Effects of developmental plasticity and antagonistic selection on phenotypic variation in spiders by Michael Matthew Kasumovic A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Ecology and Evolutionary Biology in the University of Toronto © Copyright by Michael Matthew Kasumovic 2008 Library and Bibliotheque et 1*1 Archives Canada Archives Canada Published Heritage Direction du Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington Ottawa ON K1A0N4 Ottawa ON K1A0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-39827-2 Our file Notre reference ISBN: 978-0-494-39827-2 NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library permettant a la Bibliotheque et Archives and Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par Plntemet, prefer, telecommunication or on the Internet, distribuer et vendre des theses partout dans loan, distribute and sell theses le monde, a des fins commerciales ou autres, worldwide, for commercial or non­ sur support microforme, papier, electronique commercial purposes, in microform, et/ou autres formats. paper, electronic and/or any other formats. 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Canada 11 The influence of antagonistic selection pressures on the maintenance of phenotypic variation Doctor of Philosophy, 2008 Michael Matthew Kasumovic, Department of Ecology, Evolution and Behaviour, University of Toronto ABSTRACT In this dissertation, I ask whether developmental plasticity can explain the variation of phenotypic distributions as an adaptive response to variation in population demography and changes in the strength and direction of selection. I use three spider species to examine this question. Using a combination of field attraction and mark-recapture experiments, I first ask how male spiders locate females and the choices they make while mate searching. I demonstrate that males can distinguish between females of different species, populations and ages using long-distance pheromones, and that males increase mate searching risks because they are searching for specific females. As these long-distance pheromones can provide cues of female density, I next examine whether juvenile males alter their development when reared in the presence or absence of female's pheromones (cues of high and low female density, respectively). My results demonstrate that males alter their ontogeny to mature the phenotype that is most beneficial in the competitive context they are likely to experience at maturity. Males develop significantly faster when females are present, and are significantly larger and in better condition when females are absent. Since small size is apparently the result of a decision that is independent of resource availability, I next examine whether male fitness is phenotype specific. By testing small and large males in the competitive environments in which they mature, I show that although larger males are superior in direct competitions, smaller males have higher fitness when tested in the context that leads to their more rapid development. These results challenge the concept of male quality as a fixed trait value, demonstrating the necessity of taking life- history traits into consideration. 1 next use field populations to demonstrate that demographic iii variables fluctuate within a season, and depend on the scale of the examination. The strength of selection pressures also varied significantly throughout the breeding season. As a result, males are likely to experience different competitive challenges and selection pressures at different spatial and temporal scales, making a single phenotypic optimum unlikely. I end with a discussion regarding the adaptive nature of developmental plasticity, and when it is likely to evolve. iv ACKNOWLEDGEMENTS There are many people that I would like to thank for helping me during these last five years. However, out of everyone, there's no person that Id like to thank more than my supervisor, Maydianne Andrade. Maydianne has been a supportive and patient supervisor throughout my entire degree. She has provided guidance, offering excellent advice, and has allowed me to continue research in directions that interested me. Overall, this has helped me to grow as a researcher. I know that I could not have been as successful without Maydianne. I'd also like to thank all the others I've worked with in the Integrative Behaviour and Neuroscience group, especially DamianElias and Andrew Mason. Both have been great collaborators and friends. There were also a large number of undergrads that have helped me rear the necessary study organisms and helped with experiments, most notably Kuhan Perampaladas, Nafis Tin, and Shivani Bhalla. I'd also like to thank Mariella Herberstein for all her support and for giving me a home while I was in Australia. Mariella was like a second supervisor while I was in Australia and I've been lucky to have a collaborator like her. I'd also like to thank my committee Darryl Gwynne, Helen Rodd, and Locke Rowe for their insightful comments and discussions regarding my thesis that have helped make it into what it is, and especially for offering advice regarding research and postdoctoral decisions. Thanks to all the graduate students in my cohort for their support and interaction, especially Kevin Judge, Mark Fitzpatrick, Kevin Wilson, and of course, David Punzalan. They all provided many a great discussion on science that helped me to shape some of my ideas and also provided many opportunities to relax over a cold beer or a snowboard strapped to my feet. I also wouldn't be able to get as much done as I did if it weren't for the administrative staff that helped me and made my life easier, especially Brenda Brown, Lucy Pickering, Nella Semoff, and Josie Valotta. Academic life ran more smoothly with all of their help. I would also like to take this opportunity to thank NSERC and OGS for their funding during the duration of my doctoral thesis and V Canadian Journal of Zoology, Current Biology, and Behavioral Ecology for providing copyright permission to allow reprinting of my already published papers in my thesis. And most importantly, I would also like to thank my wife Beth and my family for their support during my Ph.D. and for being so patient during all the times where things needed to be done. My whole family's continued support made it easier to finish my thesis. VI TABLE OF CONTENTS ABSTRACT 11 ACKNOWLEDGEMENTS iv TABLE OF CONTENTS vi LIST OF TABLES ix LIST OF FIGURES x CHAPTER 1: GENERAL INTRODUCTION 1 Literature Cited 13 CHAPTER 2: DISCRIMINATION OF AIRBORNE PHEROMONES BY MATE-SEARCHING WESTERN BLACK WIDOW MALES (Latrodectus hesperus): SPECIES- AND POPULATION-SPECIFIC RESPONSES 25 Abstract 26 Introduction 27 Methods 29 Results 33 Discussion 35 Acknowledgements 39 Literature Cited 41 CHAPTER 3: RISKY MATE SEARCH AND MATE PREFERENCE IN THE GOLDEN ORB-WEB SPIDER {Nephila plumipes) 50 Abstract 51 Introduction 52 Methods 53 Results 57 Discussion 60 Acknowledgements Literature Cited 66 CHAPTER 4: MALE DEVELOPMENT TRACKS RAPIDLY SHIFTING SEXUAL VERSUS NATURAL SELECTION PRESSURES 78 Acknowledgements 81 Literature Cited 82 Supplementary Data 88 Supplemental Literature Cited 92 CHAPTER 5: A CHANGE IN THE COMPETITIVE CONTEXT REVERSES SEXUAL SELECTION ON MALE SIZE 95 Abstract 96 Introduction 97 Methods 100 Results 106 Discussion 108 Acknowledgements 113 Literature Cited 114 CHAPTER 6: SPATIAL AND TEMPORAL DEMOGRAPHIC VARIATION DRIVES WITHIN-SEASON FLUCTUATIONS IN SEXUAL SELECTION 125 Abstract 126 Introduction 127 Methods 129 Results 132 Discussion 139 Acknowledgements 143 vm Literature Cited 144 CHAPTER 7: GENERAL DISCUSSION 162 Conclusion 170 Literature Cited 172 ix LIST OF TABLES Table 1.1: Examples of developmental plasticity in response to various 22 environmental factors Table 1.2: Six criteria required for plasticity to be considered adaptive 24 Table 2.1: The number of males caught at different sampling cages 45 Table 2.2: The G-statistic values for effect of treatment on male attraction to cages 46 Table 3.1: Nominal logistic analysis examining female attraction of males 71 Table 3.2: Results of two separate nominal logistic analyses examining male choice of females 73 Table 4.1: Examination of the effect of female presence and diet on male phenotypes 84 Supplemental Table 4.1: Distance of the nearest penultimate or adult female in the field affects the adult phenotype 94 Table 6.1: Effects of population,