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ECOLOGY and EVOLUTION of LEPIDOPTERA-MICROBE SYMBIOSIS by TOBIN JEREMY HAMMER B.S., University of California San Diego, 2009

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ECOLOGY and EVOLUTION of LEPIDOPTERA-MICROBE SYMBIOSIS by TOBIN JEREMY HAMMER B.S., University of California San Diego, 2009 i ECOLOGY AND EVOLUTION OF LEPIDOPTERA-MICROBE SYMBIOSIS by TOBIN JEREMY HAMMER B.S., University of California San Diego, 2009 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2018 ii This thesis entitled: Ecology and Evolution of Lepidoptera-Microbe Symbiosis written by Tobin Jeremy Hammer has been approved for the Department of Ecology and Evolutionary Biology Dr. Noah Fierer Dr. M. Deane Bowers Date The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline. iii Hammer, Tobin Jeremy (Ph.D., Ecology and Evolutionary Biology) Ecology and Evolution of Lepidoptera-Microbe Symbiosis Thesis directed by Professor Noah Fierer ABSTRACT Microorganisms are now recognized to be integral components of the biology of many animal and plant taxa. These symbionts can play critical roles in host development, physiology, and in the mediation of ecological interactions among hosts. The study of insect-associated microbial symbionts is of particular interest, as insects comprise an enormous fraction of terrestrial biodiversity, provide important ecosystem services, and include destructive pests and disease vectors. However, symbiotic microbial functions are well-understood for only a limited set of insect taxa, and the broader ecological relevance of insect-microbe symbiosis is often unclear. Here, I describe four studies I undertook to investigate the structure and function of insect-associated microbiomes, with a particular emphasis on Lepidoptera (butterflies, moths, and their larvae). First, I conducted a comprehensive review of the literature pertaining to interactions between herbivorous insect gut microbes and the chemical compounds with which plants defend their tissues; these interactions may explain insect feeding patterns and diversification. Second, I found that antibiotic treatments, commonly administered to livestock, have unintended negative consequences: antibiotics retained in cattle dung affect the microbiome of dung beetles as well as modulate emissions of microbially produced greenhouse gases. Third, I investigated the composition and developmental dynamics of bacterial communities inhabiting a butterfly, finding that the butterfly microbiome undergoes a restructuring analogous to host metamorphosis. Fourth, I explored the gut microbiomes of a diversity of larval Lepidoptera, and found evidence for their generally transient nature. Collectively, these findings demonstrate that microbiomes can be highly diverse in form and function both within species and across major clades of hosts. They may also inform management practices, such as antibiotic use or pest control strategies. iv ACKNOWLEDGEMENTS I would first like to express my sincere gratitude to my advisors Noah Fierer and Deane Bowers, who have been incredibly generous mentors, and instrumental in my growth as a scientist during the last six years. I thank my committee members Stacey Smith, Allen Herre, and Nolan Kane for their valuable feedback throughout the development of my thesis. In addition, I deeply appreciate the scientific mentorship that Daniel Janzen and Winnie Hallwachs have provided me, and for their facilitation of my field research in the Guanacaste Conservation Area. A Chancellor’s Fellowship from the Univesity of Colorado and a Graduate Research Fellowship from the National Science Foundation supported me during my graduate studies. Jessica Henley and Matt Gebert provided assistance with sequencing. Members of the Fierer and Bowers research groups provided helpful input on each research project. Evelyn Beaury assisted with dung and beetle processing in the laboratory. Jonathan Leff provided helpful input on bioinformatic and statistical analyses. Finally, I am indebted to undergraduate students Jacob Dickerson, Kristen Vaccarello, and Hunter Layton for their invaluable assistance with field collections and laboratory work. v CONTENTS CHAPTER I ...................................................................................................................................................... 1 INTRODUCTION AND OVERVIEW ............................................................................................................ 1 CHAPTER II ..................................................................................................................................................... 6 GUT MICROBES MAY FACILITATE INSECT HERBIVORY OF CHEMICALLY DEFENDED PLANTS ................. 6 Abstract ............................................................................................................................................. 6 Introduction ...................................................................................................................................... 7 Main text ........................................................................................................................................... 8 Conclusions ..................................................................................................................................... 23 CHAPTER III .................................................................................................................................................. 25 TREATING CATTLE WITH ANTIBIOTICS AFFECTS GREENHOUSE GAS EMISSIONS, AND MICROBIOTA IN DUNG AND DUNG BEETLES. .................................................................................................................. 25 Abstract ........................................................................................................................................... 25 Introduction .................................................................................................................................... 26 Methods .......................................................................................................................................... 28 Results and Discussion .................................................................................................................... 31 Conclusions ..................................................................................................................................... 37 CHAPTER IV .................................................................................................................................................. 38 METAMORPHOSIS OF A BUTTERFLY-ASSOCIATED BACTERIAL COMMUNITY ...................................... 38 Abstract ........................................................................................................................................... 38 Introduction .................................................................................................................................... 39 Methods .......................................................................................................................................... 42 Results ............................................................................................................................................. 45 vi Discussion ....................................................................................................................................... 49 Conclusions ..................................................................................................................................... 53 CHAPTER V ................................................................................................................................................... 55 CATERPILLARS LACK A RESIDENT GUT MICROBIOME ........................................................................... 55 Abstract ........................................................................................................................................... 55 Introduction .................................................................................................................................... 56 Results ............................................................................................................................................. 58 Discussion ....................................................................................................................................... 63 Methods .......................................................................................................................................... 67 CHAPTER VI .................................................................................................................................................. 69 CONCLUSIONS ....................................................................................................................................... 69 REFERENCES ................................................................................................................................................. 70 APPENDIX ................................................................................................................................................... 105 CHAPTER III APPENDIX .................................................................................................................. 106 CHAPTER IV APPENDIX.................................................................................................................. 113
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