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The Function of Pigmentation Genes in the Development and Evolution of Drosophila Mating Behavior

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The Function of Pigmentation Genes in the Development and Evolution of Drosophila Mating Behavior The Function of Pigmentation Genes in the Development and Evolution of Drosophila Mating Behavior by Jonathan H. Massey A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in the University of Michigan 2019 Doctoral Committee: Professor Patricia J. Wittkopp, Chair Assistant Professor E. Josie Clowney Assistant Professor Alison Davis Rabosky David Stern, Group Leader, Janelia Research Campus Professor George Zhang Jonathan H. Massey [email protected] ORCID iD: 0000-0001-6182-2604 © Jonathan H. Massey 2019 Dedication To Anneka, for all your encouragement, love, and support To Mom, for getting me hooked on books ii Acknowledgements I would like to thank Trisha Wittkopp for being an incredible advisor. She is endlessly encouraging and supportive. She repeatedly builds a lab group with colleagues that look forward to working with each other every day. And, she makes science fun. I have learned so much from her, not just about science, but also writing and being an effective leader. I would like to thank David Stern for believing in me, for keeping the bar set high, and for reigniting my love of insects. David is a fantastic scientist and inspires me to always work hard at the bench. His bioinformatic expertise made Chapter 4 possible. I would also like to thank: Abby Lamb for teaching me everything in lab, from PCR to CRISPR; Daayun Chung for pioneering Chapter 2; Jun Li for fearlessly injecting hundreds of embryos to make the first D. elegans ebony mutant; members of the Wittkopp lab, past and present, for their endless support, feedback, and encouragement; Shu-Dan Yeh for inspiring the work in Chapter 4, for laying the groundwork to study D. elegans and D. gunungcola in the wild, and for hosting me in Taiwan and Indonesia; Joanne Yew for hosting me in Hawaii, teaching me about CHCs, and being a fantastic collaborator; my talented and supportive Ph.D. cohort, especially Joe Walker who was always willing to help; members of the Stern lab for welcoming me when I moved to Janelia, especially Yun Ding for her mentorship; Igor Siwanowicz for imaging support and sharing my love of insects; my thesis committee, Josie Clowney, Alison Davis Rabosky, Orie Shafer, and George Zhang who all provided important insights and advice to improve this thesis; the Buttitta Lab, especially Shyama Nandakumar and Ajai Pulianmackal for walking me through IHC for the first time; the Genetics Training Program and Howard Hughes Medical Institute for professional and financial support; my family and friends for believing in me and giving me a home full of love and support; and Anneka, for brightening every day, for friendship, encouragement, and giving feedback on every talk, paper, and idea in this thesis. iii Table of Contents Dedication ..................................................................................................................... ii Acknowledgements ...................................................................................................... iii List of Figures ...............................................................................................................vi List of Tables ............................................................................................................. viii List of Appendices ........................................................................................................ix Abstract.......................................................................................................................... x Chapter 1 ....................................................................................................................... 1 The problem .............................................................................................................. 1 Mechanisms linking behavior with anatomy during development and evolution......... 1 Solving the problem in Drosophila ............................................................................ 7 Thesis overview ......................................................................................................... 7 Chapter 2 The yellow Gene Influences Drosophila Male Mating Success Through Sex Comb Melanization............................................................................................... 14 Abstract ................................................................................................................... 14 Introduction ............................................................................................................. 15 Results and Discussion ............................................................................................ 16 Materials and Methods ............................................................................................. 22 Acknowledgements.................................................................................................. 29 References ............................................................................................................... 30 Chapter 3 Pleiotropic Effects of ebony and tan on Pigmentation and Cuticular Hydrocarbon Composition in Drosophila melanogaster............................................. 41 iv Abstract ................................................................................................................... 41 Introduction ............................................................................................................. 42 Materials and Methods ............................................................................................. 43 Results ..................................................................................................................... 49 Discussion ............................................................................................................... 56 Acknowledgements.................................................................................................. 60 References ............................................................................................................... 61 Chapter 4 Genetic Dissection of Correlated Divergence in Wing Pigmentation and Mating Display............................................................................................................. 74 Abstract ................................................................................................................... 74 Introduction ............................................................................................................. 75 Materials and Methods ............................................................................................. 77 Results and Discussion ............................................................................................ 84 Acknowledgements.................................................................................................. 92 References ............................................................................................................... 93 Chapter 5 Discussion and Future Directions ............................................................ 107 What a single mutation teaches us about behavior and evolution ............................ 107 Cuticle structure and function: Consequences of pigmentation gene pleiotropy ...... 109 How behavioral and anatomical divergence map onto the genome ......................... 112 Conclusions ........................................................................................................... 115 Appendices ................................................................................................................. 120 v List of Figures Figure 2-1 The Drosophila melanogaster yellow gene is required for male mating success .......................................................................................................................... 36 Figure 2-2 yellow expression in non-neuronal doublesex-expressing cells, but not fruitless-expressing cells, is necessary and sufficient for male mating success ............... 37 Figure 2-3 yellow expression in non-neuronal 42D04-GAL4 expressing cells is necessary for sex comb melanization and male mating success ...................................................... 39 Figure 2-4 Sex comb melanization is specifically required for male mating success ...... 40 Figure 3-1 ebony and tan affect pigmentation and CHC composition in female Drosophila melanogaster .............................................................................................. 69 Figure 3-2 Effects of pharmacological treatments on CHC lengthening in ebonyCRISPR(1,2) and tan20A mutants ......................................................................................................... 70 Figure 3-3 UV laser desorption/ionization mass spectrometry (UV-LDI MS) did not detect differences in short versus long CHCs between lightly and darkly pigmented cuticle ............................................................................................................................ 71 Figure 3-4 Abdominal pigmentation co-varies with CHC length profiles in the Drosophila Genetic Reference Panel (DGRP)................................................................ 72 Figure 3-5 Variation in ebony and tan expression co-varies with CHC length profiles in the DGRP ...................................................................................................................... 73 Figure 4-1 Wing pigmentation and wing
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