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The Primate Brain: Evolutionary History & Genetics

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The Primate Brain: Evolutionary History & Genetics The primate brain: Evolutionary history & genetics Stephen H. Montgomery Darwin College, University of Cambridge 2011 This dissertation is submitted for the degree of Doctor of Philosophy Declaration This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except where specifically indicated in the text and acknowledgments. This dissertation does not exceed the 60,000 word limit excluding figure legends, referencing and appendices. Stephen H. Montgomery, BA Cambridge, 2011 Page | i The primate brain: Evolutionary history & genetics Summary The expansion of the brain is a major hallmark of primate evolution. However, the fossil record of temporal changes in primate brain size is incomplete and often difficult to interpret. As such, whether brain expansion was limited to a few lineages or was a ubiquitous trend across the primate phylogeny, and how frequently brain size has decreased, are not clear. Using phylogenetic methods and published datasets of brain size I have reconstructed the evolutionary trajectories of brain and body size in primates. The results show that, from a small-bodied and small-brained ancestor, both absolute and relative brain size have shown strong temporal trends to increase and have done so multiple times independently across primate lineages. However, despite a general trend to expand, brain size does decrease in some lineages. Major episodes of brain mass reduction occurred in the Callitrichidae and Cheirogaleidae and are associated with episodes of body size dwarfism. Relative brain size decreased less frequently and can generally be attributed to increased body mass rather than decreased brain mass. I subsequently explored whether the parallel evolution of increased brain size is due to parallelism at the molecular level by studying the molecular evolution of candidate genes across a broad selection of species representing all major clades of anthropoids. These genes were selected as their proposed roles in neurogenesis are associated with cell fate switches highlighted by The Radial Unit Hypothesis, which offers a developmental model of how mammalian brain size evolves. Using molecular tests for positive selection, I show that many of these genes have been under pervasive positive selection across anthropoids. Furthermore, it is demonstrated that the molecular evolution of several key genes is associated with neonatal brain size, suggesting a role in prenatal development that is consistent with a direct effect on neuronal proliferation, and with other structures which provide insights into the role of these genes in brain evolution. This study demonstrates that brain expansion has occurred in parallel across primates and that the genetic basis of brain size evolution may be conserved. It highlights the potential use of adopting comparative methods, and the benefits of utilising primate diversity, when studying the genetic basis of brain evolution. Page | ii Acknowledgements I am very grateful to my supervisor Dr. Nick Mundy whose guidance and tolerance of tangents has made my PhD enjoyable to do and hopefully relatively successful. I thank Drs. Isabella Capellini, Chris Venditti and Prof. Rob Barton for many helpful and stimulating discussions and for contributing to some of the ideas presented in chapters 3 and 5 (any bad ideas are mine of course). Thanks also to my advisors, Dr. Chris Jiggins and Prof. Barry Keverne, and Dr. Adrian Friday for their constructive criticism and advice at key stages of the project. Drs. Brenda Bradley and Marie Pointer were invaluable sources of advice (practical and otherwise) and together with Dr. Neil Walsh, Dr. Tim O’Connor, Oscar Brusa and Philipp Kappell made life in the lab more enjoyable than it would otherwise have been. A big thank you to Linda Wheatley for sorting out more things than I am probably aware of. The Zoology department is a friendly and helpful place and I have greatly enjoyed my time here. As well as those mentioned above the company of Dr. Marta Costa, Rich Merrill, Rich Wallbank, Vera Warmuth, late arrivals Nick Grumpton and Kelly Richards and many others helped make the more tedious days more tolerable. Thanks also to Drs. George Speller and Simon Baxter for enticing me into the Zootallurgy Cricket team; captaining the side was surely my greatest. This project could not have been completed without the help of those who donate tissue samples. We are grateful Andrew Kitchner and Drew Bain (National Museums Scotland), Mike Bruford (Zoological Society London) Leona Chemnick (Center for Reproduction of Endangered Species, San Diego Zoo), Jackie Hooley (Twycross Zoo), Kellie Wyatt (Bristol Zoo) and Christian Roos (Gene Bank of Primates, German Primate Center) for providing samples. I am greatly indebted to Charlotte BB Skelly who has kept me (mostly) sane and (overly) well fed throughout my PhD. Her patience, support and unwavering faith in my ability to muddle through has been a great help. Thanks to my brother Michael for his passionate interest in monkey brains and for his continual demand for proof that I am not a dumbass. Finally I’ve dedicated this thesis to Dr. Mum and Prof. Dad who have supported me through 21 years of education. They’ve always stressed the importance of hard work and a good education, hopefully this is proof I was listening at least some of the time. I thank the BBSRC for a 4-year studentship and the Leverhulme Trust for additional funding. Page | iii Dedication For Mum and Dad, two great apes. “I take a jealous pride in my Simian ancestry. I like to think that I was once a magnificent hairy fellow living in the trees, and that my frame has come down through geological time via sea jelly and worms and Amphioxus, Fish, Amphibians, Reptiles, and Apes. Who would exchange these for the pallid couple in the Garden of Eden?" Wilhelm N. P. Barbellion, The Journal of a Disappointed Man, 1919 Page | iv Contents Declaration i Summary ii Acknowledgements iii Dedication iv Contents v Abbreviations viii Chapter 1. Introduction 1 1.1 Primate diversity 2 1.2 The fossil record & evolutionary history of primate brains 2 1.3 The costs of brain expansion 4 1.4 The cognitive significance of brain size 6 1.5 The evolutionary ecology of primate brain architecture 7 1.6 Evolution and the development of primate brains 9 1.7 How can genetics contribute to understanding brain evolution? 12 1.8 Quantitative genetics of primate brains 13 1.9 Evolutionary genetics of primate brains 15 1.9.1 Comparative genomics & transcriptomics 16 1.9.2 Candidate genes 21 1.10 Aims & approach of this thesis 27 1:11 Thesis outline 28 Chapter 2. Materials & Methods 29 2.1 Phenotypic data 30 2.2 Phylogeny 31 2.3 Comparative methods 32 2.3.1 The comparative approach 32 2.3.2 Phylogenetically controlled regressions 33 2.3.3 Ancestral state reconstructions: Weighted Square-Change Parsimony 34 2.3.4 Ancestral state reconstructions: Maximum-Likelihood 35 2.3.5 Ancestral state reconstructions: Bayes Traits 35 2.4 Laboratory methods 37 2.5 Analysis of molecular evolution 37 2.5.1 Protein coding gene evolution & dN/dS 38 2.5.2 Site models 39 2.5.3 Branch models 39 2.5.4 Branch-Site models 40 2.5.5 Caveats with dN/dS 40 2.6 Methods of detecting evolutionary associations between genes and phenotypes 41 3. Trajectories of primate brain evolution 45 3.0 Summary 46 3.1 Introduction 47 3.2 Methods summary 51 3.3 Results & discussion 56 Page | v 3.3.1 Ancestral reconstructions: congruence & inconsistencies between estimates 56 3.3.2 Evolutionary trends in body and brain mass evolution 60 3.3.3 Brain:body allometry 63 3.3.4 Primate origins 66 3.3.5 Increases in brain mass in particular lineages 68 3.3.6 Decreases in brain mass and evolutionary scenarios for H. floresiensis 74 3.4 Conclusions 83 4. A curious case of convergence: Dwarfism, life history & brain size reductions in the callitrichids & cheirogalids 85 4.0 Summary 86 4.1 Introduction 87 4.2 Methods Summary 91 4.3 Results & Discussion 96 4.3.1 The evolution of body mass in callitrichids 96 4.3.2 The evolution of gestation length in callitrichids 102 4.3.3 The evolution of life history and reproductive strategies in callitrichids 109 4.3.4 The evolution of body mass in cheirogaleids 112 4.3.5 Effects of body mass reduction on brain size evolution 120 4.3.6 Homo floresiensis revisited & the impossibility of the pygmy marmoset 129 4.4 Conclusions 131 5. Evolutionary genetics of neural progenitor proliferation & the expansion of radial units 133 5.0 Summary 134 5.1 Introduction 135 5.2 Methods summary 139 5.3 Results & discussion 141 5.3.1 Sequence dataset 141 5.3.2 Pervasive adaptive evolution of microcephaly genes in anthropoid primates 142 5.3.3 Associations between gene evolution and anthropoid brain size expansion 147 5.3.4 Controls for specificity of gene-phenotype associations 153 5.3.5 Branch-site models to detect gene-phenotype associations 154 5.3.6 Gene-phenotype associations within the callitrichids and brain size reduction 162 5.3.7 Do microcephaly genes contribute to sexual dimorphism in brain size? 166 5.4 Conclusions 171 5.4.1 Molecular evolution of microcephaly genes and brain evolution 171 5.4.2 Why do ASPM and CDK5RAP2 differ? 173 5.4.4 Summary 174 6. Evolutionary genetics of neural progenitor proliferation & the expansion of radial growth 175 6.0 Summary 175 6.1 Introduction 176 6.2 Materials summary 181 6.3 Results & discussion 182 6.3.1 NIN evolved under positive selection during anthropoid evolution 182 6.3.2 Associations between evolutionary rate & brain mass 185 6.3.3 Associations between evolutionary rate & radial expansion 187 6.3.4 Independent genetic mechanisms for different aspects of brain evolution 191 Page | vi 6.3.5 The effects of variation in minicolumn spacing 191 6.4 Conclusion 193 7.
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