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Adaptation from Standing Genetic Variation and from Mutation

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Adaptation from Standing Genetic Variation and from Mutation Adaptation from standing genetic variation and from mutation Experimental evolution of populations of Caenorhabditis elegans Sara Carvalho Dissertation presented to obtain the Ph.D degree in Biology Instituto de Tecnologia Química e Biológica | Universidade Nova de Lisboa Oeiras, Janeiro, 2012 Adaptation from standing genetic variation and from mutation Experimental evolution of populations of Caenorhabditis elegans Sara Carvalho Dissertation presented to obtain the Ph.D degree in Evolutionary Biology Instituto de Tecnologia Química e Biológica | Universidade Nova de Lisboa Research work coordinated by: Oeiras, Janeiro, 2012 To all the people I love. Table of contents List of Figures 3 List of Tables 5 Acknowledgements 7 Abstract 9 Resumo 13 CHAPTER 1 – Introduction 17 1.1 And yet…it changes 18 1.1.2 Evolution and adaptation 19 1.1.3 Mutation and standing genetic variation 25 Mutation 26 Standing genetic variation 32 Mutation versus standing genetic variation 34 Genetic recombination among adaptive alleles 35 1.1.4 Other players in evolution 37 1.1.5 Evolution in the wild and in the lab 40 1.1.6 Objectives 43 1.2 Caenorhabditis elegans as a model for experimental evolution 45 1.2.1 Experimental populations of C. elegans 50 1.3 References 53 CHAPTER 2 – Adaptation from high levels of standing genetic 63 variation under different mating systems 2.1 Summary 64 2.2 Introduction 64 2.3 Materials and Methods 69 2.4 Results 84 2.5 Discussion 98 2.6 Acknowledgements 103 2.7 References 103 2.8 Supplementary information 110 1 CHAPTER 3 – Evolution of life-history phenotypes under dioecy and 117 androdioecy 3.1 Summary 118 3.2 Introduction 118 3.3 Materials and Methods 122 3.4 Results 133 3.5 Discussion 153 3.6 Acknowledgements 160 3.7 References 161 3.8 Supplementary information 167 CHAPTER 4 – A test on evolutionary transitions between mating 179 systems 4.1 Summary 180 4.2 Introduction 180 4.3 Materials and Methods 186 4.4 Results 189 4.5 Discussion 196 4.6 Acknowledgements 201 4.7 References 201 4.8 Supplementary information 205 CHAPTER 5 – Adaptation from mutation 209 5.1 Summary 210 5.2 Introduction 210 5.3 Materials and Methods 216 5.4 Results 221 5.5 Discussion 239 5.6 Acknowledgements 245 5.7 References 245 5.8 Supplementary information 250 CHAPTER 6 – Discussion 257 2 List of Figures Figure 1.1: Schematic representation of the relationship between genotypes, phenotypes and fitness. Figure 1.2: Additive genetic variation. Figure 1.3: Fisher’s geometric model of adaptation. Figure 1.4: Caenorhabditis elegans life cycle. Figure 1.5: Schematic representation of the morphology of C. elegans hermaphrodites and males. Figure 1.6: Schematic representation of experimental populations used in the present study. Figure 2.1: Schematic representation of the life cycle of C. elegans under laboratory conditions. Figure 2.2: Evolution of outcrossing rates. Figure 2.3: Sex ratio of male-sired progeny. Figure 2.3: Rates of spontaneous production of males in Androdioecious populations. Figure 2.4: Rates of outcrossing and population fitness. Figure 2.5: Evolution of population fitness of genetically diverse populations. Figure 3.1: Evolution of body size of males and of hermaphrodites and females of genetically diverse populations. Figure 3.2: Evolution of viability of genetically diverse populations. Figure 3.3: Diagram of components of fitness under androdioecy and under dioecy. Figure 3.4: Evolution of male competitive performance of genetically diverse populations. Figure 3.5: Evolution of lifetime reproductive success (LRS) of hermaphrodites and females of genetically diverse populations. Figure 3.6: Evolution of reproductive output of hermaphrodites and females of genetically diverse populations. 3 Figure 3.7: Evolution of egg production of hermaphrodites and females of genetically diverse populations. Figure 3.8: Reproductive schedule of self-fertilized hermaphrodites of genetically diverse populations. Figure 3.9: Lifetime production of eggs of hermaphrodites and females of genetically diverse populations. Figure 3.10: Evolution of viability of progeny produced by hermaphrodites and females of genetically diverse populations. Figure 3.11: Lifespan of males of genetically diverse populations. Figure 3.12: Lifespan of mated and unmated hermaphrodites and females of genetically diverse populations. Figure 4.1: Evolution of allele frequencies at the fog-2 locus under two evolutionary scenarios. Figure 4.2: Evolution of male frequencies under two evolutionary scenarios. Figure 4.3: Evolution of male frequencies in populations with different initial frequencies of alleles at a sex-determining locus. Figure 5.1: Evolution of population fitness of genetically homogeneous Androdioecious populations. Figure 5.2: Evolution of male competitive performance of genetically homogeneous Androdioecious and Dioecious populations. Figure 5.3: Evolution of body size of males and of hermaphrodites and females of genetically homogeneous Androdioecious and Dioecious populations. Figure 5.4: Evolution of lifetime reproductive success (LRS) of hermaphrodites and females of genetically homogeneous populations. Figure 5.5: Evolution of offspring production of hermaphrodites and females of genetically homogeneous populations. Figure 5.6: Evolution of egg production of hermaphrodites and females of genetically homogeneous populations. Figure 5.7: Evolution of the production of unfertilized eggs of hermaphrodites and females of genetically homogeneous populations. Figure 5.8: Evolution of viability of progeny produced by hermaphrodites and females of genetically homogeneous populations. 4 Figure 5.9: Evolution of daily viability of progeny produced by hermaphrodites and females of genetically homogeneous populations. List of Tables Table 2.1: Measures of genetic diversity and of inbreeding of ancestral experimental populations calculated from genotyping of microsatellite loci. Table 5.1: Measures of genetic diversity and heterozygosity of ancestral and evolved genetically homogeneous experimental populations. 5 6 Acknowledgements There are many people whom I should thank. Because they were all important (at different levels), I feel it is only fair to thank them “by order of appearance”. I would like to thank my family, for giving the possibility to study when many of them were not given that opportunity. I am truly grateful to my parents in particular, for encouraging me to pursue a career in what I’m passionate about (and not forcing me to become a lawyer or a medical doctor). And, of course, for all their love. I don’t know whom I should thank for giving me the most remarkable woman as a Mum. I thank my “little” brother, João, for sharing with me other ways to see life (I do learn a lot from you, kiddo). My “family thank-yous” would not be completed without expressing my love and gratitude to my godfather, João, and to Micá. I have to thank my high school teacher, Prof. Teresa Paradinha, for showing me that biologists in Portugal can do other things than teaching teenagers. I also thank all the members of the West Side Kru for teaching me so much about science and about life and for being great friends. I thank Luís Marques for his long-standing friendship and support. I need to thank the IGC and all the people who make of it the best Institute I know of. I am particularly grateful to Professor Coutinho for the opportunities he gave me throughout the years, for caring and for being an inspiration – as a scientist, as a director and as an individual. It was my honor and privilege to have both Prof. Coutinho and Isabel Gordo as my thesis committee as, and I thank them both deeply for having accepted my invitation. I thank Fundação para a Ciência e para a Tecnologia for their finantial support with the grant SFRH/BD/36726/2007. This process would not have been the same without close friends to share it with. I thank Catarina Pereira, Tânia Vinagre and Pedro Rifes for making it a lot more fun and exciting. 7 I thank Catarina “Parasita” for the company at late ours in the lab and for reminding me that good friends can come along at any time. I also need to thank my “second” family: Fausto, Estela e Isabel for their support and care. I thank Pedro for giving me the most precious thing, his love. And for making me laugh when everything seems terribly wrong. I thank the former and present members of the Evolutionary Genetics Lab, especially Diogo, for the welcome to the group (when I started) and his encouragement now, close to the end. I thank Miguel Roque, for his help. Ivo Chelo for always having time for my questions, for my silly things and complaints (which he had to endure ll by himself for quite some time!). I thank Ioannis, Christine, Bruno, Peter, Judith and Helena for the great atmosphere in the lab, even when it’s tough. I thank Bruno in particular for his comments and suggestions. Finally, but most importantly, I would like to thank my supervisor, Henrique Teotónio. Thank you for giving me an opportunity to start learning about science. I truly believe I could not have had a better supervisor and I feel extremely privileged for that. When I started this work Henrique told me we would know if we had met our goals if, in the end, we would discuss science and I would show him wrong. I’m not sure I’ve reached that level (yet), but I hope I wasn’t much of a disappointment. 8 Abstract Understanding the genetic basis of adaptation is crucial to explain the emergence and maintenance of the multitude of life forms we find on Earth today. Perhaps even more importantly, gaining knowledge about how fast organisms can cope with environmental changes may prove crucial in a world being altered at increasing speed due to the human actions. The study of adaptive evolution may therefore have major implications (and applications) in Agriculture, Conservation of endangered species and even Human Health.
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