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Genome Evolution During Development of Symbiosis in Extracellular Mutualists of Stink Bugs (Pentatomidae) DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Alejandro Otero-Bravo Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2020 Dissertation Committee: Zakee L. Sabree, Advisor Rachelle Adams Norman Johnson Laura Kubatko Copyrighted by Alejandro Otero-Bravo 2020 Abstract Nutritional symbioses between bacteria and insects are prevalent, diverse, and have allowed insects to expand their feeding strategies and niches. It has been well characterized that long-term insect-bacterial mutualisms cause genome reduction resulting in extremely small genomes, some even approaching sizes more similar to organelles than bacteria. While several symbioses have been described, each provides a limited view of a single or few stages of the process of reduction and the minority of these are of extracellular symbionts. This dissertation aims to address the knowledge gap in the genome evolution of extracellular insect symbionts using the stink bug – Pantoea system. Specifically, how do these symbionts genomes evolve and differ from their free- living or intracellular counterparts? In the introduction, we review the literature on extracellular symbionts of stink bugs and explore the characteristics of this system that make it valuable for the study of symbiosis. We find that stink bug symbiont genomes are very valuable for the study of genome evolution due not only to their biphasic lifestyle, but also to the degree of coevolution with their hosts. i In Chapter 1 we investigate one of the traits associated with genome reduction, high mutation rates, for Candidatus ‘Pantoea carbekii’ the symbiont of the economically important pest insect Halyomorpha halys, the brown marmorated stink bug, and evaluate its potential for elucidating host distribution, an analysis which has been successfully used with other intracellular symbionts. We find that while increased mutation rates are present, the symbiont loci are not as effective as host loci for these studies. In Chapter 2 we sequenced and analyzed the genomes of four tropical stink bug symbionts belonging to the genus Edessa. The four symbionts show similar levels of genome reduction, reaching 0.8 Mb, five times smaller than the closest free-living relative and over 20% smaller than the genome of P. carbekii. Additionally, we show that they display signatures of amino acid supplementation for their host and that these are a distinct clade from P. carbekii, indicating convergence in many genomic traits of the symbiosis. Chapter 3 expands on chapter 2 by describing 11 more genomes of stink bug symbionts with varying degrees of genome reduction, ranging from those of the previously described symbionts of Edessa to genomes equal in size to their free-living relatives. We identify the multiple stages of genome reduction, including an initial massive pseudogenization, followed by progressive degeneration of metabolic pathways including those involved in cell wall components and amino acid biosynthesis. ii Finally, Chapter 4 explores a problem with the study of the phylogenetic relatedness of genome reduced symbionts, long branch attraction artifacts, which is prevalent in many of these studies and can have profound implications in addressing the convergence of these traits. We show that our method to identify and analyze separately taxa prone to LBA can address this issue and perform similarly to more sophisticated but also more computationally expensive methods. iii This dissertation is dedicated to my parents and my grandparents iv Acknowledgments This dissertation was possible thanks to the help of many individuals. First, I would like to thank my advisor, Zakee Sabree for taking me as his student and dedicating a great amount of time, resources, and patience to my training. The opportunity to move to Columbus from Colombia was incredible and will likely be one of the most important events not just professionally, but in all aspects of my life; I am deeply thankful to him for it. I would also like to thank him for his guidance early in my program, his constant enthusiasm, and the freedom he gave me to explore both this system and to learn skills outside of the lab’s focus throughout these last few years. I thank my fellow lab mates, past and present, particularly Ben Jahnes and Arturo Vera Ponce de León, for all their help throughout the years and their kindness and willingness to help and discuss my research. I thank my committee members Rachelle Adams, Laura Kubatko, and Norm Johnson for their input during this project, as well as Shana Goffredi, a member of my Candidacy Committee, who has been vital to this project through samples, discussion, and feedback. I also thank the department of EEOB and GEES for their camaraderie, feedback, and mentorship during the program, especially Megan v Smith, Ben Stone, Becca Dillon, and Amara Huddleston. I am deeply thankful to Corey Ash and Chanelle Kinney from the main office, who were exceptional at helping me navigate the complex university bureaucracy. I acknowledge COLCIENCIAS for the funding that allowed me to focus on my research. Also, CONAGEBIO and The Organization of Tropical Studies, the staff and crew at La Selva, as well as Liz Clifton for their support during my fieldwork, the College of Arts and Sciences Unity cluster at OSU for computational resources. I acknowledge the amazing work of Laura Kenyon and Kalia Bistolas on stink bug symbionts, which has been at the core of this work from the beginning. I thank Tim Haye, Don Weber, Michael Toews, Celeste Welty, and the countless people willing to part with stink bugs from their colonies for the samples they donated to this project. Finally, I cannot thank my family enough for their love, understanding, and support in spite of the distance. They have done more for me than I can list, even during my prolonged absence. Everything I have and will ever achieve is dedicated to my parents and grandparents. I could only take on this giant project because they ensured I could fully dedicate to my studies, supported and encouraged me constantly, and have always celebrated even my smallest achievements. To my partner Mark, I cannot thank you enough for your support, encouragement, and the structure you have given my life since we met. Thank you all for everything. vi Vita 2015.............................................................B.S. Biology, Universidad de los Andes 2015.............................................................B.S. Microbiology, Universidad de los Andes 2015-2016 ...................................................Graduate Fellow, The Ohio State University 2017-2019 ...................................................Graduate Teaching Associate Department of Evolution, Ecology and Organismal Biology, The Ohio State University Publications Otero-Bravo A, Sabree ZL. 2018. Comparing the utility of host and primary endosymbiont loci for predicting global invasive insect genetic structuring and migration patterns. Biol. Control. 116:10–16. doi: 10.1016/j.biocontrol.2017.04.003. Otero-Bravo A, Goffredi S, Sabree ZL. 2018. Cladogenesis and Genomic Streamlining in Extracellular Endosymbionts of Tropical Stink Bugs. Genome Biol. Evol. 10:680– 693. doi: 10.1093/gbe/evy033. Otero-Bravo A, Sabree ZL. 2015. Inside or out? Possible genomic consequences of extracellular transmission of crypt-dwelling stinkbug mutualists. Front. Ecol. Evol. 3:1–7. doi: 10.3389/fevo.2015.00064. Fields of Study Major Field: Evolution, Ecology and Organismal Biology vii Table of Contents Abstract ................................................................................................................................ i Acknowledgments............................................................................................................... v Vita .................................................................................................................................... vii Publications ................................................................................................................... vii Fields of Study .............................................................................................................. vii Table of Contents ............................................................................................................. viii List of Tables .................................................................................................................... xii List of Figures .................................................................................................................. xiii Chapter 1 Introduction: Inside or out? Possible genomic consequences of extracellular transmission of crypt-dwelling stink bug mutualists .......................................................... 1 Abstract ........................................................................................................................... 1 Introduction ..................................................................................................................... 2 Who are the stink bugs? .................................................................................................. 3 Transmission strategies ................................................................................................... 4 Coevolution ....................................................................................................................
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