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Hamiltonella Defensa-Acyrthosiphon Pisum System As a Model For MATRYOSHKA MUTUALISMS: DEVELOPING THE BACTERIOPHAGE APSE- HAMILTONELLA DEFENSA-ACYRTHOSIPHON PISUM SYSTEM AS A MODEL FOR TRIPARTITE SYMBIOSES by STEPHANIE RAY WELDON (Under the direction of Kerry M. Oliver) Viruses are the most abundant, most diverse, and least understood organic structures on earth. While the best-studied viruses are pathogenic, many viruses engage in commensal or even mutualistic relationships with eukaryotes. In the pea aphid, Acyrthosiphon pisum, a facultative bacterial mutualist, Hamiltonella defensa, provides anti-hymenopteran parasitoid defense only when it is itself infected by virus APSE (Acyrthosiphon pisum Secondary Endosymbiont). While this is the only known instance of mutualism-by-proxy, the prevalence of mobile genetic elements in symbionts makes it unlikely that it will be the last. At present, however, the diversity, prevalence, and effects of viruses infecting insect-associated bacteria are largely unknown. I conducted four studies to elucidate the biology of the tripartite aphid/H. defensa/APSE interaction. Firstly, within-host bacterial abundance can affect conferred phenotypes and rates of transmission. All stable beneficial heritable symbiont infections must have sufficient titer to produce the beneficial phenotype and ensure vertical transmission to progeny, without engaging in over-replication that might affect host fitness. Using quantitative- PCR and standard fitness tests, I determined that in the absence of APSE H. defensa replicates at rates detrimental to its host’s development and reproduction. Secondly, previous sampling of North American APSEs in A. pisum was limited to a handful of samples from two New York counties and one in Utah. I tested more than 1100 aphids from six states for H. defensa presence and phage strain identity: in the process I identified a new strain of APSE, called APSE-8, and I present its associated defensive phenotype here. Thirdly, most studies examine effects of single heritable symbiont infection, but ~25% of individual aphids carry multiple facultative symbiont lineages despite previous reports of lower fidelity in the transmission of double infections and additional costs to hosts of superinfection I created artificially differentially-infected clonal lineages using H. defensa and its sister species, the anti-fungal defender Regiella insecticola, and determined that, under most conditions, coinfection is actually beneficial. Finally, I present the first pass at parsing aphid transcriptional responses to wasp parasitism in the presence and absence of aphid genotypic resistance and H. defensa- induced resistance, finding little-to-no evidence for the mobilization of innate immunity. INDEX WORDS: Symbiosis, bacteriophage, parasitoid, natural selection, microbial ecology MATRYOSHKA MUTUALISMS: DEVELOPING THE BACTERIOPHAGE APSE- HAMILTONELLA DEFENSA-ACYRTHOSIPHON PISUM SYSTEM AS A MODEL FOR TRIPARTITE SYMBIOSES by STEPHANIE RAY WELDON B.Sc., Emory University, 2009 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2015 © 2015 Stephanie Ray Weldon All Rights Reserved MATRYOSHKA MUTUALISMS: DEVELOPING THE BACTERIOPHAGE APSE- HAMILTONELLA DEFENSA-ACYRTHOSIPHON PISUM SYSTEM AS A MODEL FOR TRIPARTITE SYMBIOSES by STEPHANIE RAY WELDON Major Professor: Kerry Oliver Committee: Michael Strand Jacob Russell Eric Stabb Electronic Version Approved: Suzanne Barbour Dean of the Graduate School The University of Georgia December 2015 DEDICATION I dedicate this dissertation to my parents, Walt and Cindy Weldon: without their near- three decades of support, the odds that I would have stuck it out in science are slim. They taught me to prioritize the process of learning, while also exhorting me to put down the books and get outside on occasion. I still prefer my insects mashed in TRIzol at a lab bench, but my parents ensured I would never forget that my work is part of a wider world. I would also like to dedicate this work to my younger brother, Jon, who is terrified of insects. I took up entomology primarily to taunt him. iv ACKNOWLEDGEMENTS I would like to thank the Entomology Department at the University of Georgia as a whole: my graduate career was immensely well-supported by social and professional interactions with my fellow students, by excellent advising from every professor I interacted with, and by the hard work of our office staff. I would also like to thank all members, current and former, of the Oliver lab: Kerry first and foremost, for putting as much time into editing my writing projects as I did into writing them, and for always encouraging me to follow up on whatever area of research I found most interesting, and to develop my own plans. Second in order but not importance are our current lab manager Kyungsun Kim and our former lab manager Nasreen Bano, who is/was the only reason the lab survives on a day-to-day basis. Every graduate student who has come through the Oliver lab has helped me with my projects, but I would like to particularly thank Adam Martinez, Jayce Brandt, and Hannah Dykstra for making major contributions to my understanding of the system we all work in. I’d also like to thank my REU student Erin Smith, my final project mentees Jimmy Quijada and Pooja Patel, and my YSP student Jordan Harris, for teaching me far more than I taught them. I would like to acknowledge my committee member Eric Stabb’s contributions to this whole dissertation at the prospectus stage, and also Mike Strand, Kevin Vogel, and Gaelen Burke, without whom there would be no transcriptome project, and Jake Russell and Drew Smith, without whom there would be neither a diversity nor a coinfection project. Piotr Lukasik also contributed significantly to the early development of my diversity survey chapter. Finally I would like to thank the NSF (awards 1050128 and 1256794), USDA-NIFA (award 25-21-RC293-620), the UGA Graduate School, and the Department of Entomology for the funding support I needed to actually do this work. v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ........................................................................................................... v LIST OF TABLES ....................................................................................................................... ix LIST OF FIGURES ..................................................................................................................... x CHAPTER 1. INTRODUCTION AND LITERATURE REVIEW ........................................................... 1 1.1 Summary .......................................................................................................1 1.2 Introduction ....................................................................................................3 1.3 The role of phage in an aphid defensive mutualism ..................................... 10 1.4 WO phage of Wolbachia spp. ....................................................................... 20 1.5 Bacteriophage roles in the evolution of heritable symbiont genomes ........... 23 1.6 Future directions in insect-associated phage research ................................. 25 1.7 Concluding remarks ..................................................................................... 32 1.8 Acknowledgements ...................................................................................... 33 1.9 References .................................................................................................. 33 2. PHAGE LOSS AND THE BREAKDOWN OF A DEFENSIVE SYMBIOSIS IN APHIDS ............................................................................................................. 51 2.1 Abstract ........................................................................................................ 52 2.2 Introduction .................................................................................................. 52 2.3 Materials and methods ................................................................................. 54 2.4 Results ......................................................................................................... 60 2.5 Discussion ................................................................................................... 62 2.6 Acknowledgements ...................................................................................... 65 vi 2.7 References and notes .................................................................................. 65 3. DIVERSITY, FREQUENCY, AND PHENOTYPES OF PHAGE INFECTIONS IN AN APHID BACTERIAL MUTUALISM ..................................................................... 70 3.1 Abstract ........................................................................................................ 71 3.2 Introduction .................................................................................................. 71 3.3 Methods ....................................................................................................... 75 3.4 Results ......................................................................................................... 80 3.5 Discussion ................................................................................................... 88 3.6 Acknowledgements ...................................................................................... 92 3.7 References .................................................................................................. 92 4. COSTS AND
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