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Ecology and Evolution of Malarial Parasites In ECOLOGY AND EVOLUTION OF MALARIAL PARASITES IN VERTEBRATE HOSTS A Dissertation Presented to the Faculty of the Graduate School Of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy By Holly Lynn Lutz August 2016 © Holly Lynn Lutz 2016 ECOLOGY AND EVOLUTION OF MALARIAL PARASITES IN VERTEBRATE HOSTS Holly Lynn Lutz, Ph.D. Cornell University 2016 This dissertation represents a culmination of extensive field work and collections of African vertebrates and their symbionts, as well as experimental studies carried out in the laboratory. Field work was conducted primarily in the East African countries of Kenya, Malawi, Mozambique, and Uganda. Throughout these expeditions, efforts were made to improve field protocols for the comprehensive sampling of wild vertebrates and their symbionts, with particular focus on the sampling of avian blood parasites (haematozoa), ectoparasites (arthropods), endoparasites (helminths), and microbial symbionts (bacteria and viruses). This dissertation therefore includes a chapter with detailed guidelines and protocols for sampling avian symbionts based on these experiences. Following chapters rely on data from both field collections and laboratory experiments, which provide a foundation for addressing the ecology, systematics, and molecular evolution of malarial parasites in vertebrate hosts. Specifically, haemosporidian data from 2,539 Afrotropical birds and small mammals (bats, rodents, and shrews) collected during field inventories were used to (1) test hypotheses linking host life history traits and host ecology to patterns of infection by three haemosporidian parasite genera in birds (Plasmodium, Haemoproteus, and Leucocytozoon), and (2) re-evaluate the molecular phylogeny of the order Haemosporida by incorporating existing genomic data from haemosporidian parasites with data from novel parasite lineages infecting major vertebrate host groups, including birds, mammals, and reptiles. In addition to these studies of host–parasite ecology and parasite phylogeny, this dissertation includes an experimental demonstration of the utility of laser microdissection microscopy techniques as a tool for acquiring the DNA of four avian parasites (Plasmodium relictum, P. homocircumflexum, P. ashfordi, and P. cathemerium) from nucleated red blood cells of avian hosts. Experimental data derived from the application of laser microdissection microscopy techniques were subsequently combined with genomic data provided by the Wellcome Trust Sanger Institute to examine the extent to which positive Darwinian selection has shaped the evolution of gene families involved in the invasion of host cells and evasion of host immune response by the avian malarial parasite, Plasmodium relictum (lineage pSGS1). This dissertation improves our understanding of the effects of host ecology and life history on patterns of infection by haemosporidian parasites in Afrotropical birds. Life history traits such as nest type, nest height, and flocking behavior in birds have significant effects on the prevalence of malaria infection in vertebrate hosts. Phylogenetic analyses of novel parasite lineages, collected and identified from East African vertebrates, show that the evolutionary history of haemosporidian parasites involves host shifts between major vertebrate host groups, and that bats were likely the first mammals to acquire haemosporidian parasites from a sauropsid-infecting ancestor. Subsequent transitions from bats to other non-chiropteran mammals appear to have led to the extant diversity of haemosporidian parasites infecting primates and rodents. This phylogenetic hypothesis has important implications for the evolution of life history traits in haemosporidian parasites themselves, including the production of haemozoin pigment (a byproduct of haemoglobin digestion), and erythrocytic schizogony (asexual reproduction in host red blood cells). BIOGRAPHICAL SKETCH Holly Lutz was born in Altus, OK at the Altus Air Force Base. For the next five years, she moved between Oklahoma, North Dakota, and Texas, until settling in Fort Worth with her parents and siblings. Following three years of attending public schools, Holly was homeschooled for four years, after which she attended Nolan Catholic high school for grades 7–12. She began attending the University of Chicago in the fall of 2005, and received her BA in the Biological Sciences with a specialization in Ecology and Evolutionary Biology in 2009. During her time as an undergraduate, Holly worked in the marine science laboratories of Drs. Tim Wootton and Cathy Pfister, and spent several months as an assistant to Drs. Wootton, Pfister, and Robert Paine in the Pacific Northwest. There, she contributed to projects on Tatoosh Island and along the rocky intertidal of the Strait of Juan de Fuca. Following these experiences, she transitioned to working with the Field Museum of Natural History in Chicago, where she acquired extensive experience in bird and mammal specimen preparation, molecular lab work, and international field work. From 2009–2011, Holly worked as a member of the Emerging Pathogens Project at the Field Museum, completing three international expeditions to Africa and South America, and contributing to the collection of several thousand bird, mammal, and symbiont specimens for the Field Museum. It was during this time, and from examining these specimens, that Holly developed a keen interest in malarial parasites of wild birds and mammals. She carried this interest in malarial parasite ecology and evolution with her to Cornell in the fall of 2011, and it thus became the topic of her dissertation. iii DEDICATION To Elliot, Lauren, and Tycho To allow mystery, which is to say to yourself, “There could be more, there could be things we don’t understand,” is not to damn knowledge. It is to take a wider view. It is to permit yourself an extraordinary freedom: someone else does not have to be wrong in order that you may be right. - Barry Lopez (Of Wolves and Men) iv ACKNOWLEDGEMENTS My graduate committee has served as a great source of intellectual stimulation and academic guidance during my development as a scientist. I am incredibly grateful to my committee as a whole for allowing me to operate independently, while remaining available for guidance and support throughout the duration of my PhD. In particular, I thank Drs. André Dhondt and Michael Stanhope for co-chairing my committee and reviewing myriad drafts of manuscripts and proposals, always with constructive criticism, useful feedback, and great patience. I also thank Dr. Wesley Hochachka for his ever-present kindness, support, and patience as I navigated my PhD and developed my research ideas. Countless hours spent discussing general ideas or specific models helped me remain grounded and productive, particularly in the earliest stages of my dissertation. I am grateful to Dr. Irby Lovette for making available or drawing my attention to many important resources that have allowed me to effectively pursue my research. I am particularly grateful for his dedication to various aspects of ornithology-related activities, including the annual Ornithology Seminar series, and myriad Lab of Ornithology events in which he invited me to participate. Dr. Lovette’s encouragement of my participation in such events has played a very important role in both my development as a scientific communicator, and in the development of my general knowledge of avian biology. Last but not least, I am grateful for the enthusiastic encouragement and support of Dr. John Fitzpatrick, without whom I might not have applied to the graduate program at Cornell. Through a chance encounter in Chicago, I discovered Dr. Fitzpatrick’s shared passion for natural history and museums, which led me to apply for graduate study at Cornell. This understanding has v continually provided me with a strong sense of belonging in an academic setting that is incredibly diverse, and Dr. Fitzpatrick’s encouragement of independence in his students has allowed me to pursue a scientific path which otherwise might have seemed unattainable. I thank my parents for their selfless dedication to my early education, and my many friends around the world for their good humor and support as I’ve navigated my graduate program. My studies and research at Cornell were intertwined with my work at the Field Museum of Natural History in Chicago, and I would like to thank the many friends and ‘family’ at FMNH with whom I have worked over the years and during my PhD. Drs. Shannon Hackett, John Bates and Jason Weckstein were crucial in steering me towards a research career. Before meeting and working with them, I had not realized that research was an option, having come from a very different background. I am incredibly grateful for the friendship and support of Dr. Kevin Feldheim, Erica Zahnle, Brian Wray, and Josh Engel as I have worked my way through myriad laboratory, field, and life experiments. I thank Drs. Julian Kerbis, Bruce Patterson, Ben Marks, and Corrie Moreau for their friendship, mentorship, and support as I have pursued scientific-collecting and museum-based research. I will be forever grateful to Mary Hennen and Dr. Dave Willard for their patience, kindness, and friendship for as long as I had been a nuisance at the museum. Lastly, I would not be where I am as a scientist and field biologist without the guidance, encouragement, epic friendship and love of Thomas Gnoske, who permanently altered the course of my life on the day he taught me how to
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