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DISSERTATION PARASITES AND IMMUNOGENETIC DIVERSITY IN PRAIRIE DOGS Submitted by Elizabeth M. Harp Graduate Degree Program in Ecology In partial fulfillment of the requirements For the Degree of Doctor of Philosophy Colorado State University Fort Collins, Colorado Summer 2018 Doctoral Committee: Advisor: Michael F. Antolin Lora R. Ballweber N. Thompson Hobbs Ashley K. McGrew Copyright by Elizabeth M. Harp 2018 All Rights Reserved ABSTRACT PARASITES AND IMMUNOGENETIC DIVERSITY IN PRAIRIE DOGS Prairie dogs (Cynomys spp.) are an important component of North American grassland communities. Prairie dogs have been characterized as ecosystem engineers and keystone species because their extensive burrow systems alter ecosystem dynamics and provide homes for a variety of species. Prairie dog populations have declined dramatically over the past century as a result of eradication programs, habitat loss, and introduced plague. This research explores factors related to host-parasite ecology and immunogenetics of prairie dogs. The second chapter is a systematic review of parasites recorded from all five prairie dog species. The third chapter characterizes genetic diversity and investigates selection at the hyperdiverse MHC DRB locus in black-tailed prairie dogs. The fourth chapter uses multimodel inference to investigate host and environmental factors affecting flea aggregation on black-tailed prairie dogs. I found host-parasite records documenting at least 104 parasites species from prairie dogs. Over 2/3 of parasite species were ectoparasites, primarily fleas. Most endoparasites were protozoa. Bacteria and viruses are essentially undescribed from prairie dogs. Potentially related to the diversity of parasites they are exposed to, the DRB gene in black-tailed prairie dogs was characterized by high levels of diversity. I also found considerable evidence for contemporary directional selection and historical balancing selection acting on the DRB gene in black-tailed prairie dogs. However, I found only weak evidence for a relationship between DRB genotype and flea parasitism in black-tailed prairie dogs. Primary drivers of flea aggregation on black- tailed prairie dogs, identified by multimodel inference of generalized linear models, were host ii sex and month of capture. Males were more heavily parasitized than females, and flea loads are greatest in September and lowest in June. iii ACKNOWLEDGEMENTS I am deeply grateful to Mike Antolin, Tom Hobbs, Lora Ballweber, and Ashley McGrew for their expertise, guidance, support, and immense patience, especially in the final few months of this journey. Thanks especially to Mike Antolin for always encouraging my love of teaching and for never giving up on me. The field work would not have been possible without the help of a small army of enthusiastic undergraduate volunteers who gave freely of their time and talents during long, hot days that started before the sun came up. I owe immeasurable thanks to friends and family for their support and encouragement. In particular I cannot possibly thank Jarrod and Aiden enough for their patience, love, support, and encouragement. Jarrod especially has gone above and beyond what I would have asked of him, taking on much more than his fair share so that I could focus on finally finishing this degree. Thanks to my mother (Norma) and Jarrod’s mother (Lorraine) for their incredible support and encouragement. Finally, I am forever indebted to Jim Petranka, Mike Stuart, and Tim Forrest, three of the finest people I have been privileged to know. Their enthusiasm for teaching and commitment to fostering scientific curiosity in their students continues to be an inspiration to me and countless others. iv TABLE OF CONTENTS ABSTRACT .................................................................................................................................... ii PARASITES AND IMMUNOGENETIC DIVERSITY IN PRAIRIE DOGS ........................... ii ACKNOWLEDGEMENTS ........................................................................................................... iv TABLE OF CONTENTS .................................................................................................................v CHAPTER ONE ..............................................................................................................................1 INTRODUCTION ....................................................................................................................... 1 Summary of research ........................................................................................................... 3 Summary of results .............................................................................................................. 4 LITERATURE CITED ............................................................................................................... 7 CHAPTER TWO ...........................................................................................................................11 A REVIEW OF THE PARASITES OF PRAIRIE DOGS (CYNOMYS SPP.) ......................... 11 Introduction ........................................................................................................................... 11 Materials and Methods .......................................................................................................... 17 Literature Search ................................................................................................................ 17 Recorded Information ........................................................................................................ 18 Statistical Analyses ............................................................................................................ 20 Results ................................................................................................................................... 21 Fleas ................................................................................................................................... 24 Lice .................................................................................................................................... 26 Mites .................................................................................................................................. 27 Ticks ................................................................................................................................... 27 Helminths ........................................................................................................................... 28 Protozoa ............................................................................................................................. 29 Bacteria .............................................................................................................................. 30 Viruses ............................................................................................................................... 30 Discussion .............................................................................................................................. 31 Fleas ................................................................................................................................... 31 Lice .................................................................................................................................... 33 Mites .................................................................................................................................. 35 Ticks ................................................................................................................................... 36 Helminths ........................................................................................................................... 37 Protozoa ............................................................................................................................. 40 Bacteria .............................................................................................................................. 41 Viruses ............................................................................................................................... 42 v Other parasites ................................................................................................................... 43 Summary and Conclusions ................................................................................................ 45 LITERATURE CITED .......................................................................................................... 86 CHAPTER THREE .....................................................................................................................111 DIVERSITY, SELECTION, AND THE MHC CLASS II DRB LOCUS IN BLACK-TAILED PRAIRIE DOGS (CYNOMYS LUDOVICIANUS) FROM PAWNEE NATIONAL GRASSLAND, COLORADO ................................................................................................. 111 Introduction ......................................................................................................................... 111 Methods ............................................................................................................................... 114 Sample collection and DNA extraction ........................................................................... 114 Molecular methods..........................................................................................................
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