Individual Host to Population Scale Dynamics of Parasite Assemblages in African Buffalo of Kruger National Park, South Africa
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AN ABSTRACT OF THE DISSERTATION OF Caroline Kate Glidden for the degree of Doctor of Philosophy in Integrative Biology presented on June 1, 2020. Title: INDIVIDUAL HOST TO POPULATION SCALE DYNAMICS OF PARASITE ASSEMBLAGES IN AFRICAN BUFFALO OF KRUGER NATIONAL PARK, SOUTH AFRICA Abstract approved: ___________________________________________________________ Anna E. Jolles The last century has experienced a marked increase in emerging infectious disease (EID, hereafter) – jeopardizing human, domestic animal, and wildlife health. EIDs are commonly associated with spillover from one host species into a novel host species, with many destructive diseases, for both livestock and wildlife, emerging at the wildlife- livestock interface. As global change continues to erode the boundaries between human and wildlife systems, it will become increasingly more important to understand the key components influencing host susceptibility as well as pathogen/parasite spread and persistence. However, understanding disease systems, especially within wildlife, is complex, as processes at multiple scales of biological organization are relevant to pathogen/parasite dynamics. At the within-host scale, pathogens interact with host cells and co-infecting pathogens, and these within-host dynamics affect host susceptibility, infectious period, and pathogen transmission potential. At the host population-level scale, heterogeneity across hosts as well as pathogen dispersal between hosts interacts with within-host processes to ultimately influence the distribution of infectious agents within-hosts, across hosts, and over time. Studying disease in natural systems enables researchers to observe the outcome of interactions of numerous multi-scale sources of variation and predict realistic parasite/pathogen dynamics. Ultimately, this work should enable the development of adaptive disease management. For my PhD dissertation, I explored how within-host patterns and processes inform population-level patterns in African buffalo (Syncerus caffer) of Kruger National Park (KNP), South Africa. Specifically, I studied infectious agents associated with two diseases that infect cattle and buffalo at the South African wildlife-livestock interface: the bovine respiratory disease complex and theileriosis. In Chapter 2, I found that evolutionarily conserved immune responses (i.e., non-specific inflammatory response) can be used to detect disease exposure without a priori knowledge of pathogen identity – a tool than can be further developed for EID surveillance. In Chapter 3, I weighed the effect of host traits, pathogen co-occurrence and environmental variability on probability of infection by viral and bacterial pathogens within the bovine respiratory disease complex as well as characterized temporal trends in pathogen incidence. I found that the importance of each factor was inconsistent across pathogens – co-occurrence was the best indicator of virus occurrence whereas host ID was the best indicator of bacterial infection. Importantly, I found that within-host dynamics only partially elucidated seasonal cycling in population-level disease dynamics. In Chapter 4, I developed molecular methods to quantify cryptic spatio-temporal variation in vector-borne, hemoparasite (Theileria: the etiological agent of theileriosis) assemblages of African buffalo. In Chapter 5, I used the high resolution data from Chapter 4 to describe the structure of Theileria assemblages within and across hosts, in both space and time. Chapter 5 uses novel analytical approaches to distill complex Theileria assemblages into functional groups based upon their life-history patterns. This characterization enabled me to estimate the relative importance of dispersal and host heterogeneity on distribution of these parasites thereby enabling me to predict efficacy and side-effects of vector-borne disease management tools. ©Copyright by Caroline Kate Glidden June 1, 2020 All Rights Reserved INDIVIDUAL HOST TO POPULATION SCALE DYNAMICS OF PARASITE ASSEMBLAGES IN AFRICAN BUFFALO OF KRUGER NATIONAL PARK, SOUTH AFRICA by Caroline Kate Glidden A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented June 1, 2020 Commencement June 2021 Doctor of Philosophy dissertation of Caroline Kate Glidden presented on June 1, 2020 APPROVED: Major Professor, representing Integrative Biology Head of the Department of Integrative Biology Dean of the Graduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Caroline Kate Glidden, Author ACKNOWLEDGEMENTS Anna, thank-you for your dedicated mentorship and guidance throughout my PhD. Thank-you for providing me with the opportunity to be involved in so many different research projects as well as always supporting my many intellectual pursuits. Thank-you for providing me the opportunity to live and do fieldwork in Kruger National Park, South Africa as well as the encouragement to collaborate with the University of Melbourne (and live in Melbourne, Australia for a year). I can’t imagine a better (or more fun) graduate school experience. Thank-you to the National Science Foundation, Achievement Rewards for College Scientists, and University of Melbourne for funding this work. I also thank my graduate committee: Dave Lytle, Jan Medlock, Virginia Lesser, and Taal Levi. Thank- you for your input on this work at its multiple stages of development. Your constructive comments were helpful and much appreciated. Thank-you members of the Jolles Lab, past and present, for support and feedback on my work throughout graduate school. Special thanks to Dr. Brianna Beechler for leading the FMDV field project as well as providing me many more research projects and opportunities to travel back to South Africa. Thank-you Dr. Hannah Tavalire for being an amazingly supportive mentor and friend, and for always going above and beyond to provide me feedback on analyses, grants and manuscripts. Thank-you Dr. Michelle Steinauer for providing thoughtful guidance, even though our schistosome manuscript didn’t make it into my dissertation. Thank-you members of the Jabbar Lab and Gasser Lab for being such wonderful hosts while I was at the University of Melbourne – and for kindly teaching me so many different laboratory techniques and protocols. Thank-you South Africa National Parks, especially the Veterinary Wildlife Services and Game Capture Team. This work would not have been possible without you. Thank-you Drs. Lindsay Biga, Lori Kayes, Carmen Harjoe, and Devon Quick for providing unparalleled teaching support and guidance. I cannot imagine graduate school without the unwavering support of so many compassionate, smart, and fun friends: Vanessa Constant, Hannah Tavalire, Carmen Harjoe, Tim Schrautemeier, Trang Weitemier, Miram Gleiber, Alissa Rickborn, Ashely Friedland, Kaylyn Bopp, Megan Page, Claire Taylor, and Shannon Mason. Special thanks to Vanessa Constant for always lending an ear, keeping me laughing, and keeping me optimistic. Thank-you Kris and Margaret T. Bauer for your unconditional support. Finally and foremost, thank-you to my family: Sarah-Kate, Peter, Diana, Sean, Rachael, Nicolette, Luke, Sage, and Cole. Grandad and Grandma, thank-you for instilling in me a love of wildlife and travel. Rachael, Nicolette, Luke thank-you for always being forgiving and always being there for me. Mom, thank-you for always being proud of my accomplishments, encouraging my dreams, and being such an amazing role model. CONTRIBUTION OF AUTHORS Chapter 2: Caroline K. Glidden led analyses and writing and was involved in field work and laboratory work; Anna Jolles was project PI, PhD advisor to CG, involved in study conceptualization, field work, lab work and manuscript writing; Bree Beechler was involved in study conceptualization, field work, lab work, analyses; Peter Buss was scientific liaison for South African National Parks Veterinary Wildlife Services; Bryan Charleston was project PI for the Pirbright Institute, involved in project design and lab work; Lin-Mari de Klerk-Lorist was a state veterinarian involved in project design and leading the experimental study; Francois Maree was involved in diagnostic lab work, experimental study design and implementation; Timothy Muller was involved in analysis of data from the FMDV experiment; Eva Pérez-Martin was involved in field work, lab work; Katherine Scott was involved in field work, lab work; Ockert Louis van Schalkwyk was a state veterinarian involved in project design and leading the experimental study. Chapter 3: Caroline K. Glidden led analyses and writing and was involved in study conceptualization and laboratory work; Anna Jolles was project co-PI, PhD advisor to CG, involved in study conceptualization, field work, lab work and manuscript writing; Courtney Coon was involved in study conceptualization, analyses, and manuscript writing; Bree Beechler was involved in field work and lab work; Chase McNulty was involved in laboratory work; Vanessa Ezenwa was project co-PI, involved in field work, lab work and manuscript writing. Chapter 4: Caroline K. Glidden was involved in study design, field work, laboratory work and led bioinformatics, phylogenetic, and community analyses as well as manuscript preparation. Anna E. Jolles led the field study design, contributed towards manuscript preparation and acted as mentor to CKG. Anson