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UC Santa Cruz UC Santa Cruz Electronic Theses and Dissertations Title Evolutionary consequences of Cenozoic climate change on African lacertid lizards (Squamata: Lacertidae) Permalink https://escholarship.org/uc/item/23p1k768 Author Hipsley, Christy Anna Publication Date 2012 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA SANTA CRUZ EVOLUTIONARY CONSEQUENCES OF CENOZOIC CLIMATE CHANGE ON AFRICAN LACERTID LIZARDS (SQUAMATA: LACERTIDAE) A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in ECOLOGY AND EVOLUTIONARY BIOLOGY by Christy A. Hipsley September 2012 The Dissertation of Christy Hipsley is approved: _________________________________ Professor Barry Sinervo, Chair _________________________________ Professor Giacomo Bernardi _________________________________ Professor Johannes Müller _________________________________ Tyrus Miller Vice Provost and Dean of Graduate Studies Copyright © by Christy A. Hipsley 2012 TABLE OF CONTENTS LIST OF TABLES AND FIGURES …………………………………………………………. v ABSTRACT ……………………………………………………………………………… vii ACKNOWLEDGEMENTS ………………………………………………………………… ix INTRODUCTION ……………………………………………………………………..……. 1 CHAPTER 1. INTEGRATION OF BAYESIAN MOLECULAR CLOCK METHODS AND FOSSIL-BASED SOFT BOUNDS REVEALS EARLY CENOZOIC ORIGIN OF AFRICAN LACERTIDS LIZARDS…………………………………………………………………… 9 Abstract ………………………………………………………………………… 9 Background …………………………………………………………………….. 10 Methods ………………………………………………………………………… 11 Results ……………………………………………………….…………………. 13 Discussion………………………………………………………….………………16 CHAPTER 2. MORPHOLOGICAL CONVERGENCE IN ARID-DWELLING AFRICAN LACERTID LIZARDS DRIVEN BY ECOLOGICAL AND CLIMATIC FACTORS………………. 22 Abstract ………………………………………………………………………... 22 Introduction ……………………………………………………………………. 23 Materials and Methods ………………………………………………………… 26 Results ……………………………………………………………………..…… 33 Discussion ……………………………………………………………………….. 37 CHAPTER 3. EFFECTS OF CENOZOIC ARIDIFICATION ON TAXONOMIC AND MORPHOLOGICAL DIVERSIFICATION OF AFRICAN LACERTID LIZARDS…………………. 76 Abstract ……………………………………………………………………….. 76 Introduction …………………………………………………………………… 77 Materials and Methods ………………………………………….……………… 82 Results ………………………………………………………………..………… 87 Discussion ……………………………………………………….……………… 90 LITERATURE CITED …………………………………………………………………… 110 iii LIST OF TABLES AND FIGURES CHAPTER 1: Table 1. GenBank accession numbers for mitochondrial and nuclear gene sequences used in the phylogenetic analysis of Lacertidae …………………………12 Table 2. Natural logarithm of Bayes factors for the molecular clock models Compound Poisson Process (CPP), Dirichlet Model (DM), Uncorrelated lognormal (ULN), and the strict Molecular Clock (MC), based on the concatenated data set …………………………………………………………… 16 Figure 1. Exponential prior probability distribution with a minimum bound ………13 Figure 2. 95% majority rule consensus tree for Lacertidae with divergences estimated under an Uncorrelated Lognormal relaxed molecular clock, based on a concatenated data set of 3 mitochondrial and 2 nuclear genes …………………15 Figure 3. Comparison of divergence dates estimated in the Bayesian programs TreeTime and BEAST …………………………………………………………… 16 Figure 4. Comparison of mitochondrial DNA and nuclear DNA based estimates of divergence times …………………………………………………… 16 Figure 5. Influences of individual calibration points on node ages …………………17 Figure 6. Paleogeographic map of Europe and North Africa in the late Eocene . 18 CHAPTER 2: Table 1. Traits studied in relation to interspecific morphological variation in Lacertidae …………………………………………………………………………43 Table 2. Species included in phylogenetic and morphological analyses of Lacertidae, with GenBank accession numbers and sample sizes (N) for each data set .................................................................................................................. 44 Table 3. Bioclimatic variables extracted for each individual in Data set 2 from the Worldclim database …………………………………………………………………46 Table 4. Loadings from the first four principal components of morphological variables in a) Data set 1, and b) Data set 2 …………………………………………47 Table 5. F-test scores across pairs of a) biome types in Data set 1 and b) substrate types in Data set 2 …………………………………………………………48 Table 6. Results of Pagel’s lambda test for phylogenetic signal in morphological variables in a) Data set 1 and b) Data set 2 …………………………49 Table 7. Bioclimatic variables in order of importance for predicting morphological variation of lacertids in arid-dwelling African clades …………… 50 iv Figure 1. Lacertid sampling sites for Data set 2 in a) Sudan, and b) Namibia ……51 Figure 2. Time-calibrated molecular phylogenies used in the comparative analyses of lacertid taxa in a) Data set 1, and b) Data set 2 …………………………52 Figure 3. Morphological variation in Lacertidae along the first two principal components axes ………………………………………………………………… 53 Appendix 1. Data set 1 taxon sampling ……………………………………………54 Appendix 2. Data set 1 summary ……………………………………………………60 Appendix 3. Data set 2 summary ……………………………………………………64 Appendix 4. Phylogenetic and molecular clock analysis …………………………68 Appendix 5. Phylogenetic trees for comparative analyses …………………………70 CHAPTER 3: Table 1. Paleoclimatic events in the Cenozoic with potential effects on African biota ………………………………………………………………………96 Table 2. Osteological characters used in ancestral state reconstructions of Lacertidae, based on Arnold (1983, 1989a, b, 1991) and Arnold et al. (2007) ……97 Table 3. Results of Pagel’s (1994) correlation analyses of osteological characters and habitat type for Lacertidae ……………………………………… 98 Table 4. Results of Pagel’s (1994) correlation analyses of osteological characters ………………………………………………………………………… 99 Figure 1. X-ray computed tomographic rendered skulls of a) the mesic- dwelling palearctic lacertid Podarcis muralis, with principal dorsal bones labeled, and b) the arid-dwelling north African lacertid Acanthodactylus boskianus, showing common derived features ………………………………… 100 Figure 2. Time-calibrated Bayesian phylogeny for Lacertidae based on 1012 bp of the nuclear gene RAG-1 ……………………………………………………101 Figure 3. Ancestral character state reconstructions of osteological cranial characters found to be significantly correlated with transitions to arid habitat ……102 Figure 4. Lineage-through-time plots for a) the family Lacertidae and two of its main clades, and b) the African subclade Eremiadini, split into its component groups …………………………………………………………………103 Figure 5. Net rate of diversification estimated from the molecular phylogeny for a) Lacertidae and b) its subclades ………………………………………………104 v Appendix 1. Taxon sampling and catalogue numbers of museum specimens scored for osteological characters based on CT ……………………………………105 Appendix 2. Description of osteological characters listed in Table 2, based on morphological analyses of Arnold (1983, 1989a, b, 1991) and Arnold et al. (2007) ………………………………………………………………………………106 Appendix 3. Character distributions and habitat assignments used in ancestral state reconstructions of Lacertidae ……………………………………………… 108 vi ABSTRACT EVOLUTIONARY CONSEQUENCES OF CENOZOIC CLIMATE CHANGE ON AFRICAN LACERTID LIZARDS (SQUAMATA: LACERTIDAE) CHRISTY A. HIPSLEY The evolutionary diversification of many terrestrial vertebrate groups is strongly linked to climatic events in the Cenozoic, the period from 65 Million years ago to today when modern animals first appeared. I investigated the effects of Cenozoic climate change on the taxonomic and morphological diversification of the Old World lizard family Lacertidae, with particular emphasis on the African radiation. African lacertids exhibit an unusual pattern of diversification, in which their highest species richness occurs in deserts north and south of the equator, despite being spread throughout the continent. This disparity is particularly surprising given that desert lacertids are thought to be evolutionarily younger than their mesic-dwelling relatives, suggesting increased diversification rates in arid habitats. To identify the evolutionary factors underlying this pattern, I use a combination of phylogenetic, morphological and ecological techniques. In Chapter 1, I apply Bayesian methods and fossil-based calibrations to molecular sequence data to construct a time-calibrated phylogeny for Lacertidae. I estimate that the family arose in the early Cenozoic, with the majority of their African radiation occurring in the Eocene and Oligocene. In Chapter 2, I describe changes in lacertid body shape across biomes and substrates, and find widespread morphological convergence in similar habitat types. I suggest that in addition to foraging demands, fluctuating and extreme climatic conditions, largely driven by precipitation and temperature, contribute to morphological convergence across independent arid-dwelling clades. Finally, I test if ancestral transitions in ecology, morphology, and rates of diversification temporally coincide with paleoclimatic events in the Cenozoic. I use High Resolution X-ray Computed Tomography to characterize changes in the skull related to life in arid habitats, and apply vii maximum likelihood methods to test if the origins of those traits temporally coincide with significant shifts in habitat, diversification rates and climatic changes. My results show that African lacertids experienced three major peaks in diversification, accompanied by the evolution of suites of arid-adapted morphological traits.

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