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Using Drosophila Pigmentation to Study How Differences in Traits Arise

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With Flying Colors: Using Drosophila Pigmentation to Study How Differences in Traits Arise. By Alisha Victoria John A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Molecular, Cellular, and Developmental Biology) in the University of Michigan 2017 Doctoral Committee: Professor Patricia J. Wittkopp, Chair Associate Professor Scott E. Barolo Associate Professor Gyorgyi Csankovszki Assistant Professor Monica Dus Alisha V. John [email protected] ORCID iD: 0000-0002-7610-8494 © Alisha V. John 2017 Dedication To all those who made this journey possible - my family for their unwavering support and unconditional love, my friends for their welcomed distractions and encouragement, JG for believing in me and standing with me through all of life’s adventures, for all young women who dream of exploring STEM fields, and for the younger version of myself – that little girl with a fierce love of science and unending curiosity, may she live forever in my soul and fuel my future endeavors. ii Acknowledgements Throughout this journey, I was surrounded by many individuals who helped make this achievement not only possible, but also enjoyable and worthwhile. They helped celebrate the triumphs and made the challenges tolerable. First, I will forever be thankful for the guidance, support, and inspiration offered by my advisor, Trisha Wittkopp. Over the last five years, she has encouraged me to be the best scientist I can be – sometimes directly and sometimes indirectly by being a brilliant, eloquent, and creative scientist. Her influence and support in my life, both personally and professionally, is undeniable and I will forever be thankful to have spent these years working with such an incredible mentor. I could not imagine a better environment to have completed the work presented than in the Wittkopp Lab. I was constantly surrounded by immensely talented and helpful scientists, creating an environment in which everyone could thrive and work together to encourage the production of great scientific study. I am also grateful for all the coworkers who have become friends – this journey would not have been the same without our lab adventures. I would give specific thanks, but it would simply be a list of all of those who have been part of the Wittkopp Lab since 2011. I would also like to acknowledge the Program in Biomedical Sciences (PIBS) and the department of Molecular, Cellular, & Developmental Biology (MCDB). PIBS allowed me the freedom to explore my scientific interests during my first year of graduate school; without that opportunity, I would not have been able to discover my interest in gene regulation and evolution iii nor find the Wittkopp Lab. In addition, PIBS has offered incredible support throughout my graduate studies – both financially by supporting my travel to scientific conferences and professionally by offering opportunities for career exploration, professional development, and networking. After my first year, MCDB welcomed me into their department and I am appreciative for the sense of community and support I found there. I would especially like to thank my fellow graduate students, specifically those on the MCDB Graduate Student Council, for the sense of comradery it brought. One of my biggest passion projects outside of research these past years has been science communication and outreach. These activities, and the individuals involved in them, impacted my development as a scientist greatly. I am better able to communicate my enthusiasm for science and inform others after these experiences. Specifically, I’d like to thank the founding members of MiSciWriters – Ada Hagan, Bryan Moyers, Irene Park, Kevin Boehnke, and Shweta Ramdas; working with these individuals sharpened my writing and editing skills and encouraged me to explore scientific interests outside of the work presented here. I’d also like to acknowledge the following opportunities for their influence on my personal and professional development: the Portal to the Public Science Communication Fellowship at the Detroit Zoo, FEMMES at the University of Michigan, the WISE GISE Summer Camp Human Genetics Focus Group (specifically Anat Belasen for being an amazing person to develop a curriculum with), and my cohort at the National Association of Interpretation Certified Interpretive Guide training course at the Brookfield Zoo in Chicago, IL. While the importance of the scientific support I received is undeniable, the personal support is equally important. In this regard, my family and friends must be acknowledged. To my mom, who encouraged me to complete one more rotation (which happened to be in the Wittkopp iv Lab) before deciding that my place in the scientific community wasn’t going to be found at the University of Michigan. To my dad, for always waiting on the sidelines in case I wanted or needed additional support. To my stepdad, for planting the seed of attending graduate school in my mind early in life and for always believing I could accomplish anything I set my mind to. To my sister, for being an inspiration for how to keep a full schedule and still be successful. To my nephews, for inspiring me to not only tell them, but also show them that science is cool and that with hard work they can accomplish their dreams. To my entire family, for their unconditional love, their unwavering support, and their willingness to drop everything if/when I need it. To those friends who have become family, you give my life color; thank you for the laughter and encouragement through it all. And lastly, to JG, for always understanding, always accepting, always appreciating, always believing – this journey would have been far less enjoyable without you to share it with. Finally, to all of those not specifically mentioned who played a role in this great accomplishment, thank you. v Table of Contents Dedication ...................................................................................................................................... ii Acknowledgements ...................................................................................................................... iii List of Tables .............................................................................................................................. viii List of Figures ............................................................................................................................... ix Abstract ......................................................................................................................................... xi Chapter 1 Introduction: Understanding how traits change over time and the contribution of noncoding sequences to phenotypic evolution ....................................................................... 1 Understanding how traits change over time ............................................................................................. 1 Mechanisms of phenotypic evolution ....................................................................................................... 1 The role of coding and noncoding sequences in phenotypic evolution .................................................... 2 Pigmentation in Drosophila as a model system for studying phenotypic evolution ................................ 5 Pigmentation synthesis and regulation in Drosophila............................................................................... 7 Drosophila americana and Drosophila novamexicana as a model for phenotypic evolution ................. 9 Thesis overview ...................................................................................................................................... 12 References .............................................................................................................................................. 13 Chapter 2 Sensitivity of allelic divergence to genomic position: Lessons from the Drosophila tan gene .................................................................................................................... 20 Abstract ................................................................................................................................................... 20 Introduction ............................................................................................................................................ 21 Materials and Methods ........................................................................................................................... 24 Results and Discussion ........................................................................................................................... 30 Acknowledgments .................................................................................................................................. 38 References .............................................................................................................................................. 38 Chapter 3 Evaluating the contribution of tan to pigmentation divergence between D. americana and D. novamexicana using transgenic alleles ....................................................... 43 Abstract ................................................................................................................................................... 43 Introduction ............................................................................................................................................ 44 Materials and Methods ..........................................................................................................................
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