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Dynamics Underlying Interacting Mechanisms of Sexual Selection

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Dynamics Underlying Interacting Mechanisms of Sexual Selection Dynamics underlying interacting mechanisms of sexual selection by Jeffrey Allan Stoltz A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Ecology and Evolutionary Biology University of Toronto © Copyright by Jeffrey Allan Stoltz 2010 Dynamics underlying interacting mechanisms of sexual selection Jeffrey Allan Stoltz Doctor of Philosophy Ecology and Evolutionary Biology University of Toronto 2010 Abstract Sexual selection drives the evolution of male morphology, life history, physiology, and behaviour across taxa. Here I examine the mechanisms of sexual selection that arise at various stages in mating interactions to identify congruence or conflict between the traits selected by choice and competition. I first examine plasticity of developing male Australian redback spiders (Latrodectus hasselti) and show that male metabolic rates vary adaptively to facilitate the scramble to reach virgins. Next, I show that females cease sex pheromone production after mating and re-advertise receptivity later in their reproductive season effectively creating two windows in which males may compete. I show that females discriminate against males that do not meet a threshold courtship duration suggesting that courtship is the trait selected through choice. However, male-male competition leads to reductions in courtship effort provided to females. During the first window paternity is split equally if rival males mate in quick succession with a virgin female. However, if the second mating is delayed, there is a strong bias in the paternity of the second male. A delay in the second mating is beneficial to females as it reduces longevity costs of polyandry. However, delays in the initial mating decrease female longevity, likely because of elevated metabolic rates of virgins. My research shows that the trait favoured by female choice is in opposition to selection via male-male competition. Females’ sex pheromone production yields windows during which mating will optimize female, but not male, ii fitness. Studies that isolate the mechanisms of sexual selection are valuable in that they can identify the traits under selection. However, my research shows that considering these processes in isolation can lead to incorrect inferences about the net effect of sexual selection. iii Acknowledgements This thesis would not have been possible without the support and input from numerous sources. First, my supervisor, Maydianne Andrade, provided numerous opportunities for my development as a scientist. She allowed me to independently develop and pursue my research interests but has always been available to provide direction and input into projects. She has funded me to go and conduct fieldwork in Australia and conferences to present our research as well as diverted media attention from herself. I am greatly indebted to Maydianne for the time that I was able to spend in her research group. Second, I would like to thank my committee including Helen Rodd and Darryl Gwynne. They provided valuable input into projects and greatly improved the clarity and focus of the manuscripts. Third, I would like to thank the members of the Integrative Behavior and Neuroscience Group at the University of Toronto Scarborough notably Andrew Mason, Norman Lee, Damian Elias, Paul DeLuca and Dan Howard who provided extremely valuable feedback on experiments and presentations. Fourth, I greatly thank my fellow graduate students in the Andrade Lab, Maria Modanu, Janice Ting and Emily MacLeod, for helpful discussions and direction on projects. Maria Modanu deserves special mention for editing my entire thesis. I greatly look forward to her reading her PhD thesis in the future. This research would also not have been possible without the help of the numerous Andrade lab undergraduate volunteers that I have had the pleasure of interacting with over the years. Particularly our lab managers over the past few years Kuhan Perampaladas, Sen Sivalinghem and Tanya Stemberger who ensured populations of the spiders were readily available. Mariella Herberstein at the Macquaire University graciously provided a home away from home while completing my field work and I am indebted to her. Chris Wellstood at Qubit Systems was instrumental in collecting metabolic data and was always available to help calibrate our system. I would also like to thank the Natural Sciences and Engineering and Research Council of Canada and University of Toronto Fellowships for providing funding. Lastly, I would like to thank Lesley Smith for constant encouragement and the sacrifices she has made for me as well as my family for their support throughout this time. iv Table of Contents ABSTRACT II ACKNOWLEDGEMENTS IV TABLE OF CONTENTS V LIST OF TABLES VIII LIST OF FIGURES IX LIST OF APPENDICES XI CHAPTER 1: GENERAL INTRODUCTION 1 References 16 CHAPTER 2: PLASTICITY IN MALE METABOLIC RATES PREDICTED BY CUES OF SEXUAL SELECTION 24 Abstract 24 Introduction 25 Methods 29 Results 32 Discussion 34 Acknowledgements 38 References 39 CHAPTER 3: MALES USE CHEMICAL CUES TO DISCRIMINATE JUST-MATED FEMALES FROM VIRGINS IN REDBACK SPIDERS 57 v Abstract 57 Introduction 58 Methods 61 Results 64 Discussion 65 Acknowledgements 68 References 69 Copyright Acknowledgement 76 CHAPTER 4: FEMALE’S COURTSHIP THRESHOLD ALLOWS INTRDUING MALES TO MATE WITH REDUCED EFFORT 77 Abstract 77 Introduction 78 Methods 81 Results 85 Discussion 88 Acknowledgements 92 References 93 Copyright Acknowledgement 102 CHAPTER 5: FEMALE CRYPTIC CHOICE AND A COST OF SIMULTANEOUS POLYANDRY 103 vi Abstract 103 Introduction 104 Methods 109 Results 114 Discussion 118 Acknowledgements 125 References 127 CHAPTER 6: LONGEVITY COST OF REMAINING UNMATED UNDER DIETARY RESTRCITON 144 Abstract 144 Introduction 146 Methods 151 Results 155 Discussion 158 Acknowledgements 164 References 166 Copyright Acknowledgement 187 CHAPTER 7: GENERAL DISCUSSION 188 References 203 APPENDIX 208 vii List of Tables Table 2.1: Comparison of predictions from two hypotheses for how the 45 resting metabolic rates of male redback spiders may be affected by indicators of the form and intensity of selection. Table 2.2: Sample sizes for a 2x3 rearing design. 46 Table 2.3: Results from a MANOVA examining two fixed factors and one 47 random factor on variation in male characteristics. Table 2.4: Results from three-way ANOVAs. 48 Table 4.1: Proportion of male redback spiders that obtained the first and 97 second copulations. Table 5.1: Relationship between P2 and the relative traits of rival males, or 134 relative features of first and second matings. Table 5.2: Reproductive output of female redback spiders. 135 Table 6.1: ANCOVA for effects of diet, mating status, and initial mass on 175 female longevity. Table 6.2: Effects of diet, and time on resting energetic rates of mated or 176 virgin female redback spiders. viii List of Figures Figure 2.1: Scatter plot of mass and resting metabolic rates. 51 Figure 2.2: Reaction norms of males reared in the absence and presence of 52 females in three different diet treatments. Figure 2.3: Relationship between likelihood of male-male competition and 53 development time as a function of whether females were absent or present. Figure 2.4: Resting metabolic rates of males reared on three diet treatments 54 in the presence of a variable density of male competitors. Figure 3.1: Activity levels of male redback spiders. 75 Figure 4.1: Frequency histogram showing the relationship between 99 premature cannibalism and total courtship duration. Figure 4.2: Relationship between total courtship duration prior to the first 100 copulation and whether males were prematurely cannibalized. Figure 4.3: Duration of courtship following rival introduction. 101 Figure 5.1: Paternity of the second male to mate when two rival males 139 copulated. Figure 5.2: Reproductive output of females measured at different time 140 intervals. Figure 5.3: Lifespan of females that copulated with two males at different 143 time intervals. Figure 6.1: Female Australian redback spider on her web with an egg sac. 180 Figure 6.2: Female longevity as a function of mating status and resource 181 availability. Figure 6.3: Relationship between initial mass (mg) of female redback 182 ix spiders prior to experimental treatments and adult survivorship (days). Figure 6.4: The number of spiderlings produced in the first six successive 183 egg sacs. Figure 6.5: The number of offspring produced per egg sac and body mass 184 of mated female redback spiders in the laboratory and field. Figure 6.6: Total reproductive output of mated females that were either fed 185 normally or placed in a dietary restriction treatment. Figure 6.7: Resting energetic rates of females with different reproductive 186 status and diets. x List of Appendices Male competition and female mass 208 xi 1 Chapter 1 General Introduction Sexual selection arises due to variation in reproductive success among individuals via male-male competition (Darwin 1871, Andersson 1994) and female choice (Darwin 1871, Kirkpatrick 1982). These agents of sexual selection can extend beyond mating and continue operating after copulation in the form of sperm competition (Birkhead & Møller 1998) and cryptic female choice (Thornhill 1983, Eberhard 1985, Eberhard 1996). There is little debate about how mechanisms of male-male competition operate or fit into the theory of sexual selection. In a wide range of taxa, males that are larger or have superior weapons are more successful in competition, more likely to mate with females (Andersson 1994), and sometimes monopolize mating relative to rivals (e.g. LeBoeuf 1974). Traits favouring success in sperm competition have also been widely documented and include increased sperm production (Parker 1998), ejaculatory proteins that affect female receptivity (Chapman et al. 1995), and deposition of sperm plugs (Thornhill & Alcock 1983). In contrast, from its first suggestion by Darwin (1871), female choice has had a contentious history as a mechanism of sexual selection (Huxley 1938, see Cronin 1993). Currently there is no debate as to the existence, importance and strength of selection that female choice can exert on male traits (Kirkpatrick 1982, Jennions & Petrie 1997, Andersson & Simmons 2006; e.g.
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