Phylogenetics, Comparative Parasitology, and Host Affinities of Chipmunk Sucking Lice and Pinworms Kayce Bell

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Phylogenetics, Comparative Parasitology, and Host Affinities of Chipmunk Sucking Lice and Pinworms Kayce Bell University of New Mexico UNM Digital Repository Biology ETDs Electronic Theses and Dissertations 7-1-2016 Coevolving histories inside and out: phylogenetics, comparative parasitology, and host affinities of chipmunk sucking lice and pinworms Kayce Bell Follow this and additional works at: https://digitalrepository.unm.edu/biol_etds Recommended Citation Bell, Kayce. "Coevolving histories inside and out: phylogenetics, comparative parasitology, and host affinities of chipmunk sucking lice and pinworms." (2016). https://digitalrepository.unm.edu/biol_etds/120 This Dissertation is brought to you for free and open access by the Electronic Theses and Dissertations at UNM Digital Repository. It has been accepted for inclusion in Biology ETDs by an authorized administrator of UNM Digital Repository. For more information, please contact [email protected]. Kayce C. Bell Candidate Department of Biology Department This dissertation is approved, and it is acceptable in quality and form for publication: Approved by the Dissertation Committee: Dr. Joseph A. Cook , Chairperson Dr. John R. Demboski Dr. Irene Salinas Dr. Kenneth Whitney Dr. Jessica Light i COEVOLVING HISTORIES INSIDE AND OUT: PHYLOGENETICS, COMPARATIVE PARASITOLOGY, AND HOST AFFINITIES OF CHIPMUNK SUCKING LICE AND PINWORMS by KAYCE C. BELL B.S., Biology, Idaho State University, 2003 M.S., Biology, Idaho State University, 2006 DISSERTATION Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Biology The University of New Mexico Albuquerque, New Mexico July 2016 ii ACKNOWLEDGEMENTS Completion of my degree and this dissertation would not have been possible without the guidance and support of my mentors, family, and friends. Dr. Joseph Cook first introduced me to phylogeography and parasites as undergraduate and has proven time and again to be the best advisor a graduate student could ask for. His encouragement and mentoring have prepared me for a future in research and given me an exceptional appreciation of museums and fieldwork. Dr. John Demboski not only served on my committee, he brought me into the wonderful world of chipmunk research and has provided valuable input and a wealth of chipmunk knowledge. I am very grateful for the parasite expertise of Dr. Jessica Light and Dr. Eric Hoberg. Through their guidance I learned about louse and pinworm biology and how my research fits into the broader scheme of parasite research. Dr. Julia Allen has provided so much bioinformatic support, but more importantly has been a patient teacher. In addition to Dr. Cook, Dr. Demboski, and Dr. Light, I thank my additional committee members, Dr. Irene Salinas and Dr. Kenneth Whitney, for their input and time. My Ph.D. research spanned multiple areas of biology and my committee has provided encouragement and knowledge, particularly in areas where I am less well versed. Many people assisted on this project in the field and in the lab. I am grateful for field assistance from Daniel Kessler, Bryan McLean, Randle McCain, Schuyler Liphardt, Lois Alexander, Patty McDonald, Wayne Bell, Jessicia Campbell, and Iris Demboski. I was assisted in the lab by Kendall Calhoun, Diego Matek, and Schuyler Liphardt. Samples were collected from museum study skins by Diego Matek, Bryan McLean, and Mrs. Suzy Dunnum’s 2014 7th grade gifted life sciences classes. This work would not iii have been possible without museum samples from the Burke Museum of Natural History, Denver Museum of Nature & Science, Monte L. Bean Life Sciences Museum, Moore Laboratory of Zoology, Museum of Southwestern Biology, Natural Science Research Laboratory, Royal Ontario Museum, and United States National Museum of Natural History. Additionally, James Patton, Eric Rickart, Duke Rogers, and Angela Hornsby collected samples in the field and sent them to me. Lastly, but most importantly, my family has taken care of me and given unconditional support during my graduate career. My husband Daniel Kessler has been unbelievably understanding about the work hours and time away and can always be counted on for an adventure when I need a break. My parents, Patty McDonald, Wayne Bell, Billie McDonald, and Lorraine Bell have been my role models and seen my potential, even when I may not have. My siblings, Jessicia Campbell, Meredith Bell, Nichole Schwend, and Sara McDonald have helped with fieldwork and are always there for a much-needed outside perspective. iv COEVOLVING HISTORIES INSIDE AND OUT: PHYLOGENETICS, COMPARATIVE PARASITOLOGY, AND HOST AFFINITIES OF CHIPMUNK SUCKING LICE AND PINWORMS by Kayce C. Bell B.S. Biology, Idaho State University M.S. Biology, Idaho State University Ph.D., Biology, University of New Mexico ABSTRACT Diversification of parasite species, in light of their host association, is an area ripe for testing hypotheses of evolution when one species requires another for survival. The 23 species of western North American chipmunks (genus Tamias) host two species of ectoparasitic sucking lice (Anoplura) and two species of endoparasitic pinworms (Nematoda). I used a phylogenetic approach to investigate the evolutionary histories of the parasites in light of the hosts and the landscape. In comparing the parasites, I found that the two pinworm species have similar diversification patterns, linked to hosts, but those processes occurred on different time scales. As another paired investigation, the chipmunk sucking lice revealed some lineages that correspond to host relationships, but the lice have different histories from the hosts, as well as each other. Overall, this system demonstrates that parasite diversification cannot be explained as a simple process of codivergence and that parasite evolution, even when comparing parasites from the same hosts and ecological roles, is complex and the history is unique to each species. While I found a role for hosts, host demographic history, and landscape in shaping genetic structure in all four parasites, these processes impacted each parasite species differently. v TABLE OF CONTENTS INTRODUCTION………………………………………………………………………...1 Literature Cited…………………………………………………………………....6 CHAPTER 1: Expanded Host Range of Sucking Lice and Pinworms of Western North American Chipmunks (Genus Tamias) …………………………………………………...7 Abstract…………………………………………………………………………....7 Acknowledgements………………………………………………………………14 Literature Cited…………………………………………………………………..15 Tables………………………………………………………………………….…20 Figure Legend.…………………………………………………………………...24 Figure………………………………………………………………………….…25 Supplement………………………………………………………………………26 CHAPTER 2: Temporal and spatial mosaics: deep host association and shallow geographic drivers shape genetic structure in a widespread pinworm, Rauschtineria eutamii………………………………...…………………………………………….....…36 Abstract…………………………………………………………………………..37 Introduction……………………………………………………………………....38 Materials and Methods…………………………………………………………...42 Results…………………………………………………………………………....45 Discussion………………………………………………………………………..47 Acknowledgements……………………………………………………………....55 References……………………………………………………………………….56 Figure Legends…………………………………………………………………..67 vi Tables…………………………………………………………………………….68 Figures……………………………………………………………………………70 Appendices……………………………………………………………………….74 Supplemental Figure Legends……………………………………………………79 Supplemental Tables……………………………………………………………..80 Supplemental Figures……………………………………………………………83 CHAPTER 3: Multiple parasites show deep, but asynchronous, concordance in diversification that contrasts with shallow phylogeographic structure………….……….85 Abstract…………………………………………………………………………..85 Introduction……………………………………………………………………....85 Methods…………………………………………………………………………..91 Results…………………………………………………………………………....96 Discussion………………………………………………………………………101 Acknowledgements……………………………………………………………..113 Literature Cited…………………………………………………………………114 Figure Legends…………………………………………………………………125 Tables…………………………………………………………………………...127 Figures…………………………………………………………………………..129 Supplemental Figure Legends…………………………………………………..134 Supplemental Tables……………………………………………………………135 Supplemental Figures…………………………………………………………..138 Appendices……………………………………………………………………..141 vii CHAPTER 4: Disentangling lousey relationships: a phylogenomic perspective on host and parasite diversification………….……………………………………………….…150 Abstract…………………………………………………………………………150 Introduction……………………………………………………………………..151 Methods…………………………………………………………………………153 Results…………………………………………………………………………..158 Discussion………………………………………………………………………161 Acknowledgements……………………………………………………………..165 Literature Cited…………………………………………………………………166 Figure Legends…………………………………………………………………171 Figures…………………………………………………………………………..172 CONCLUSION….……………………………………………………………………...177 Literature Cited…………………………………………………………………179 viii INTRODUCTION The evolution of interacting species and their selective influence on one another has interested biologists for some time; even Darwin (1859) described it in On the Origin of Species. In the past, coevolutionary investigations generally expected cospeciation when the interaction is sufficiently tightly linked for one species to require the other. However, biologists are discovering that the evolution of interacting organisms is more nuanced than simplistic assumptions about cospeciation. In fact, some have even questioned if classic examples of host-parasite codivergence, such as gophers and chewing lice (Hafner and Nadler 1988, 1990), were robustly assessed (Brooks et al. 2015). While this overturns a paradigm of coevolutionary thought, it leaves many open questions of how interacting organisms
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