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Female Mate Choice and Male Ornamentation in the Stalk-Eyed Fly, Diasemopsis Meigenii

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Female Mate Choice and Male Ornamentation in the Stalk-Eyed Fly, Diasemopsis Meigenii de la Motte & Burkhardt 1983 1 Female Mate Choice and Male Ornamentation in the Stalk-Eyed Fly, Diasemopsis meigenii James Malcolm Howie Submitted for Ph.D. University College London 2 I, James Malcolm Howie, 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. 3 A C K N O W L E D G E M E N T S First and foremost, I would like to thank my two Ph.D. supervisors, Professor Kevin Fowler (Kevin) and Professor Andrew Pomiankowski (POM). Both have been excellent, and have pushed, and pulled, and sometimes frustrated me into shape. I have learned a lot from them, and I suspect the lessons (the ‘Kevin’ and ‘POM’ in my head) will keep on coming. Thanks guys!! Next, I would like to thank all of the members of the stalkie lab, and also, more recently, those of the Drosophila lab. The Ph.D. would not have happened without you – and that means all of you, really. Thanks! The names of you lot are (in – I hope – alphabetical order), Aaron Towlson, Alison Cotton, David Ellis, Elisabeth (Liz) Harley, Lara Meade, Lawrence Bellamy, Luke Lazarou, Nadine Chapman and Sam Cotton (as well the Drosophila guys, Filipe Ruzicka and Mark Hill). I want to also give a special thanks to Nadine Chapman, who helped me a great deal when I first arrived at this lab, and got me started and integrated. Thanks too, to David Murrel for his advice at my upgrade – it helped. For those who want to share that advice, in short: things take longer than you think. Further to this, I have a raft of summer students and third year students and further fourth year project students to thank for their help. These are, Emily Heathwood, Sam Finnegan (who, I believe, now joins us in the stalkie lab – hurrah!), Maya Konishi, Jack Munns, Isabel Burgess, Zak Jolly --- and a very, very large thanks has to go out to the main man, Harry Dawson, who got down in the trenches, when we counted, and counted, and collected and collected, and dissected and dissected our way through the largest experiment of this Ph.D. and (so far) my life. Thanks man! Now, to the two lab assistants who also helped for short stints. Actually, these are more than lab assistants, as they are my good friends, Anna Aichinger (well, more than a friend), and Koichi Yamanoha. Thanks to you too guys J 4 Of course, on top of all this, there are the friends and fellow scientists from this university and a few others without whom this would all have been that bit less awesome. These include, Claire Asher, Claire Fourcade, Deirdre Dinneen, Federico Mancinelli, Jeremy (Jez) Owen, Mark (the ‘fish king’) Ransley, Anna Rudzinski, Andy, Fraser, Kate Brown, Ian Evans, Ali – the main man at security – James Michaels (without this man’s drill!!), Ridhima and Omer M Sharif. For excellent bro time, and scientific debate, a massive shout out has to be made for Henry Ferguson-Gow. I also want to thank Rich, Greg (Tomlinson), Jon Kennedy, Rafi Latif, Arun Rao, Chloë Swart, Edite Garjane, Steph Ratcliffe, Stephen Bush, Steven Cass, Sebastian Revell, Mish Doyle, Sam Bedford, Maggie May, and Daisy Dickenson – for keeping me alive. After this, I have, of course, to thank my funders – NERC. And now, to the extended family: Annette and John Calver, Tabitha and Nigel, Martine and John, Uncle Dave and Marg, Michelle and Hailey. I have to give a serious thanks to Elisabeth and Christian Aichinger, and to Theresa Aichinger, Doris Lamplmair, and Steffi Rizaj. Thanks! Now to my close relations: thanks Jon, for being, well, about. Thanks more than I can say, to my parents, Siân Howie, and Malcolm Howie. Without these guys, I wonder if I’d ever have made it to the end of this. If I had more time, I would say more. But you are the best parents that one could want. Thanks so much. And then there’s Anna! Ich liebe dich! Und danke! You have helped in more ways than you can know, as well as in the literal help with my diagrammatic figures, and in the lab, and in the band. Well, you are the best. Finally, I would like to dedicate this work to my grandparents, none of whom will either be here, or be able to see this – but without you, I wouldn’t be here (of course) but I also wouldn’t have become the person that I have. To, Helen Findlay, George Findlay, Mary Howie, and Allen Howie – thanks! 5 A B S T R A C T Female mate choice is a crucial driver of sexual selection, leading to the evolution of the diverse male sexual ornaments seen in nature. Yet little is known about the factors that cause variation in different components of female preference, or how these components interact to influence the series of choices that exert selection on male ornaments. Likewise, it is not known how the signals of genetic condition revealed by male ornaments, or reproductive capacity, vary across environments. But this variation is important for both the direct and indirect genetic benefits of female mate choice, as well as for the male-driven effects of reproductive investment on ejaculate allocation and sexual selection. Here, I use the sexually dimorphic African stalk-eyed fly species Diasemopsis meigenii to conduct empirical studies to address these issues. First, I manipulate female mating status (virgin versus mated) and use mathematical and statistical techniques to decompose mate choices made in a repeated sequential no-choice design into estimates of preference, and selection on the male ornament. I show that choosiness and selection, but not the preference function, are elevated in mated females. Second, I use larval diet manipulation and a series of crosses within and between a suite of inbred lines to investigate the across-environmental genetic condition dependence of male sexual ornaments relative to nonsexual traits. I find evidence for the heightened condition dependence of the male sexual trait (male eyespan), and for a novel gene-by-environment interaction in which the effects of genetic stress on sexual trait expression are masked in both high and low but not intermediate environments. Finally, I measure the effects of environmental (E) and genetic (G) stress on reproductive, fertility and attractiveness traits, and find evidence for a qualitative alignment of trait responses (all tend to be positive), but a negative integration across traits (traits that respond most to E respond least to G). The results have important implications for the operation of sexual selection in nature. 6 T A B L E O F C O N T E N T S Chapter 1: General introduction 1.1 Overview 12 1.2 Sexual selection: an historic overview 13 1.3 Theories of inter-sexual selection 16 1.4 Models of condition-dependent sexual selection 29 1.5 The maintenance of additive genetic variance 35 1.6 Reproductive investment 42 1.7 Female mate choice 49 1.8 A review of the literature on stalk-eyed flies 63 1.9 Overview of thesis chapters 83 Mating status affects components of female mating Chapter 2: behaviour and sexual selection in the stalk-eyed fly, Diasemopsis meigenii 2.1 Abstract 89 2.2 Introduction 90 2.3 Methods 97 2.4 Results 111 2.5 Discussion 125 Environmental variation can amplify or mask the signal Chapter 3: of genetic condition in sexual ornaments, in stalk-eyed flies 3.1 Abstract 140 3.2 Introduction 141 3.3 Methods 145 3.4 Results 154 3.5 Discussion 160 7 Environmental and genetic condition dependence of pre- Chapter 4: and post-copulatory reproductive traits in the stalk-eyed fly, Diasemopsis meigenii 4.1 Abstract 173 4.2 Introduction 174 4.3 Methods 182 4.4 Results 190 4.5 Discussion 202 Chapter 5: General discussion 5.1 Overview 216 5.2 Summary of principal findings 217 5.3 Future directions 237 5.4 Final thoughts 247 Chapter 6: References 248 Chapter 7: Appendix 7.1-A Chapter 2. Supplementary material 284 7.1-B Chapter 3. Supplementary material 312 7.1-C Chapter 4. Supplementary material 340 7.2 Female Sneak Copulation 396 7.3 Evolution: Sex or Survival 409 8 L I S T O F F I G U R E S Figure 1.1 51 Figure 1.2 53 Figure 2.1 112 Figure 2.2 113 Figure 2.3 114 Figure 2.4 116 Figure 2.5 118 Figure 2.6 119 Figure 2.7 120 Figure 2.8 122 Figure 2.9 124 Figure 2.10 126 Figure 3.1 147 Figure 3.2 155 Figure 3.3 159 Figure 3.4 161 Figure 3.5 162 Figure 4.1 184 Figure 4.2 191 Figure 4.3 193 Figure 4.4 194 Figure 4.5 196 9 L I S T O F T A B L E S Table 4.1 198 10 CHAPTER 1 GENERAL INTRODUCTION 11 1.1 O V E R V I E W In this introduction, I firstly outline the classical models of sexual selection and discuss the mechanisms by which female preference for elaborate male secondary sexual ornamental traits can evolve. I then describe the lek paradox, introduce the concept of condition and discuss how condition dependence and gene- environment (G x E) interactions can interact to increase additive genetic variation (VA) in sexual traits, resolve the lek paradox, or undermine ornament reliability and the indirect benefits of choice.
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