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The Phylogenetic Signal in the Skull of New World Monkeys by Alexander Bjarnason a Dissertation Submitted in Fulfilment of the D

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The Phylogenetic Signal in the Skull of New World Monkeys by Alexander Bjarnason a Dissertation Submitted in Fulfilment of the D The phylogenetic signal in the skull of New World monkeys by Alexander Bjarnason A dissertation submitted in fulfilment of the degree of Doctorate of Philosophy in Biological Anthropology University College London 1 I, Alexander Bjarnason 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. 2 Dedicated to my parents & The memory of Charlie Lockwood 3 Acknowledgements I would like to thank the following for financial support for the research undertaken: Department of Anthropology, UCL, the graduate research fund, UCL graduate school, the central research fund, University of London, and SYNTHESYS. I am indebted to the following institutions for allowing me to study the primate collections in their care: Natural History Museum London, Field Museum of Natural History Chicago, Museum fur Naturkunde Berlin, Naturhistorische Museum Wien, Smithsonian National Museum of Natural History Washington DC, Naturhistoriska Riksmuseet Stockholm, Anthropological Institue & Museum University of Zurich. The staff at the Natural History Museum London in particular (Louise Tomsett, Roberto Portela Miguez and Paula Jenkins) have given me fantastic access to their collections. A big thank you to Bill Stanley who made me feel at home in Chicago on my first research trip, his kindness and warmth meant a great deal to me. Thank you also to the following for providing access to their collections- Bettina Wimmer, Frieder Mayer, Barbara Herzig, Olavi Gronwall, Tea Jashashvili and Marcia Ponce de Leon. I apologise to all those who helped but have been forgotten! This project was proposed by, and developed with, my late supervisor Charlie Lockwood. His loss was devastating personally and professionally. It would be impossible to describe the positive impact he had on my life, and I will just say that my life has been better for having known him, and I hope I have done him proud. From the sadness of his passing new friendships have been formed and old bonds have been strengthened: thank you to Katharine Balolia, Eric Lewitus, Fire Kovarovic, Nick Walton, Roshna Wunderlich, Rich Lawler, Brenda Bradley, Jeremiah Scott and the Lockwood family. I am deeply grateful to my supervisors Sarah Elton and Christophe Soligo, who stepped in to supervise this project and have provided a great deal of academic and pastoral support throughout the years. They each bring something completely different to my work, and can only apologise to them for my complete inability to get my head around singular & plural forms of taxa and data. Andrea Cardini and Brian Villmoare have also both provided an incredible amount of help and support, and I am grateful to them both. Many other researchers have provided varying input over the years (sometimes just a brief e-mail, but it all helps!) and I thank them all- Jim Rohlf, Chris Klingenberg, Chris Gilbert, Alfie Rosenberger, Walter Hartwig, Susan Ford, Rich Kay, Gabriel Marroig, Jim Cheverud, David Polly, Todd Rae, Andrew Chamberlain, Bill Kimbel, John Lynch, Filippo Aureli, John Aguiar and John Fleagle. Thanks to my friends 4 who have put up with me for all these years, offering a break from academia and provided a better work-life balance that has helped me stay sane and happy, especially the lads at football and Aude Moffitt, her family and Edward. Thanks to my extended support network, especially Dr Roger Howells, Tina Grigoriou and Sarah Heke. Sorry to anyone who has helped or contributed over the years but I’ve forgotten to mention. Thank you to my parents and family. They have given me incredible emotional and financial support over the years, and I could not have done this project or thesis without them. Finally, thank you to the monkeys & assorted primates sampled in this project, what an interesting and odd bunch you are. I’m sorry that so many of you got shot and killed, which must have been quite annoying. 5 Abstract Many phylogenetic relationships based on morphology were rejected following the molecular revolution, yet there is a need for phylogenetic analysis of morphology that reliably infers phylogenetic relationships so that we can understand the evolutionary relationships of extant and fossil taxa. I use geometric morphometric and distance-based phylogenetic methods to study the phylogenetic signal in the skull of a clade of primates, the platyrrhines or New World monkeys, and re-examine congruence between molecular and morphological analyses. I collected digital anatomical landmark data from around 1400 specimens belonging to 16 genera and 50 species of New World monkeys, and nine primate outgroup taxa. I take a modular approach, inferring phylogenies based on the whole skull, face and cranial base, with a range of outgroups and outgroups combinations, and repeat analyses for male, female, pooled sex and separate sex data. Inferred relationships are compared to the most recent platyrrhine molecular phylogeny and past morphology-based analyses. Strepsirrhine outgroups performed slightly better as outgroups, as platyrrhines and Old World monkey or ape outgroups often shared homoplasy that interfered with accurate phylogenetic analysis. Phylogenetic analysis of all platyrrhines recovers a weak phylogenetic signal, but phylogenetic analysis of each of the three major molecular clades, atelids, pitheciids and cebids, finds greater congruence between molecular and morphological analyses. The atelids have a strong phylogenetic signal in the face, the pitheciids in all regions of the skull, and the cebid skull and face support three molecular lineages for callitrichines, cebines and owl monkeys, but infer molecular incongruent relationships within the callitrichines. Phylogenetic analysis of the face holds a stronger phylogenetic signal than expected, whereas the cranial base was more plastic and had a weak phylogenetic signal. In platyrrhines, phylogeny, diet, allometry and encephalization all have an important role in shaping craniodental morphology. 6 Abstract Table of contents Chapter 1 Introduction 19 1.1 Project aims 20 1.2 Phylogenetic theory 21 1.3 Geometric morphometrics 24 1.4 The use of morphology to infer phylogenetic relationships 25 1.5 Cladistics 26 1.6 Character Coding 28 1.7 Distance-based phylogenetic analysis & geometric morphometrics 29 1.8 Morphological & molecular matrix correlations 30 1.9 Distances from partial warps 32 1.10 Distances from principal components 32 1.11 The problem with principal components 34 1.12 Alternative methods for phylogenetic analysis of geometric morphometric data 35 1.13 Phylogenetic analysis of morphology 38 1.14 The phylogenetic signal of the primate skull 39 1.15 Modularity 39 1.16 Modularity & primate phylogenetics 41 1.17 The basicranium as the source of a phylogenetic signal 42 1.18 Phylogenetic signal of the face and cranial vault 43 1.19 Body size, scaling and allometry 44 7 1.20 Research Aim and Hypotheses 46 Chapter 2 Platyrrhine phylogenetics and evolution 48 2.1 Platyrrhine taxonomy 49 2.2 Platyrrhine morphological traits 54 2.3 Platyrrhine evolution 61 2.4 Molecular phylogenies of the New World monkeys 63 2.5 The adaptive evolution of platyrrhines 71 2.6 The role of phylogeny, diet and size in platyrrhine morphological evolution 78 Chapter 3 Materials and Methods 81 3.1 Summary 81 3.2 Materials 83 3.3 Methods 86 3.4 Summary 86 3.5 Landmark selection 87 3.6 Geometric morphometrics 94 3.7 Distance-based phylogenetic analysis 97 3.8 The neighbor-joining method 101 3.9 How neighbor-joining works 101 3.10 Outgroups 104 3.11 Craniodental regions and modularity 107 3.12 Modules used in phylogenetic analysis 108 3.13 Male, female, pooled and separate sex analyses 109 3.14 Error 111 8 3.15 Outliers 111 3.16 Tests of landmark error 111 3.17 Removal of landmarks 116 3.18 Sample error 117 3.19 Distances and spaces 118 Chapter 4 Platyrrhine phylogenetic analysis 120 4.1 Introduction 120 4.2 Materials and Methods 133 4.3 Results 136 4.3.1 Whole skull morphology 136 4.3.2 Facial morphology 138 4.3.3 Cranial base morphology 141 4.3.4 Summary of results 145 4.4 Discussion 150 4.4.1 Phenetic craniodental evolution 151 4.4.2 Phylogenetic analysis of platyrrhine morphology 152 4.4.3 Synthesising past and present analyses 154 Chapter 5 Atelid phylogenetic analysis 156 5.1 Introduction 156 5.1.1 Howler monkeys 162 5.1.2 Spider monkeys 162 5.1.3 Muriquis 163 5.1.4 Woolly monkeys 163 9 5.1.5 Atelid phylogenetic relationships 164 5.2 Methods & materials 167 5.3 Results 169 5.3.1 Whole skull 169 5.3.2 Facial morphology 171 5.3.3 Cranial base 174 5.3.4 Summary of results 176 5.4 Discussion 177 5.4.1 Atelid phenetic evolution 177 5.4.2 The atelid phylogenetic signal 178 5.4.3 Phylogenetic analyses considered 179 Chapter 6 Pitheciid phylogenetic analysis 185 6.1 Introduction 185 6.1.2 Callicebus 187 6.1.3 Pithecia 187 6.1.4 Chiropotes 188 6.1.5 Cacajao 189 6.1.6 Pitheciid phylogenetic relationships 189 6.2 Methods & Materials 195 6.3 Results 196 6.3.1 Whole skull 196 6.3.2 Face 197 6.3.3 Cranial base 200 10 6.3.4 Summary of results 206 6.4 Discussion 207 6.4.1 The pitheciid phenetic-phylogenetic signal 207 6.4.2 Pitheciid craniodental evolution 210 6.4.3 Phylogenetic analysis considered 210 6.4.4 Cranial base evolution 213 Chapter 7 Cebid phylogenetic analysis 216 7.1 Introduction 216 7.1.1 Callitrichines 216 7.1.2 Callithrix- One Genus or Four? 218 7.1.3 Callithrix 221 7.1.4 Callimico 222 7.1.5 Saguinus 223 7.1.6 Leontopithecus 224 7.1.7 Cebines 224 7.1.8 Cebus 227 7.1.9 Saimiri
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