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Human Population History and Its Interplay with Natural Selection

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Human population history and its interplay with natural selection Veronika Siska Department of Zoology University of Cambridge This dissertation is submitted for the degree of Doctor of Philosophy Trinity College 2018 September Human population history and its interplay with natural selection Veronika Siska Summary The complex demographic changes that underlie the expansion of anatomically modern humans out of Africa have important consequences on the dynamics of natural selection and our ability to detect it. In this thesis, I aimed to refine our knowledge on human population history using ancient genomes, and then used a climate-informed, spatially explicit framework to explore the interplay between complex demographies and selection. I first analysed a high-coverage genome from Upper Palaeolithic Romania from ~37.8 kya, and demonstrated an early diversification of multiple lineages shortly after the out-of-Africa expansion (Chapter 2). I then investigated Late Upper Palaeolithic (~13.3ky old) and Mesolithic (~9.7 ky old) samples from the Caucasus and a Late Upper Palaeolithic (~13.7ky old) sample from Western Europe, and found that these two groups belong to distinct lineages that also diverged shortly after the out of Africa, ~45-60 ky ago (Chapter 3). Finally, I used East Asian samples from ~7.7ky ago to show that there has been a greater degree of genetic continuity in this region compared to Europe (Chapter 4). In the second part of my thesis, I used a climate-informed, spatially explicit demographic model that captures the out-of-Africa expansion to explore natural selection. I first investigated whether the model can represent the confounding effect of demography on selection statistics, when applied to neutral part of the genome (Chapter 5). Whilst the overlap between different selection statistics was somewhat underestimated by the model, the relationship between signals from different populations is generally well-captured. I then modelled natural selection in the same framework and investigated the spatial distribution of two genetic variants associated with a protective effect against malaria, sickle-cell anaemia and β0 thalassemia (Chapter 6). I found that although this model can reproduce the disjoint ranges of different variants typical of the former, it is incompatible with overlapping distributions characteristic of the latter. Furthermore, our model is compatible with the inferred single origin of sickle-cell disease in most regions, but it can not reproduce the presence of this disorder in India without long-distance migrations. ii Declaration This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except as declared in the Preface and specified in the text. It is not substantially the same as any that I have submitted, or, is being concurrently submitted for a degree or diploma or other qualification at the University of Cambridge or any other University or similar institution except as specified in the text. I further state that no substantial part of my dissertation has already been submitted, or, is being concurrently submitted for any such degree, diploma or other qualification at the University of Cambridge or any other University or similar institution. The main text does not exceed the prescribed word limit for the relevant Degree Committee (School of Biology). Veronika Siska 2018 September iii Acknowledgements I would like to give my thanks to the many people in many countries who I met through my PhD journey and without whom the work presented in this thesis would not have been possible. First and foremost, I would like to thank my supervisor, Andrea Manica. Thank you for your continuous support, your understanding and your advice in both academic matters and regarding general life issues. Thank you also for your trust and for giving me the freedom to explore my ideas. I am also grateful for the continuous support of the postdocs in our group – without them, this PhD would have been a very lonely experience. Thank you, Eppie, for your guidance on ancient DNA, for my first, fully positive experience about collaborative research, and for your incredible support when I was searching for my path. I also want to thank Anders for creating the model I could build on; Pier for his warm support (especially in the last, frantic period) and the many useful discussions and Mario and Robert for their effort on modelling. I would like to also thank my advisors, Chris Jiggins and John Welch for insightful comments on my project. Another warm thank goes to those who have given their time to read through my thesis and make sure it is actually in English: to Philipp, Eppie, Pier, Anne-Sophie and Riva. I am also grateful for all of the organisations who supported me. The Gates Cambridge Trust provided the financial basis that enabled me to conduct this research and attend conferences. Even more importantly, the Trust provided a stimulating environment through workshops on general humanitarian and personal development topics and by acting as a platform to meet with like-minded scholars. I also would like to thank the Cambridge Philosophical Society for their financial help in the last year of my PhD studies. Lastly, living in Cambridge would not have been such an incredible, unique experience without my college, Trinity, who not only helped me financially, but was also my home for over three years. In particular, the support of my college tutor, David Spring, the lively discussions over dinner on the Trinity Biology Seminars and the warmth and helpfulness of every member of the college staff made me feel welcome in Cambridge and at Trinity College. The Department of Zoology and the Evolutionary Ecology Lab provided the basis of all of my academic work. The frequent coffee breaks, happy hours, talks showcasing various animals and the odd lunch meeting created a lovely working space. I am grateful for the staff iv to make all of our work possible and feel honoured to have met so many incredible people at Zoology: Riva, Anne-Sophie, Eppie, Pier, Anahit, Robert, Mario, Tim, Anders, Maddie, Maanasa, Lizzie, Alison, James, Jim, Arne and so many others. Such an environment made it possible to keep focused and bounce back at the inevitable downs - I will miss everyone! I also would like to thank my friends who had my back through these exciting, but often challenging years. In Cambridge, Anne-Sophie helped me manage my own expectations and demonstrated that work-life balance is possible, Riva showed what being passionate about a research topic really is like and Young Mi was always there when things were not going according to plan. Another warm thanks goes to David for his support; Konrad for helping me find a job; Daniel, Tim and Lawrence, my climbing companions, and to all the friendly Trinitarians, Zoologists and other Cambridge residents I’ve met. Special thanks to all of my friends in Budapest who made the effort to keep in touch with me through my ever-changing life, visited me and met with me at home: Péter, Szilvi, Laura, Bence and Bálint kept me in touch with “real life” beyond Cambridge. Finally, I am eternally grateful for my family for supporting me in a foreign environment and for giving me the strong roots that I could rely on. This PhD was an incredible journey leading to new destinations. I would like to dedicate my thesis to those closest to me who helped me find my own way: to my parents, Éva and Péter, and to my partner, Philipp. v Contents Contents .................................................................................................................................... vi Chapter 1 General introduction .......................................................................................... 11 1.1 History of anatomically modern humans .................................................................. 11 1.1.1 Evolution of anatomically modern humans ....................................................... 11 1.1.2 The expansion of anatomically modern humans out of Africa .......................... 13 1.1.3 Neolithic transition............................................................................................. 15 1.2 Genome sequencing .................................................................................................. 16 1.2.1 Introduction to genome sequencing ................................................................... 16 1.2.2 Ancient DNA ..................................................................................................... 17 1.3 Modelling .................................................................................................................. 19 1.3.1 Demography ....................................................................................................... 19 1.3.2 Genetics.............................................................................................................. 20 1.4 Natural selection ........................................................................................................ 22 1.4.1 Introduction to natural selection ........................................................................ 22 1.4.2 Confounding effects ........................................................................................... 23 1.5 Bibliography .............................................................................................................. 24 Chapter 2 Palaeolithic Oase genome implies diversification and extinction events across
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