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THESIS SPATIAL, DEMOGRAPHIC, and PHYLOGENETIC PATTERNS of BARTONELLA DIVERSITY in BATS Submitted by Clifton Dyer Mckee Graduate

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THESIS SPATIAL, DEMOGRAPHIC, and PHYLOGENETIC PATTERNS of BARTONELLA DIVERSITY in BATS Submitted by Clifton Dyer Mckee Graduate THESIS SPATIAL, DEMOGRAPHIC, AND PHYLOGENETIC PATTERNS OF BARTONELLA DIVERSITY IN BATS Submitted by Clifton Dyer McKee Graduate Degree Program in Ecology In partial fulfillment of the requirements For the Degree of Master of Science Colorado State University Fort Collins, Colorado Summer 2015 Master’s Committee Advisor: Colleen T. Webb Michael Y. Kosoy W. Chris Funk Tony Schountz David T. S. Hayman Copyright by Clifton Dyer McKee 2015 All Rights Reserved ABSTRACT SPATIAL, DEMOGRAPHIC, AND PHYLOGENETIC PATTERNS OF BARTONELLA DIVERSITY IN BATS Much recent attention has focused on bats as potentially exceptional reservoirs of pathogens. Bats are known to carry zoonotic viruses deadly to humans with no apparent signs of pathology, however the evolutionary and physiological processes that are behind this ability remain largely unknown. Despite this uncertainty, bats’ long lifespans, deep evolutionary history, sociality, and migratory behavior make them a fascinating system in which to study patterns of diversity in viruses, bacteria, and other infectious organisms. This thesis explores ecological and evolutionary processes that structure the diversity of infectious bacteria in bats. I focus on Bartonella, a genus of vector-borne intracellular bacteria, because of its high prevalence and genetic diversity within bats. I examined the structure of Bartonella species assemblages in Eidolon spp. fruit bats across Africa and Madagascar using newly developed molecular and statistical tools. The results from this examination indicate that fruit bats from distant geographic locations host similar communities of Bartonella; I attribute this to widespread dispersal and communal roosting behavior in Eidolon spp. bats. To understand how Bartonella diversity has evolved and is structured geographically, I assembled a global dataset of Bartonella genotypes from bats and their ectoparasites. Using this dataset, I analyzed the contributions of cospeciation and sympatry among host species to the diversity of Bartonella in bats. Continued development of this research could provide a model system for the study of ecological and evolutionary processes contributing to pathogen diversification and infection dynamics in natural systems. ii ACKNOWLEDGMENTS I am deeply indebted to a number of people for their guidance and support during my work on this thesis. I am grateful for the training and mentorship that Michael Kosoy, Ying Bai, and Lynn Osikowicz have given me in the lab at the Centers for Disease Control (CDC) Division of Vector-Borne Diseases (DVBD). This project would have been impossible without their patience and direction. I sincerely thank David Hayman for his continued insights on bats, bacterial evolution, and everything in between. I have been fortunate to work with such a dedicated and passionate scientist. I appreciate the number of collaborators that have contributed samples to this work including Cara Brook, Ivan Kuzmin, Alison Peel, and Richard Suu-Ire. I owe enormous praise to my advisor Colleen Webb, who has helped me to advance as a scientist and academic, and has greatly influenced the scope and purpose of this thesis. I also thank additional members of my committee, the Webb and Kosoy labs, and other collaborators that have provided valuable input during the development of this work. I must also give thanks to numerous people cheering for me along the way. To my family, I am forever grateful for your love and advice throughout my academic career; I would not be where I am now without you. To my friends, I am abundantly grateful for your encouragement and the perspective achieved from a shared glass of beer, a long run, and some time away from the computer screen. Finally, I am lucky to have the support of my partner, Ava Hoffman, who has been my councilor, editor, and exuberant cheerleader throughout this work. Materials and laboratories facilities for experiments were provided by the CDC DVBD Bacterial Diseases Branch. This work was partially supported by the Wellcome Trust and the Research and Policy for Infectious Disease Dynamics (RAPIDD) program of the Science and iii Technology Directorate (US Department of Homeland Security) and the Fogarty International Center (NIH). iv TABLE OF CONTENTS Abstract ........................................................................................................................................ii Acknowledgements ......................................................................................................................iii List of tables .................................................................................................................................vii List of figures ...............................................................................................................................viii Chapter 1: Generation and maintenance of Bartonella diversity in bats .....................................1 Chapter 2: Phylogeography of Bartonella bacteria in Eidolon spp. fruit bats across Africa.......5 Introduction ............................................................................................................................5 Materials and methods ...........................................................................................................9 Study system ....................................................................................................................9 Sample collection .............................................................................................................10 DNA extraction and PCR amplification ..........................................................................11 Sequencing and Bartonella species identification ...........................................................13 Modelling Bartonella species abundance from multiple primers ....................................14 Modelling Bartonella species phylogeography ...............................................................16 Statistical analysis of bartonella prevalence ....................................................................17 Results ....................................................................................................................................18 Sequencing and Bartonella species identification ...........................................................18 Multiple primer model .....................................................................................................19 Phylogeography model ....................................................................................................20 Logistic models of bartonella prevalence ........................................................................21 Discussion ..............................................................................................................................23 References ..............................................................................................................................41 Chapter 3: Phylogenetic and geographic constraints on Bartonella transmission among bat species ..........................................................................................................................................47 Introduction ............................................................................................................................47 Materials and methods ...........................................................................................................50 Compiled sequence data ..................................................................................................50 Compiled geographic range data .....................................................................................52 Phylogenetic analysis of sequence data ...........................................................................52 Correlation between bat phylogeny and sympatry...........................................................53 Tests of cophylogeny .......................................................................................................54 Global fit tests ..................................................................................................................54 Bayesian phylogenetic analysis and reconstruction of host switches ..............................55 Results ....................................................................................................................................57 Phylogenetic analysis .......................................................................................................57 Correlation between bat phylogeny and sympatry...........................................................57 Global fit tests ..................................................................................................................58 Bayesian phylogenetic analysis and reconstruction of host switches ..............................59 Discussion ..............................................................................................................................62 References ..............................................................................................................................78 Chapter 4: Concluding remarks and future directions .................................................................82 Appendices ...................................................................................................................................86 v Appendix I: Supplementary materials for Chapter 2 .............................................................86
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