Bruno Buzatto Phd Thesis
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The evolution of male dimorphism in arthropods Bruno Alves Buzatto BSc (Hons) Biological Sciences, MSc Ecology Centre for Evolutionary Biology School of Animal Biology The University of Western Australia This thesis is presented for the degree of Doctor of Philosophy of The University of Western Australia 2012 ! ! ! ! Summary Discrete morphological variation within conspecific males puzzled Darwin, and still fascinates evolutionary biologists today. Known as male dimorphism, this phenomenon reflects alternative mating tactics (AMTs) among males: the large male morphs typically guard females or reproductive territories and have more elaborate weaponry; the small male morphs normally sneak copulations and have reduced weaponry. Male dimorphism is particularly common among arthropods, and generally results from a conditional strategy in which the expression of distinct male morphs depends on the status of individuals. In this thesis I firstly review the occurrence of male dimorphism and AMTs in insects, and also provide an overview of how current theory explains their evolution. I then move on to investigate empirically some of the several unanswered questions about the genetic architecture and the evolution of male dimorphism. Firstly, using the bulb mite Rhizoghyphus echinopus as a model system, I show that there is genetic variation for the switchpoint that links male morph expression to the status of individuals, which is an important prediction of quantitative genetics models that explain the genetics of such dimorphisms. Secondly, I disentangle the sources of heritability of male morph in R. echinopus, showing that this trait is strongly influenced by a paternal effect that could either be linked to the Y chromosome of males or an indirect genetic effect that is environmentally transmitted. Next, I use the dung beetle Onthophagus taurus to investigate the importance of maternal effects for the ecology of male dimorphism. I demonstrate that female O. taurus perceive population density and respond by changing the phenotype of their offspring, through a new type of maternal effect that represents a transgenerational response of AMTs to demography. Finally, I investigate the coevolution of male dimorphism and sexual dimorphism in a group of arachnids called harvestmen (Opiliones). I show that the evolution of sexual dimorphism usually precedes the evolution of male dimorphism, and that the latter is much more evolutionarily labile than the former, providing some support for an hypothesis that states that male dimorphism mechanisms are evolutionarily co-opted from previously existing mechanisms of sexual dimorphism. My research enhances our comprehension of the different mechanisms affecting the expression of male dimorphism, from genetic, ecological, and evolutionary perspectives. ! i! ii! ! Contents Summary i Contents iii Acknowledgments v Publications arising from this thesis vii Prologue 1 Chapter one, general introduction: Alternative tactics within mating systems 3 1.1 Introduction 5 1.2 Modelling the origin and evolutionary maintenance of AMTs 10 1.3 Ecological genetics and the genetic architecture of AMTs 15 1.4 Alternative mating tactics are widespread in insects 18 1.5 Variation in female mating systems 31 1.6 Conclusion 33 Chapter two: Genetic variation underlying the expression of a polyphenism 35 2.1 Abstract 37 2.2 Introduction 38 2.3 Methods 42 2.4 Results 45 2.5 Discussion 48 Chapter three: Paternal effects on the expression of a male polyphenism 55 3.1 Abstract 57 3.2 Introduction 58 3.3 Methods 60 3.4 Results 63 3.5 Discussion 67 ! iii! Chapter four: Maternal effects on male weaponry: female dung beetles produce major sons with longer horns when they perceive higher population density 77 4.1 Abstract 79 4.2 Introduction 80 4.3 Methods 83 4.4 Results 87 4.5 Discussion 94 Chapter five: Correlated evolution of sexual dimorphism and male dimorphism dimorphism in a lineage of Neotropical harvestmen 101 5.1 Abstract 103 5.2 Introduction 104 5.3 Methods 107 5.4 Results 124 5.5 Discussion 132 Epilogue 141 References 145 iv! ! Acknowledgements The long story of this thesis started several years ago, and for unconditional love and support through all these years, I thank my parents. I also thank my sister, who put up with me for so long and who was an important part of my childhood and bringing up. In a long list of loved ones, I want to thank all my family (a lot of people), including grandmothers, aunties, uncles and cousins, all dearly missed in these long years away from home. Absolutely all of them refuelled my energies in my visits to Brazil, and without that I could not have finished this thesis. They consider me the crazy biologist of the family, for what I am really thankful. I must also thank all the people that influenced my decision to become a biologist, through inspiration, example, and encouragement. My mother has always been the example of extreme dedication, and she is part of the reason I pursued the dream of being a biologist without hesitation. My aunt Lúcia was the first biologist I ever met, and in many ways helped me fall in love with biology. More specifically, I keep tracking my passion for arthropods back to the rocky shores of Itanhaém in southeast Brazil, where my father used to take me to watch small shore crabs. They were so amazing I just fell in love with their articulated legs and claws. I tried to convince my cousins to come with me watch these crabs day after day, and could not understand why they did not think that was the greatest way to spend a sunny day on the beach. I thank them for putting up with me, and I extend my thanks to all the family members who spent time with me at ‘tio Tella’s house’. Finally, a great friend from my childhood, Bart, once said he would grow up to be a biologist and live in a tent in the middle of the desert studying scorpions. Neither of us ever did exactly that, but that sentence never left my mind, and also played a role in what I am today. After I chose to become a biologist, many obstacles in the way could only be surpassed with the help of amazing friends. Here I must specifically cite William, who is the closest I have to a brother (which makes Carol a step sister), Niltão to help me avoid so many “dias cinzas”, and a special group of people called ‘bio 01D’, so many of them so important to me. Being on the track to become a biologist and already in love with arthropods, I still needed to fall in love with science, and that only happened because of Glauco. Thanks for teaching me how to see past the green blur of the forest, Glauquito! And here I extend my thanks to all the others that were at the Museu de História Natural at Unicamp with me: Billy, Tais, Sam, Tiago, Egito, Fátima, Fran, Jean, ! v! Barrinho, Renata, Pato, and to the friends that I later spent time with at USP: Marie, Camila, Musgo, Rachel, Miúdo, and Roberto. Here I also want to thank the ‘Lunch club’ and all its great members: Adal, Glauco, Sam, Miúdo, Alê, Mário and Marco. After I came to Perth, life had lots of new challenges, and I am so thankful to everyone that made my life easier and happier through the course of my years here. That includes Danilo & Steph, my greatest housemates ever, all the football guys (especially Loui, Lam and Classic V), Lalo & family, Bart, Leo & Andrea, Mariana, Danilo & Letícia, Heidi, Steve, Renee, Esther, Janine, Mike, Pete, Jane, Jen, Fran, Emma, and also all the many friends from the ODC, especially Jérôme, Clive, Will and Robin. Pretty much everyone at the Centre of Evolutionary Biology helped me somehow at some stage, especially Paco, John Fitzpatrick, and my supervisors Leigh and Joe. Also a special thanks to all the fellow postgrads that were so important: all the officemates in my three different offices (19 in total!), lab mates, fellow postgrad representatives, and fellow demonstrators. Many of them fall in two or more of these categories. I am also thankful for everyone that helped me in the lab by teaching me something or doing something for me when I was away or with a broken hand: Nalu, my parents (again!), Mariana, Bruno, Janine, Rachel, Guilherme, Fran, Marisa, and Talia. Moreover, I am very grateful to a number of experts for invaluable advice and comments on theory and statistics: Jacek Radwan, Wade Hazel, Curt Lively, James D. Fry, Damian Dowling, Martin Bader, Bill Eberhard, Michael Taborsky, H. Jane Brockmann, Mark A. Elgar, and everyone at the R group. The last component of my thesis included field and museum work in Brazil, and I am grateful to Nalu, Musguinho, ‘Doug’ (Guilherme), Giupponi, Adrik, and Gustavo Miranda for vital assistance in the field trips; Cecilia de Faria for granting access to P.N. Serra dos Órgãos; Ricardinho and Adrik for granting access and assisting my visits to zoological collections; and Glauco again for help in all stages of this trip back home. For funding, I thank the Australian Research Council, the University of Western Australia, Education Australia Limited, and the International Society for Behavioral Ecology. Finally, but most importantly, I thank Nalu for being with me in the last many years, sometimes living together, sometimes a whole world apart, but always supporting and encouraging me.! vi! ! Publications arising from this thesis This thesis is submitted as a series of manuscripts. The first manuscript has been submitted as a book chapter for a peer reviewed scientific book, and the remaining manuscripts have been submitted to or published in international journals. I. Buzatto BA, Tomkins JL, Simmons LW, In press.