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Studying the Evolutionary History of Single Markers and the Demographic History of African Populations

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Studying the Evolutionary History of Single Markers and the Demographic History of African Populations Margarida Cardoso Reis Sá Coelho Studying the evolutionary history of single markers and the demographic history of African populations: The evolution of lactase persistence; Genetic structure of Bantu-speaking populations; and the microevolutionary impact of the Atlantic slave trade 2010 Dissertação apresentada à Faculdade de Ciências da Universidade do Porto para a obtenção do grau de Doutor em Biologia Thesis presented to the Faculty of Sciences, University of Porto for the Doctor degree in Biology Orientador científico/Supervisor: Jorge Rocha Agradecimentos/ Acknowledgments A concretização desta tese não teria sido possível sem a colaboração e apoio de muitas pessoas às quais não poderia deixar de agradecer. À Fundação para a Ciência e a Tecnologia agradeço a concessão da bolsa de doutoramento – SFRH/BD/22651/2005. Ao Professor Jorge Rocha, agradeço a oportunidade de realizar os diversos trabalhos que compõem esta tese, nesta fascinante área de investigação. Agradeço também a ajuda e orientação ao longo destes anos bem como todos os conhecimentos que me transmitiu. Ao Professor Sobrinho Simões, agradeço o caloroso acolhimento no IPATIMUP, a atenção dedicada ao meu trabalho, o entusiasmo e a confiança transmitidos. Da Universidade Pedagógica de Moçambique, agradeço ao Professor António Prista e ao Doutor Sílvio Saranga, por terem tornado possível a minha viagem por Moçambique, da qual guardo preciosas recordações e experiências que enriqueceram a maneira de olhar para o meu próprio trabalho. From Stanford University, I would like to thank to Joanna Mountain, Chris Gignoux, Brenna Henn and Matt Jobin, for the warm welcome during my short visit to their research group. Aos colegas do CIBIO, agradeço a ajuda e colaboração, em particular ao Fernando Sequeira, pela paciência e entusiasmo. A todos os co-autores das publicações apresentadas nesta tese agradeço a importante ajuda e colaboração, em especial à Isabel, no decurso dos trabalhos incluídos no Artigo 4. O “bom astral” e verdadeiro espírito de equipa no decorrer do trabalho “dos DIPSTRs” foram sem dúvida uma “armadura” face às dificuldades que surgiram. Incontornavelmente, as frases “É muito difícil levar a vida honradamente” e “Deixem-me dizer estas coisinhas” vão ficar ligadas a este trabalho. Ah, e obrigada também pela Figura I.4! Gostaria também de agradecer a todos os meus colegas do IPATIMUP por terem contribuído, de diversas formas para a realização desta tese. Em particular: Aos colegas da informática, pela ajuda na resolução dos quebra-cabeças “in silico”; Aos colegas e amigos mais próximos com quem tive o privilégio de partilhar saberes e experiências, assim como as alegrias e as tormentas do dia-a-dia: Mafalda, Cirnes, Rui, Alexandra, Filipe, Vânia, Sandra Martins, Sandra Beleza, Susana Seixas, João, Zélia, Patrícia; e, de uma forma muito especial, à Rita, à Sofia, à Joana Rebelo, à Joana Campos e à Isabel (parte 2!)- foi um enorme privilégio poder contar com o vosso apoio e amizade a toda a prova. Obrigada por colorirem os meus dias com a vossa alegria e autenticidade. Aos meus pais, ao Filipe, à Ana Alexandra, ao Ricardo, à Olinda, à Sara e ao Tiago. Foi entre vocês que encontrei a calma, a confiança e a força necessárias para levar este trabalho a bom porto. Table of contents Summary 11 Resumo 15 GENERAL INTRODUCTION 19 1. The study of human evolutionary history through the use of genetic tools 21 1.1 Study of functionally relevant genes: the importance of genes underlying traits 21 with adaptive relevance 1.2 Study of demographic processes underlying human evolutionary history: the 24 importance of the African continent 1.3 Integrating adaptive and demographic histories 28 2. Work outline 30 References 33 PART 1 – The evolutionary history of lactase persistence 39 1.1 Introduction 41 1.1.1 Geographic distribution of lactase persistence and evolutionary hypotheses 43 1.1.2 The molecular basis of lactase persistence 46 1.1.3 The -13910*T allele as a tool to study the evolutionary history of lactase 47 persistence References 49 1.2 Results and Discussion 51 Article 1: 53 Coelho, M., D. Luiselli, G. Bertorelle, A. I. Lopes, S. Seixas, G. Destro-Bisol, and J. Rocha. 2005. Microsatellite variation and evolution of human lactase persistence. Hum Genet 117:329-39. 1.2.1 Comments 67 1.2.1.1 Implications for the evolutionary history of lactase persistence 69 1.2.1.2 Recent developments in the study of lactase persistence evolution 70 References 76 PART 2 – On the edge of Bantu expansions: genetic studies in 79 Southwest Angola and Mozambique 2.1 Introduction 81 2.1.1 Southwestern Angola 86 2.1.2 Mozambique 88 References 92 2.2 Results and Discussion 95 Article 2: 97 Coelho, M., F. Sequeira, D. Luiselli, S. Beleza, and J. Rocha. 2009. On the edge of Bantu expansions: mtDNA, Y chromosome and lactase persistence genetic variation in southwestern Angola. BMC Evol Biol 9:8. Article 3: 133 Alves, I, M. Coelho, C. Gignoux, A. Damasceno, A. Prista and J. Rocha. 2010. Genetic homogeneity across Bantu-speaking groups from Mozambique and Angola challenges early split scenarios between East and West Bantu populations. Hum Biol (in press). 2.2.1 Comments 167 2.2.1.1 Interactions between Bantu-speaking people and hunter-gatherer 169 populations 2.2.1.1.1 Interactions between Bantu and Pygmy populations 170 2.2.1.1.2 Interactions between Bantu and Khoisan-speaking populations 171 2.2.1.1.2.1 Inference based on haplogroups characteristic of Khoisan or 171 Bantu populations 2.2.1.1.2.2 Novel insights provided by the study of the -14010*C lactase 172 persistence associated allele 2.2.1.1.2.3 Implications for the search of the extinct Kwadi gene pool 174 2.2.1.2 Recent developments in the study of the Bantu expansions 175 References 179 PART 3 – Human microevolutionary history and the Atlantic slave 183 trade: a case study from São Tomé 3.1 Introduction 185 3.1.1 The origins of the Atlantic slave trade 187 3.1.2 The origins of African slaves 188 3.1.3 The plantation complex and the Atlantic slave trade 191 3.1.4 Populations emerging in the context of the Atlantic slave trade as models of 192 human microevolution: the case-study of São Tomé References 195 3.2 Results and Discussion 197 Article 4: 199 Coelho, M., C. Alves, V. Coia, D. Luiselli, A. Useli, T. Hagemeijer, A. Amorim, G. Destro-Bisol, and J. Rocha. 2008. Human microevolution and the Atlantic slave trade: a case study from São Tome. Curr Anthropol 49:134-143. 3.2.1 Comments 223 3.2.1.1 Implications for study designs in human populations 225 3.2.1.2 Implications for the genesis of the Angolar language 225 3.2.1.3 The relevance of founder events during human evolution 227 3.2.1.4 Analysing the associations between languages and genetics 228 3.2.1.5 Searching for biogeographic ancestry 230 References 231 CONCLUDING REMARKS 233 References 237 Summary Summary The major contributions provided by genetic tools to our understanding of human evolutionary history can be divided in two main areas. One area comprises the identification and characterization of genes that have been targeted by selection, providing insights into the processes by which human species have dealt with different environments and lifestyles. The other area is related with the reconstruction of the demographic history of human populations, which mainly relies on the combined study of different types of markers with distinct characteristics and modes of transmission. This thesis is divided in three parts. In the first part we present a study on the evolutionary history of lactase persistence, a genetic trait that allows lactose to be digested throughout life. This trait is thought to provide a selective advantage in dairying populations due to the added nutritional benefits of drinking milk. In the second and third parts, we focused on two episodes of the African demographic history: one related with the study of populations from Mozambique and Angola in the context of the large scale migration of Bantu-speaking populations and, the other, centred on the analysis of the population of the small island of São Tomé. Our investigation on the lactase persistence was triggered by the finding that the - 13910*T allele was a robust marker for this trait in individuals of Finnish origin. In fact, at the onset of our work, most studies on the evolutionary history of lactase persistence had been mainly based on the interpretation of correlations between phenotypic frequencies and environmental variables. In a first stage we intended to address two major key points related to the evolution of the -13910*T lactase persistence associated allele: a) to test the role of selection in shaping its present day distribution, and b) to estimate the age of the allele. To this purpose, we studied the microsatellite-defined haplotype variation closely linked to the -13910*T allele in several African and European populations to perform a formal neutrality test. Based on this test we conclude that the -13910*T allele is too recent to have reached its current frequencies without the influence of positive selection. The linked microsatellite variation was also used to calculate absolute ages of the allele, indicating that the -13910*T allele originated only after the separation between European and African populations and may be as recent as 12,500-7,500 years. This estimate associates the origin of the -13910*T allele with cattle domestication in Eurasia. Taken together, our results support the hypothesis that the -13910*T allele arose in Eurasia and reached its present distribution in a relatively short time due to the selective advantage of lifelong unrestricted use of milk.
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