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THE EVOLUTIONARY ECOLOGY OF HOST-MICROBIOME SYMBIOSIS IN ONTHOPHAGUS DUNG BEETLES Erik Stetson Parker Submitted to the faculty of the University Graduate School in partial fulfillment of the requirements for the degree Doctor of Philosophy in the Department of Biology, Indiana University February 2021 Accepted by the Graduate Faculty, Indiana University, in partial fulfillment of the requirements for the degree of Doctor of Philosophy Doctoral Committee ______________________________________ Armin P. Moczek, Ph.D. ______________________________________ Jen Lau, Ph.D. ______________________________________ Jay T. Lennon, Ph.D. ______________________________________ Irene L.G. Newton, Ph.D. ______________________________________ Whitney M. Schlegel, Ph.D. February 24th, 2021 ii ACKNOWLEDGEMENTS This dissertation would not have been possible without the help and support of many people. First, I would like to thank all the members of my committee: Jen, Jay, Irene, and Whitney. Your time, effort, and attention over the years have made me a better scientist and have made the work contained within this dissertation exponentially better than it would have been otherwise. Thank you all for sharing your valuable time with me, and more than anything thank you for caring. I would also like to thank all the past and present members of the Moczek lab for their support and shared expertise over these last six years. Being able to turn to all of you for help with projects when I needed it was almost as important as being able to turn to you all for distraction and entertainment when I was feeling burnt out. Thank you all for being there for me, and especially you, Anna. You were universally a great group of coworkers and I will look back on our time together fondly, even as I miss sharing my days with you all. I also would like to thank my advisor, Armin for everything. It’s no exaggeration to say that I would not have completed this PhD without his unending reservoir of support and encouragement. Heck, I honestly wouldn’t have even enrolled in the program if it wasn’t for his encouragement! So, Armin, thank you for always believing in me and for imagining a greater future than what I myself dreamed could be possible. I wouldn’t be here if it wasn’t for you. Thank you. Finally, thank you to my wife, Chelsie, and our sons, Flynn and Felix. Chelsie, I quite literally would never have physically come to Bloomington, Indiana if it were not for you leading the way, and I certainly would not have made it all the way through my PhD if it was not for your love and support. Thank you for always being my biggest fan and believing even when I did not. iii And to Flynn and Felix, thank you for teaching me important lessons about time management and how to prioritize tasks, and for always reminding me about the important things in life. Thank you, and I love you all. iv Erik Stetson Parker THE EVOLUTIONARY ECOLOGY OF HOST-MICROBIOME SYMBIOSIS IN ONTHOPHAGUS DUNG BEETLES The effect of host-microbe interactions on diverse aspects of host biology are increasingly appreciated across biological disciplines, yet the roles played by these interactions in shaping host evolution remain poorly understood. My dissertation research seeks to address these and related issues using the dung beetle genus Onthophagus. Previous work in this genus has demonstrated that mothers reliably pass to their offspring a conserved group of gut microbes, and that these vertically inherited microbes enhance offspring growth, development, and survival, especially under stress. In the first three chapters of my dissertation, I employed a manipulative method which allowed for the exchange of gut microbiota between Onthophagus species. Using this technique, I was able to first show that different species have diverged to make use of non- interchangeable gut microbiota, and that disruption of these specific host-microbiota relationships has potentially long-term evolutionary consequences. Secondly, I then showed that this host-microbiota species specificity can arise over evolutionarily short timespans, including recently divergent, broadly sympatric and often syntopic sister species sharing virtually identical ecologies. In my third chapter, I was able to show that Onthophagus microbiota may influence population adaptation to local thermal conditions. However, contrary to my original hypotheses, results suggested that local host microbiome interactions may limit, rather than enhance, host fitness. Finally, in my fourth chapter, I employed a microbial sequencing approach to provide an in-depth assessment of the taxonomic composition of the gut microbiota of several dung beetle species, and to determine to what extent microbiome composition changes when hosts are v introduced to novel geographic ranges. As a whole, my dissertation employs a diversity of methodologies to better understand the evolutionary and ecological ramifications of dung beetle microbiome symbioses. vi TABLE OF CONTENTS ACKNOWLEDGEMENTS ....................................................................................................................................... III CHAPTER 1 ........................................................................................................................................................... 1 OVERVIEW ............................................................................................................................................................... 1 THE MICROBIAL ENVIRONMENT AND ITS ROLE IN ADAPTATION ............................................................................. 2 ONTHOPHAGUS DUNG BEETLES .............................................................................................................................. 4 OUTLINE ................................................................................................................................................................... 5 REFERENCES ............................................................................................................................................................. 7 CHAPTER 2 ......................................................................................................................................................... 13 ABSTRACT .............................................................................................................................................................. 13 INTRODUCTION ...................................................................................................................................................... 14 MATERIALS AND METHODS ................................................................................................................................... 17 RESULTS ................................................................................................................................................................. 20 DISCUSSION ........................................................................................................................................................... 23 ACKNOWLEDGMENTS ............................................................................................................................................ 29 REFERENCES ........................................................................................................................................................... 30 FIGURES AND LEGENDS .......................................................................................................................................... 37 CHAPTER 3 ......................................................................................................................................................... 40 ABSTRACT .............................................................................................................................................................. 40 INTRODUCTION ...................................................................................................................................................... 41 MATERIALS AND METHODS ................................................................................................................................... 44 RESULTS ................................................................................................................................................................. 48 DISCUSSION ........................................................................................................................................................... 50 CONCLUSIONS ........................................................................................................................................................ 54 ACKNOWLEDGMENTS ............................................................................................................................................ 56 REFERENCES ........................................................................................................................................................... 57 FIGURES AND LEGENDS .......................................................................................................................................... 65 CHAPTER 4 ......................................................................................................................................................... 70 ABSTRACT .............................................................................................................................................................
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