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Pagos Birds and Their Parasites Noah Kerness Whiteman University of Missouri-St

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Pagos Birds and Their Parasites Noah Kerness Whiteman University of Missouri-St University of Missouri, St. Louis IRL @ UMSL Dissertations UMSL Graduate Works 5-2-2006 Evolutionary epidemiology of endemic Gal¿pagos birds and their parasites Noah Kerness Whiteman University of Missouri-St. Louis, [email protected] Follow this and additional works at: https://irl.umsl.edu/dissertation Part of the Biology Commons Recommended Citation Whiteman, Noah Kerness, "Evolutionary epidemiology of endemic Gal¿pagos birds and their parasites" (2006). Dissertations. 610. https://irl.umsl.edu/dissertation/610 This Dissertation is brought to you for free and open access by the UMSL Graduate Works at IRL @ UMSL. It has been accepted for inclusion in Dissertations by an authorized administrator of IRL @ UMSL. For more information, please contact [email protected]. University of Missouri-St. Louis Department of Biology Program in Evolution, Ecology and Systematics Evolutionary Epidemiology of Endemic Galápagos Birds and their Parasites by Noah Kerness Whiteman M.S., Entomology, University of Missouri-Columbia, 2000 B.A., cum laude Distinction in Biology, Saint John’s University-Minnesota, 1998 Dissertation Advisory Committee: _____________________________ ______________________________ Patricia G. Parker, Ph.D. (Advisor) Elizabeth A. Kellogg, Ph.D. (Chair) _____________________________ ______________________________ Robert J. Marquis, Ph.D. Kevin P. Johnson, Ph.D. (External) _____________________________ Robert E. Ricklefs, Ph.D. A dissertation presented to the Graduate School of Arts and Sciences of the University of Missouri-St. Louis in partial fulfillment of the requirements for the degree of Doctor of Philosophy December 2005 Saint Louis, Missouri 1 Dissertation Abstract In order to better understand parasite diversification, I went to the Galápagos Islands to study the ecology and evolution of a model bird-parasite system, which included four phylogenetically independent ectoparasite lineages infecting the Galápagos Hawk (Aves: Buteo galapagoensis). The parasites comprised two lice (Insecta: Phthiraptera: Amblycera, Ischnocera), a lousefly (Diptera: Hippoboscidae) and an avian skin mite (Acari: Epidermoptidae). Ultimately, my goal was to examine ectoparasite evolutionary epidemiology and disease susceptibility in relation to the host’s ecological and colonization history. At the outset, I hypothesized that parasite natural history was key in influencing the coalescent process. Accordingly, I found differences in prevalence, abundance and degree of aggregation among each hawk ectoparasite species. I proposed using parasite population genetics to infer host history as a new rationale for parasite conservation. In that context, a DNA barcoding approach revealed predictable differences in transmission rates of two Galápagos dove (Zenaida galapagoensis) louse genera to hawks during predation events. A ‘generalist’ mite species from Galápagos hawks and Flightless cormorants (Phalacrocorax harrisi) comprised two cryptic species, one of which was structured genetically between two hawk island populations. The hawk amblyceran and lousefly harbored less population genetic structure than the ischnoceran, which was more differentiated than the host, although isolated populations of both lice contained unique, fixed haplogroups, illuminating cryptic parasite diversity and restricted host gene flow among islands. This variation, however, was only related to host genealogy in the 2 ischnoceran and the rate of molecular evolution was faster in the ischnoceran than in the host. Among islands, hawk inbreeding explained louse infection intensity and natural antibody levels, and the latter was inversely related to amblyceran louse abundance, which encounters the host immune system. Separately from the ectoparasite work, I collaborated on a characterization of Avipoxvirus isolates from Galápagos birds, showing significant recombination among pox strains, and we recovered Haemoproteus-like parasites from multiple seabird species on Genovesa. Finally we showed that a vector of avian disease was established on Isla Santa Cruz (Culex quinquefasicatus). This study was the first to examine host-parasite evolutionary epidemiology within the Galápagos avifauna, one of the most intact and threatened island bird communities. 3 Table of Contents Chapter I: General Introduction………………………………………..………… 10 Chapter II: Using Parasites to Infer Host History…………………..……….……. 22 Chapter III: Body Condition and Parasite Load Predict Territory Ownership in the Galápagos Hawk………………………..……………………..……………............ 48 Chapter IV: Effects of Host Sociality on Ectoparasite Population Biology............ 72 Chapter V: Differences in Straggling Rates Between Two Genera of Dove Lice (Insecta: Phthiraptera) Reinforce Population Genetic and Phylogenetic Patterns…………………………………………………………………..…............. 109 Chapter VI: Disease Ecology in the Galápagos Hawk (Buteo galapagoensis): Host Genetic Diversity Parasite Load and Natural Antibodies………………………….. 134 Chapter VII: Establishment of the Avian Disease Vector Culex quinquefasciatus Say 1823 (Diptera: Culicidae) on the Galápagos Islands, Ecuador…………………….. 164 Chapter VIII: Characterization of Canarypox-like Viruses Infecting Endemic Birds in the Galápagos Islands……………………………………………………………… 177 Chapter IX: Population Genetics of the Galápagos Hawk (Buteo galapagoensis): Genetic Monomorphism within Isolated Populations……………………………… 209 Chapter X: Phylogeography of the Galápagos Hawk (Buteo galapagoensis): A Recent Arrival to the Galápagos Islands…………………………………………………… 242 Chapter XI: Health Assessment of Seabirds on Isla Genovesa, Galápagos Islands……………………………………………………………………………… 281 Chapter XII: Cryptic Host Specificity and Genetic Epidemiology of a Generalist Avian Skin Mite (Acari: Astigmata) from Two Sympatric and Threatened Galápagos 4 Endemic Birds……………………………………………………………………… 310 Chapter XIII: Comparative Population Genetic and Phylogeography of a Model Host- Parasite System from the Galápagos Islands………………………………………. 358 Please note that nine chapters (I through VII, XII and XIII) are manuscripts on which I was first author and for which I was primarily responsible and four chapters (VIII through XI) are manuscripts on which I was a co-author but are directly related to my first-authored chapters. 5 Acknowledgments First, I would like to thank my dissertation advisor, Dr. Patricia G. Parker, for her enthusiasm and steadfast belief in me. I have benefited tremendously as a result of her mentoring and I am thankful for our candid conversations, which have led to many conceptual breakthroughs in the context of my research. Moreover, I thank Dr. Parker for simultaneously taking me under her wing when times were difficult for me, and giving me the freedom to decide on a Ph.D. research topic completely of my choosing, and in a taxonomic group with which she was not directly familiar (at least the parasite half of the equation). Without hesitation and with full intellectual and infrastructural support, she allowed me to utilize her incredibly interesting model research system in the Galápagos (the Galápagos Hawk) in which to ask my dissertation research questions, under the broader rubric of her then new avian disease ecology and evolution study in the archipelago. Dr. Parker sent me to Australia for the Phthiraptera Congress, which was essential to my professional development. She helped channel my extreme and sometimes scattered energy in ways that challenged and benefited me greatly. Dr. Parker encouraged me to publish from day one (and to never give up), which was sound advice. Dr. Parker involved me in her avian pox and Genovesa seabird disease research project, which were great experiences for me since they allowed me to work with microparasites in addition to the macroparasites on which I focused for the core of my dissertation research. I look forward to many years of rich collaboration with Dr. Parker. I would also like to thank each member of my dissertation committee for their insights and support (including numerous letters of support that they have furnished), especially those communicated during my dissertation proposal defense, the fruit of 6 which led to several successfully-funded grant proposals and gave me a clear springboard into the remaining years of my dissertation research. Dr. Kellogg benefited my training in many ways, including by serving as an excellent Director of Graduate Studies during my first year at UM-St. Louis. Dr. Kellogg gave us a helpful and clear academic plan during our Ph.D. student-orientation, which I tried to follow closely. Dr. Kellogg also helped train me in the theory of systematics and evolutionary biology more generally, and encouraged me to find and pursue my interests. Dr. Kevin Johnson visited campus early during my dissertation research, and along with Dr. Vince Smith, provided support of my ideas and research plan, which was very important to me since they are students of louse biology. Dr. Johnson provided crucial information in a collaboration that led to the publication of our straggling paper. Dr. Johnson has given me many specimens, data from which have been included in this dissertation. Dr. Marquis has helped ensure that my data collection, analyses and questions were as rigorous as possible. I am especially thankful of his support during the peer-review process. Dr. Marquis also challenged me to think about the importance of host-defenses as a driver of parasite diversification. Finally, I am thankful of Dr. Ricklefs’ early encouragement and support of my research.
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