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Function and Diversity of Sex Pheromones in Representative Species of the Black Widow Spiders (Genus

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Function and Diversity of Sex Pheromones in Representative Species of the Black Widow Spiders (Genus Function and diversity of sex pheromones in representative species of the black widow spiders (genus Latrodectus, Araneae: Theridiidae) by Luciana Baruffaldi A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Ecology and Evolutionary Biology University of Toronto © Copyright by Luciana Baruffaldi 2016 Function and diversity of sex pheromones in representative species of the black widow spiders (genus Latrodectus, Araneae: Theridiidae) Luciana Baruffaldi Doctor of Philosophy Ecology and Evolutionary Biology University of Toronto 2016 Abstract Understanding causes and consequences of signal diversity can give insight into how individual fitness is affected by communication, and how this relates to processes from species diversification to mate preferences. During my PhD, I first examined functional divergence in sex pheromones in widow spiders (Theridiidae: Latrodectus), focusing on six species representing different clades and biogeographic regions. I tested the hypothesis that divergence in sex pheromones was predicted by phylogenetic divergence (measured as CO1 sequence dissimilarity). I showed that the most distantly related of my focal species responded only to pheromone extracts from the silk of conspecifics; whereas males from the other species also responded to extracts from more closely related heterospecifics, and, as predicted, male response and genetic divergence were negatively correlated. Next, focusing on two focal Latrodectus species with different mating systems, I showed that males can use sex pheromones alone to discriminate among females of different feeding conditions. Inter- ii specific differences in male discrimination suggested that preferences may arise from benefits of avoiding risky matings with potential cannibals, rather than from seeking fecund, well-fed females. Finally, I examined one Latrodectus species with a recently-demonstrated, novel male mating tactic (mating with immature females), asked whether the tactic is likely to be costly for females, and whether it affects female mate-attraction tactics (pheromone production). I found no cost of immature-mating for females in terms of fertility, fecundity or longevity. Moreover, I showed that immature-mated females do not produce sex pheromones after moulting and so would not attract additional mates after moulting, unlike recently- moulted females that are unmated. My research shows how sex pheromone function varies among species and individuals with different ecologies and mating behaviours, and how this may affect individual fitness and mating decisions, yielding intriguing new insights into how sexual signals are affected by speciation and sexual selection. iii Acknowledgments A doctoral thesis requires enormous discipline and hard work. The fact that I completed my thesis not only in another language, but also in a country with a culture and climate so different from my own, was a huge personal challenge, and my success was made possible by the unconditional support of several people to whom I am deeply grateful. First of all I would like to thank to my amazing supervisor, Maydianne Andrade, for everything that I have learned as her student - about science, mentorship, and most importantly, about growing as a more compassionate human being. Since we met and I joined her laboratory her support has been unconditional at all levels. She is one of the smartest people I have ever met, and is also one with the most humble character demonstrated in the way that she interacts with students and peers. Her level of support surpassed my expectations as she taught me new things and helped me with the problems that I faced during the course of my PhD. Maydianne gave me the space and independence to develop my own ideas at my own pace. Without her constant support, it would not have been possible for me to include as many species in my research, have the opportunity to travel to different regions to collect them, or present my results at numerous conferences during the course of my PhD tenure. She has not only been my mentor, but someone with whom I could share other personal aspects of my life and I hope that our friendship will continue into the future. I would also like to thank my lab partners Sheena Fry, Charmaine Condy, Emily MacLeod, Maria Modanu and Monica Mowery for always being at my side helping me with my papers, and presentations and contibuting to rich discussions about the direction and impact of my projects. Their friendships and support through the years have been invaluable. I want to especially thank Charmaine Condy for her unconditional support and collaboration with the genetic analysis in Chapter 2 of the thesis and for hugging me every day; and Maria Modanu for her friendship and for making me understand that good friends can be found in any place and time in life. I would also like to thank the members of my PhD Committee, Darryl Gwynne and Jason Weir, for their support, availability, comments and suggestions during the course of my tenure which had a great impact in defining my projects. I am grateful to Emily MacLeod, Sheena Fry, and Michael Kasumovic for collecting and providing spiders from California and Australia. To all of my laboratory and field assistants over the years, without your collaboration it would have been very difficult to take care of all the spider populations. I want to especially thank Humera Siddiqui and Athithya Thambiappah for their help with the volatile pheromone experiments. Also to all the volunteers and laboratory managers, thank you for your very important role in growing and maintaining our spider populations. I would like to especially thank all the members of the Laboratory of Ethology, Ecology and Evolution (IIBCE-Uruguay) for all their unconditional support over the years, especially to Laura Montes de Oca for her help with L. mirabilis in the field and in the laboratory, and Anita Aisenberg and Fernando Costa for their affection and always allowing me to develop experiments in the laboratory. I am grateful to the “Direccion General de Recursos Naturals Renovables-Division de Areas Protegidas y Fauna- Departamento de Fauna (Montevideo- Uruguay)” for allowing me to collect and export L. mirabilis from Uruguay. iv I am grateful to the financial support from the Animal Behaviour Society,The Society of Integrative and Comparative Biology, and the “Comision Sectorial de Investigacion Cientifica (Uruguay)”. To my fellow Latinos at UofT!! Paola, Santiago, Maya, Alfredo, Eli, Santiago, Sol, thanks for the moments we shared together including parties, meals, and nights out that made me feel at home during all of the times that we spent together. I want to also thank Mauricio Terebiznik and his family for opening their home to us all. To my friends back home, they made me feel closer than ever and were always by my side, just only a call away listening and encouraging me at every step, Sol, Naty, Lu, Carla, Magy, Lali, Lili and Lau. To my family, especially my parents for whom it was not easy to have me so far from home, but always unconditionally supporting my studies. Since a very young age, they taught me the importance of having the best education possible in order to have more opportunities in life and be able to choose what makes you happy, even if it meant to travel so far and work with poisonous spiders and not cutter animals. To Mar, for being always by my side, in the lowest and highest moments of our journey together, for caring so much when I needed you the most, and for always looking on the bright side of things. Without your support, friendship, understanding and love nothing would have been easier! To Bicha…. Thanks, Lu Agradecimientos Una tesis de doctorado requiere de mucha disciplina, esfuerzo y trabajo. Especialmente para mí, hacerla no solamente en otro idioma sino también en un país con una cultura y clima tan diferente, fue un desafío personal muy grande y fue posible por el apoyo incondicional de varias personas a las cuales les estoy profundamente agradecida. Primero que nada me gustaría agradecerle a mi maravillosa supervisora, Maydianne Andrade, por todo lo que he aprendido siendo su estudiante sobre ciencia, tutelaje y también sobre crecer como un ser humano mas compasivo. Desde que nos conocimos y me uní a su laboratorio, su apoyo ha sido incondicional a todos los niveles. Ella es una de las personas más inteligentes que he conocido, y también es una de las más humildes en su manera de interactuar con sus estudiantes y pares. Su nivel de apoyo fue más allá de mis expectativas a la hora de enseñarme y ayudarme con los problemas a los que fui enfrentándome durante el transcurso de mi doctorado. Maydianne me dio la independencia para poder desarrollar mis propias ideas y a mi propio ritmo. Sin su constante apoyo no hubiese sido posible para mí incluir numerosas especies en mi tesis, ni poder viajar a colectarlas a diferentes regiones, como tampoco poder presentar mis resultados en numerosos congresos durante el transcurso de mi doctorado. No solo ha sido mi mentora, sino alguien con quien pude compartir otros aspectos de mi vida y espero que nuestra amistad continúe por muchísimo tiempo. También me gustaría agradecerles a mis compañeras de laboratorio Sheena Fry, Charmaine Condy, Emily MacLeod, Maria Modanu and Monica Mowery por estar siempre a mi lado v ayudándome con mis presentaciones, papers y en numerosas charlas acerca de la dirección e impacto de mis proyectos. Su amistad y apoyo en todo este tiempo ha sido invaluable. Quiero especialmente agradecerle a Charmaine Condy por su ayuda incondicional y colaboración en el capítulo 2 de la tesis y por abrazarme todos los días; y a Maria Modanu por su amistad y por hacerme entender que muy buenos amigos se pueden encontrar en cualquier lugar y momento de la vida. A mi comité de seguimiento Darryl Gwynne y Jason Weir, por su apoyo, disposición, comentarios y sugerencias a lo largo del transcurso de mí doctorado los cuales tuvieron un gran impacto a la hora de definir mis proyectos.
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