple linear regression was calculated to predict ln body weight based on ln M1 area. A significant regression equation was found (F(1, 149)=1495.7, p<0.001), with an R2 of

0.91. Prosimian predicted ln body weight is equal to 2.728 + 1.563 (ln M1 size) grams

2 when ln M1 size is measured in mm (Table C.4).

265 Shapiro-Wilk tests of normality indicates that the generation time derived from

Millar and Zammuto’s (1983) regression equation and from my regression equation follow a normal distribution, D(8) = 0.934, p = 0.519; D(8) = 0.927, p = 0.457, respectively. There were significant differences in the generation times derived from my regression equation (M = 1.01 years, SD = 0.178 years) and those estimated from the regression equation provided by Millar and Zammuto (1983) (M = 6.87 years, SD =

0.941 years); t(8.57) = -18.36, p < 0.001.

A simple linear regression was calculated to predict ln body weight based on ln

M1 area. A significant regression equation was found (F(1, 149)=1495.7, p<0.001), with

2 an R of 0.91. Prosimian predicted ln body weight is equal to 2.728 + 1.563 (ln M1 size)

2 grams when ln M1 size is measured in mm (Table C.4). A simple linear regression was calculated to predict ln generation time in years based on ln body weight in grams. A significant regression equation was found (F(1, 34) = 143.06, p<0.001), with an R2 of

0.80. Prosimian predicted ln generation time is equal to 1.801 + 0.355 (ln body weight) years when ln body weight is measured in grams (Table C.5).

I estimate an average body weight of 174.25 grams and an average generation time of 1.01 years for the Ignacius and Phenacolemur species under study. To check the precision of my regression equations, I use the Arctocebus calabarensis individual that I excluded from my regression analyses to compare my estimates to the known average body weight and generation time of A. calabarensis. The A. calabarensis individual has

2 an M1 area that measures 7.85 mm . The recorded average body mass and generation time for A. calabarensis is 258.01 grams and 0.82 years, respectively. Using my body

266 weight regression equation, I estimate that the body weight of the A. calabarensis individual would have been 383 grams. This results in a difference of 124.99 grams from the recorded average body mass for A. calabarensis. Using Conroy’s (1987) equation for body mass I obtain an estimate of 401 grams, which results in a difference of 142.99 grams from the recorded average body mass for A. calabarensis. I estimate a generation time of 1.18 years for the A. calabarensis individual using my generation time regression equation, which results in a difference of 0.36 years. Using Millar and Zammuto’s (1983) equation for generation time, I obtain an estimate of 7.79 years, which results in a difference of 6.97 years.

C.4 Discussion and Conclusions

The results indicate that my regression equation for estimating Ln body weight from Ln M1 size provides results that do not differ significantly from the regression equation that was provided by Conroy (1987). The regression analysis shows that my model explains 91% of the observed variation around its mean compared to 83% reported by Conroy (1987).

My regression equations for estimating body weights (grams) and generation times (years) do better at estimating true values than the regression equations provided by

Conroy (1987) and Millar and Zammuto (1983). The body mass and generation time estimates of the Arctocebus calabarensis individual using my regression equations, were closer to the recorded average body mass and generation time of this species than either of the estimates that were made from Conroy’s (1987) or Millar and Zammuto’s (1983) equations. Therefore, I justify the use of my regression equations over theirs.

267 I estimate an average body weight of 174.25 grams and an average generation time of 1.0 years for the Ignacius and Phenacolemur species under study.

C.5 Figures

Prosimians

9

8

7

6 Ln Adult Body Mass (grams)

5

4

1 2 3 Ln m1 Area (mm^2) Fig C.1 Regression of ln body weight on ln m1 size in prosimian primates. Black line represents the least squares regression and the gray bands around the line represent the standard error of the regression coefficient.

268 Prosimians

1.5

1.0

0.5 Ln Generation Length (years) Ln Generation

0.0

−0.5

4 5 6 7 8 Ln Adult Body Weight (grams) Fig. C.2 Regression of ln generation time on ln body weight in prosimian primates. Black line represents the least squares regression and the gray bands around the line represent the standard error of the regression line.

269 C.6 Tables

Table C.1

Upper and lower limits Grade/Study Regression equation R2 of confidence interval

Prosimians/This study Ln B = 1.563 Ln A + 2.728 0.91 1.483 – 1.643

Prosimians/Conroy (1987) Ln B = 1.614 Ln A + 2.67 0.83 1.284 – 1.944

Table C.1 Regression equations, ln of body weight (grams) on ln of lower first molar area (mm2) in prosimian primates from this study and Conroy (1987).

Table C.2 Upper and lower limits of Grade/Study Regression Equation R2 confidence interval

Prosimians/This study Ln B = 0.355 Ln A - 1.801 0.80 0.295 – 0.415

All mammals/Millar and Ln B = 0.27 Ln A + 0.554 0.82 - Zammuto (1983)

Table C.2 Regression equations, ln of generation time (years) on ln of body weight (grams) in prosimian primates from this study and Millar and Zammuto (1983).

270

Table C.3 Ln generation time on Ln body Ln body weight on Ln m1 area weight

Grade/Study Mean Square F value p -value Mean Square F value p -value

Prosimians/This 243.27 1495.7 <0.001 6.538 143.06 <0.001 study

Prosimians/Conroy 32.05 97.08 <0.001 - - - (1987)

Table C.3 Analysis of variance in the regressions of Ln of body weight on Ln of lower first molar area in prosimian primates from this study and Conroy (1987). Analysis of variance in the regressions of Ln of generation time on Ln of body weight from this study.

271

Table C.4

Estimated body weight Estimated body weight (g) using regression (g) using Conroy (1987) Species equation from this study regression equation

Ln B = 1.563 Ln A + 2.728 Ln B = 1.614 Ln A + 2.67

P. willwoodensis 121.44 122.61

P. simonsi 185.78 190.19

P. citatus 206.45 212.08

P. fortior 282.02 292.68

P. praecox 267.09 276.69

P. pagei 170.57 174.13

I. graybullianus 185.78 190.19

I. frugivorus 99.51 99.82

I. fremontensis 49.65 48.68

Average all species 174.25 178.56

Table C.4 Estimated body weights in grams for each species of Ignacius and Phenacolemur using the regression equation from this study and the regression equation provided by Conroy (1987).

272

Table C.5

Estimated generation time (yrs) using Estimated generation time (yrs) using regression equation from this study the all mammals regression equation Species Ln B = 0.355 Ln A - 1.801 from Millar and Zammuto (1983) Ln B = 0.27 Ln A + 0.554 P. willwoodensis 0.907 6.37

P. simonsi 1.06 7.13

P. citatus 1.10 7.33

P. fortior 1.22 7.98

P. praecox 1.20 7.87

P. pagei 1.02 6.97

I. graybullianus 1.06 7.13

I. frugivorus 0.85 6.03

I. fremontensis 0.66 4.99

Average all species 1.01 6.87

Table C.5 Estimated generation times in years for each species of Ignacius and Phenacolemur using the regression equation from this study and the all mammals regression equation provided by Millar and Zammuto (1983).

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