UNTANGLING THE COEVOLUTIONARY HISTORY BETWEEN DOVES AND THEIR PARASITIC LICE BY ANDREW DONALD SWEET DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Ecology, Evolution, and Conservation Biology in the Graduate College of the University of Illinois at Urbana-Champaign, 2018 Urbana, Illinois Doctoral Committee: Dr. Kevin Johnson, Chair, Director of Research Professor May Berenbaum Professor James Whitfield Associate Professor Brian Allan Assistant Professor Julian Catchen ABSTRACT In host-parasite systems, any given host species can be associated with multiple types of parasites, each of which can have a unique ecological relationship with the host. However, it remains unclear how these ecological differences link to evolutionary patterns. What shapes the dynamics of a host-parasite interaction over evolutionary time? An ideal approach for addressing this question is to compare multiple lineages of similar parasites that are associated with the same group of hosts but have distinct ecological differences – or “ecological replicates.” For my dissertation, I applied this strategy by focusing on the wing and body lice of doves. These two “ecomorphs” of lice are not closely related yet exclusively parasitize the same group of hosts. Notably, wing lice have a greater capability for dispersal than body lice. Dispersal is an important ecological component of host-parasite interactions and speciation in general. The first part of my dissertation examined broad cophylogenetic patterns across the dove-louse system. I found that wing and body lice did not have correlated patterns, and body lice showed more cospeciation with their hosts. This pattern agreed with previous studies, the results of which suggested that the increased cospeciation in body lice was due to differences in dispersal ability. In contrast with previous work, I also found that both wing and body louse phylogenies are statistically congruent with the host phylogeny. However, the previous studies had limited taxon sampling compared to my study, indicating that taxon sampling can have a significant impact on the results of cophylogenetic comparisons, and that there can be variable cophylogenetic patterns ii within a host-parasite system. Cophylogenetic variation in dove lice was further highlighted by my study on lice from phabine doves, a clade native to Australia and Southeast Asia. In this system, wing lice have higher levels of cospeciation with their hosts than did body lice, which is the opposite pattern found in other dove louse systems. The second part of my dissertation focused on the wing and body lice of New World ground-doves. All three groups (wing lice, body lice, and doves) are monophyletic and have relatively few species, which makes the system ideal for obtaining a comprehensive taxonomic sample. As a group that straddles the population-species boundary, ground-dove lice are also useful for gaining insight into host-parasite evolution at phylogenetic and population scales. I used Sanger or whole-genome sequencing data to estimate phylogenetic and/or population patterns of the ground-dove hosts and both groups of lice. For the louse genomes, I developed a novel pipeline to assemble nuclear genes for phylogenetic analysis and call SNPs for population analysis. My results indicate that dispersal is a key factor in shaping the evolution of this host-parasite system. Body lice had higher levels of cospeciation with their hosts, were more host-specific, and had higher rates of divergence than wing lice. At the population level, some body lice also showed host-specific structure, whereas wing lice did not. Body lice also had lower levels of heterozygosity than wing lice, suggesting higher levels of inbreeding. However, dispersal is likely not the only factor that shapes this host-parasite system. Host phylogeny appears to have a significant effect as well. Both wing and body louse phylogenies were statistically congruent with the host phylogeny, and the congruence metrics for individual associations were correlated between the two types of lice. Biogeography may also dictate host-parasite interactions. The wing louse phylogeny was iii significantly structured according to biogeographic region, and both wing and body lice also showed some biogeographic structure at the population level. Together, these results show that host-parasite interactions can be dictated by many ecological factors over evolutionary time, even in the presence of a primary, dominant factor (e.g., parasite dispersal). iv ACKNOWLEDGEMENTS I have been a tree amid the wood And many a new thing understood That was rank folly to my head before. -Ezra Pound, “The Tree” Although my name is on the title page, this dissertation is the culmination of work that has been supported by myriads. First, I am indebted to my advisor, Kevin Johnson. He took me on as a green student with relatively little research experience, and helped me to become a better scientist and scholar. I am grateful for his frequent guidance on my research, honest and constructive criticism of my writing, and help with organizing fieldwork. One day, I hope he is able to bask in the glory of a Twins victory over the Yankees in a playoff series. I also want to thank my dissertation committee present and past: Brian Allan, May Berenbaum, Julian Catchen, Jim Whitfield, and Zac Cheviron. Their guidance was invaluable as my dissertation took shape, and several of them wrote me recommendation letters for various award applications. A special thanks to Brian Allan for serving as the chair for my preliminary exam. Collaborators from all over the world, some of whom I have never met in person, have been foundational for my research. Thank you to Vitor de Q. Piacentini and Michel v Valim for collecting many louse specimens for me in Brazil, especially after my plans to collect in person fell through. Thank you to the many people who have over the years collected lice I used in my dissertation: Sarah Bush, Dale Clayton, Jeff DaCosta, Robert Faucett, John Klicka, Peggy Guttan-Mayerma, Ian Mason, Kevin McCracken, Matthew Miller, Robert Palmer, Garth Spellman, and Robert Wilson. Also thank you to Terry Chesser for collaborating on the phabine project. For my fieldwork in Ecuador, thank you to Jose Luis Rivera-Parra for helping to organize the trip, arrange field sites, etc. I was able to collect important samples, but the trip would not have been possible without Jose’s effort. I am especially grateful for two individuals who helped me in the field: Edith Montalvo and Edison Auqui. They were instrumental in collecting the samples I needed, while simultaneously putting up with my terrible Spanish and marginal mist- netting “skills.” Also, thank you to Henry Pollock for showing me the ropes on mist- netting, and for allowing me to bring some of his nets with me to Ecuador. I am grateful for the many sources of financial support I have received while at Illinois. Thank you to the Program in Ecology, Evolution, and Conservation for several summers of RA support and for travel grants to attend conferences and workshop. I am also thankful for the TA positions that were available through my program. I received some summer support through the Clark Summer Fellowship. The Graduate College Dissertation Travel Grant gave me generous funding to conduct fieldwork. I also received support for fieldwork through an American Ornithological Society student research award, the Herbert Holdsworth Ross Award, and the Francis M. and Harlie M. Clark Research Support Grant. The Graduate College Dissertation Completion Fellowship allowed me to focus on finishing my dissertation work during my final year. vi I am also thankful for the support of my friends throughout my graduate studies. Julie Allen and Bret Boyd have been two of my greatest mentors. They are amazing scientists and wonderful teachers, and I am glad to have overlapped with them in the Johnson Lab. Therese Catanach has been a good friend, and we have had some good times chasing doves in Texas, watching World Series games at Crane Alley, and of course playing catch whenever possible. Scott Shreve was a great mentor during my first year, and as a senior graduate student was very helpful during my transition to graduate school life. Thank you also to the various graduate and undergraduate students in the Johnson Lab for helpful discussions and assistance in obtaining data: Patrick Grady, Robert De Moya, Stephany Herrera, Gabriela Escalante, Brandon Jones, Ashley Markazi, Jennifer Nowak, and Matthew Mason. I took part in many good paper discussions with the Systematics Discussion Group, one of which spurred a fun collaborative side project on human hepatitis B virus. The two seasons with the Softballogists provided some healthy competition and good times with fellow biologists and friends. I feel compelled to briefly acknowledge some crucial sources of inspiration and mental well-being. As I began graduate school, I quickly discovered the importance of satisfying the right hemisphere of my brain. And so, thank you to Frost and Faulkner, Strand and Hemingway, Harding and Robinson, Beethoven and Pärt, Saint-Saëns and Barber, Brahms and Mozart, Pollock and Picasso, Vermeer and Ruisdael, Raphael and Van Eyck. I am also grateful the Krannert Art Museum was across the street from my office. Finally, I would like to thank my family. I doubt these last six years would have been sustainable without their love and support. Thank you to my parents, who have vii always encouraged my zeal for science. I am grateful for their enthusiasm to learn about my dissertation research, and for their excitement to read my first published papers. They have been, and will continue to be, big role models in my life. Thanks to my siblings – Jeremiah, Hannah, and Jerushah. I am glad they made several visits to central Illinois. Thank you also to all four of my grandparents, who have always supported and expressed great interest in their grandchildren’s endeavors.