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The Enigmatic Evolutionary Relationships of Paleocene Mammals and Their Relevance for the Tertiary Radiation of Placental Mammals

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The Enigmatic Evolutionary Relationships of Paleocene Mammals and Their Relevance for the Tertiary Radiation of Placental Mammals THE ENIGMATIC EVOLUTIONARY RELATIONSHIPS OF PALEOCENE MAMMALS AND THEIR RELEVANCE FOR THE TERTIARY RADIATION OF PLACENTAL MAMMALS Thomas John Dixon Halliday UCL Submitted for examination for the degree of Doctor of Philosophy I, Thomas John Dixon Halliday, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis 1 To Charlotte, the best placental mammal 2 ABSTRACT Understanding the general pattern of how a clade evolves over time is a central aim of palaeontology and evolutionary biology. The observation that the tree of life is asymmetric in species distribution necessitates that rates of evolution, speciation, and extinction vary through time and across phylogeny. The way this variation is distributed can help to inform on historic events, selection pressures, and relationships. Often, at the origination of a clade, it is supposed that there is an ‘early burst’ of diversification, before rates of speciation and morphological evolution slow down as the clade ages. One example of a supposed ‘early burst’ is that of placental mammals, but the internal relationships of the earliest members of this group have prevented further study of macroevolutionary parameters. In this thesis, by building the largest cladistic data matrix to date, I test the relationships of mammals from the earliest Cenozoic, and from the resulting phylogenies, test the hypotheses that the end-Cretaceous mass extinction resulted in an adaptive radiation of placental mammals. I show that Phenacodontidae are most parsimoniously ancestral to Perissodactyla, that a division between Boreoeutheria and Atlantogenata is better supported than one between Xenarthra and Epitheria or Afrotheria and Exafroplacentalia at the root of Placentalia, and that all “condylarths” can be placed, with varying degrees of confidence, as stem members of laurasiatherian orders. I show that there was an increase in rate of morphological evolution immediately after the end-Cretaceous mass extinction, that Placentalia is extremely likely to have originated less than 70 million years ago, and that the rise of Placentalia was associated with an increase in morphospace occupation, and, with a lag, mean pairwise dissimilarity of taxa. These conclusions support the contention that the end-Cretaceous mass extinction was not just an important time in Earth’s ecological history, but crucial to the diversification of mammals to the level observed today. 3 TABLE OF CONTENTS Abstract 3 Table of Contents 4 List of Figures and Tables 8 Acknowledgements 10 1) Introduction 11 a) The Paleocene as an important period 12 b) The hypothesised effect of the end-Cretaceous on mammal 15 evolution c) Measuring morphological rates and disparity 18 d) Biogeographical and climatic context 22 e) Review of placental mammal systematics 24 i) The extant placental tree 24 ii) Paleocene clades and grades 30 iii) Earliest members of extant placental clades 46 f) Aims and objectives of the thesis 51 2) Phylogenetic relationships among Paleocene and Cretaceous 55 mammals a) Abstract 55 b) Introduction 56 i) The effect of the end-Cretaceous mass extinction 56 ii) Hypothesised relationships among Paleocene placental 58 mammals iii) Objectives 60 c) Methods 61 i) Choice of taxa and characters 61 ii) Use of continuous characters 63 iii) Constraining relationships 63 iv) Phylogenetic analysis 67 v) Templeton’s Tests 68 vi) Relative Bremer Support 69 d) Results 69 i) Phylogenetic topology 69 ii) Templeton’s Tests 84 4 iii) Relative Bremer supports 86 e) Discussion 88 i) Resolving placental relationships 88 ii) Dating the origin of Placentalia 92 f) Conclusions 94 3) Dating the origin of placental mammals and rates of evolution 95 over the K-Pg Boundary a) Abstract 95 b) Background 95 c) Methods 98 i) Selecting a tree 99 ii) Dating the phylogenies 103 iii) Calculating evolutionary rate 104 d) Results 108 i) Dating the origin of Placentalia 108 ii) Rates of evolutionary change 111 e) Discussion 113 4) Morphological disparity of eutherians across the Cretaceous- 126 Paleocene mass extinction a) Abstract 126 b) Introduction 126 c) Materials and Methods 128 i) Source of the tree 128 ii) Cladistic disparity 129 iii) Ancestral State Reconstruction 132 iv) Time-binning data 132 v) Calculating disparity 134 d) Results 135 e) Discussion 142 f) Conclusions 149 5) Testing the inhibitory cascade model in Mesozoic and 150 Cenozoic mammaliaforms a) Abstract 150 b) Background 151 i) Inhibitory Cascade Model 151 5 c) Methods 154 i) Taxonomic Sampling 154 ii) Measurements 158 iii) Data analysis 159 d) Results 161 i) Correlations of measurements 161 ii) Comparison of IC Model with previous studies 162 iii) Phylogeny and Diet 165 e) Discussion 168 6) Conclusions 174 a) Key findings 174 i) Phylogenetic relationships of enigmatic Paleocene 174 mammals ii) Dating the origin of Placentalia 175 iii) Rates of evolution across the K-Pg boundary 176 iv) Disparity across the K-Pg boundary 177 v) Conservation of developmental patterns across 178 Mammalia b) Broader context 179 i) Explaining the mammalian radiation in terms of an 179 adaptive radiation ii) Understanding the placental phylogeny 181 c) Future directions 182 i) Biogeography 182 ii) Genomic data 183 iii) Completeness 184 iv) Exploring the use of network analyses on 185 morphological data v) Hidden support in the morphological analyses of 186 eutherian phylogeny vi) Covariation of characters 187 d) Summary 190 7) References 191 8) Appendices 220 a) Appendix 1 – Abbreviations 220 6 b) Appendix 2 – Description of electronic SI 220 c) Appendix 3 – Dietary assignments for Chapter Five 226 Electronic Supplementary Information 1 – List of specimens coded in matrix CD 2 – Discrete character matrix CD 3 – Continuous character matrix CD 4 – List of character states used in matrix CD 5 – List of synapomorphies for major clades of eutherian mammals CD 6 – Bremer support trees CD 7 – Rates analysis code CD 8 – Disparity analysis code CD 9 – Raw tooth measurements used in Chapter Five CD 7 LIST OF FIGURES AND TABLES Figure 1.1 – Contrasting interpretations of the effect of the K-Pg on 19 evolutionary parameters Figure 1.2 – Riostegotherium, an already derived earliest member 29 of an extant superorder Figure 2.1 – Broad-scale changes in the placental mammal 59 phylogeny Figure 2.2 – Constraint topology applied to phylogenetic analysis 65 Table 2.1 – Abbreviations for sets of trees 68 Table 2.2 – Tree statistics for each analysis 70 Figure 2.3 – Topology from the DU analysis 71 Figure 2.4 – Topology from the DF analysis 72 Figure 2.5 – Topology from the DE analysis 73 Figure 2.6 – Topology from the DP analysis 74 Figure 2.7 – Topology from the CF analysis 75 Figure 2.8 – Topology from the CE analysis 76 Figure 2.9 – Topology from the CP analysis 77 Table 2.3 – Results of Templeton’s tests comparing topologies 85 Table 3.1 – Start and end dates of time bins used in dating the 99 topologies Table 3.2 – Occurrence data for genera within the time bins 100 Table 3.3 – Reconstructed divergence dates for major placental 108 clades Figure 3.1 – Distributions of divergence dates for major placental 109 clades Table 3.4 – t-tests comparing the reconstructed dates with the K-Pg 110 boundary Figure 3.2 – Example time-scaled phylogeny showing branch-based 111 rate shifts Figure 3.3 – Example time-scaled phylogeny showing node-based 112 rate shifts Figure 3.4 – Rate of evolution across time bins 116 Figure 3.5 – Lineage accumulation rate through time 121 Figure 4.1 – Comparison of different ways of binning morphology 130 8 Figure 4.2 – Effect of sample size on range-based measures of 136 disparity Figure 4.3 – PCO of cladistic disparity matrix 137 Figure 4.4 – Sums of range of PCO scores through time 138 Figure 4.5 – Sums of variance of PCO scores through time 139 Figure 4.6 – Mean Pairwise Distance of morphologies through time 140 Figure 4.7 – Sums of variance of PCO scores with equal length time 141 bins. Figure 4.8 – Changes in morphospace position for continuous data 143 derived topologies Figure 4.9 – Changes in morphospace position for discrete data 144 derived topologies Figure 5.1 – Illustration of molar size changes in Pentacodon and 153 Hyracotherium Figure 5.2 – High-level phylogeny used to delimit groups in 157 Chapter Five Table 5.1 – Correlations between size parameters in lower molars 162 Table 5.2 – Comparison of regression parameters across analyses 163 Table 5.3 – m2 area as a proportion of total occlusal area 163 Figure 5.3 – Lower molar ratios for 132 mammal genera 164 Figure 5.4 – Minimum area polygons for taxonomic divisions of 165 lower molar area Figure 5.5 – Morphospace positions for Mesozoic mammals, extant 166 and “archaic” ungulates Figure 5.6 – Minimum area polygons for dietary divisions of lower 167 molar area Table 5.4 – Morphospace clustering due to diet and phylogeny 168 9 ACKNOWLEDGEMENTS First and foremost, thanks are due to Dr Anjali Goswami, as primary supervisor of this project, for three and a half years of advice, support, and encouragement above and beyond the level normally expected for a supervisor, for my first experience of palaeontological fieldwork, and for pushing me to get as much from this project as possible. Thanks are also due to Dr Paul Upchurch, whose experience in phylogenetics was invaluable in the tree-building portion of this project, and who has provided a great deal of motivation. Along with Dr Paul Bown, I would also like to thank him for the comments on my upgrade report which marked the transition from MPhil to PhD student status. Advice and help with running the computer programs used in this thesis, and instruction on how to code properly was invaluable from Dr Graeme Lloyd, Dr Mark Bell, Dr David Bapst, and Dr Pablo Goloboff.
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