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Geographical Variation in Social Structure, Morphology, and Genetics of the New World Honey Ant Myrmecocystus Mendax by Ti H. E

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Geographical Variation in Social Structure, Morphology, and Genetics of the New World Honey Ant Myrmecocystus Mendax by Ti H. E Geographical Variation in Social Structure, Morphology, and Genetics of the New World Honey Ant Myrmecocystus mendax by Ti H. Eriksson A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Approved July 2018 by the Graduate Supervisory Committee: Jürgen Gadau, Co-Chair Jay Taylor, Co-Chair Jennifer Fewell Bert Hӧlldobler Robert Johnson Stephen Pratt ARIZONA STATE UNIVERSITY August 2018 ABSTRACT Persistent cooperation between unrelated conspecifics rarely occurs in mature eusocial insect societies. In this dissertation, I present evidence of non-kin cooperation in the Nearctic honey ant Myrmecocystus mendax. Using microsatellite markers, I show that mature colonies in the Sierra Ancha Mountain of central Arizona contain multiple unrelated matrilines, an observation that is consistent with primary polygyny. In contrast, similar analyses suggest that colonies in the Chiricahua Mountains of southeastern Arizona are primarily monogynous. These interpretations are consistent with field and laboratory observations. Whereas cooperative colony founding was observed frequently among groups of Sierra Ancha foundresses, founding in the Chiricahua population was restricted to individual foundresses. Furthermore, Sierra Ancha foundresses successfully established incipient laboratory colonies without undergoing queen culling following emergence of the first workers. Multi-queen laboratory Sierra Ancha colonies also produced more workers and repletes than haplometrotic colonies, and when brood raiding was induced between colonies, queens of those with more workers had a higher survival probability. Microsatellite analyses of additional locations within the M. mendax range suggest that polygyny is also present in some other populations, especially in central- northern Arizona, albeit at lower frequencies than that in the Sierra Anchas. In addition, analyses of multiple types of genetic data, including microsatellites, the mitochondrial barcoding region, and over 2000 nuclear ultra-conserved elements indicate that M. mendax populations within the southwestern U.S. and northwestern Mexico are geographically structured, with strong support for the existence of two or more divergent i clades as well as isolation-by-distance within clades. This structure is further shown to correlate with variation in queen number and hair length, a diagnostic taxonomic feature used to distinguish honey ant species. Together, these findings suggest that regional ecological pressures (e.g. colony density , climate) may have acted on colony founding and social strategy to select for increasing workforce size and, along with genetic drift, have driven geographically isolated M. mendax populations to differentiate genetically and morphologically. The presence of colony fusion in the laboratory and life history traits in honey ant that are influenced by colony size, including repletism, brood raiding, and tournament, support this evolutionary scenario. ii DEDICATION To my parents, Jimmy and Thuha Eriksson, for their unending support, encouragement, and love. iii ACKNOWLEDGMENTS I am very grateful to my co-chairs, Jürgen Gadau and Jay Taylor, for their intellectual and material support throughout this endeavor. Despite his busy schedule, Jürgen always find time to answer questions and help refining my work. Jay’s mentoring has been indispensable, and without his love of birding and collecting zeal, half of the specimens in this dissertation would not have been available. I am also thankful to Stephen Pratt for his wisdom on navigating statistics and academia, to Bert Hӧlldobler for his knowledge of Myrmecocystus, to Jennifer Fewell for graciously allowing my colonies (and mess) to take up precious space in her laboratory for so long, and to Bob Johnson for contributing and identifying specimens of this taxonomically challenging group of ants. My appreciation also goes to Christian Rabeling and his laboratory, especially to Marek Boroweic and Jeff Sosa-Calvo for their valuable support and contribution to the UCE project. I want to thank the entire amazing Social Insects Research Group at ASU for the intellectual stimulation, laughter, and support that have helped keep me afloat, especially Ioulia Bespalova, Abby Finkelstein, Johnathon Jackson, Christina Kwapich, and Ben Pyenson. I also want to acknowledge Elizabeth Cash, Josh Gibson, Martin Helmkampf, and Rick Overson for their guidance during my early days in the Gadau Lab at ASU. Thanks go to Kevin Haight for getting me into the Thursday-at-Boulder’s routine, as well as Yohan Cho and Zach Shaffer for regularly letting me borrow their six-legged subjects for outreach. Field work would not have been possible without Kevin Demater, Christian D'Orgeix, Harry Grissom, Brandon Siqueiros, Asia (Joana) Sulich, and Rafael Testai. Last but not least, thanks to my cat, Martin, for allowing me to pet him daily. iv TABLE OF CONTENTS Page LIST OF TABLES ..................................................................................................................... vii LIST OF FIGURES ................................................................................................................. viii CHAPTER 1 INTRODUCTION ................................................................................................... 1 2 A CASE STUDY OF VARIATION IN COLONY FOUNDING BEHAVIOR AND SOCIAL ORGANIZATION OF MYRMECOCYSTUS MENDAX............. 8 Introduction ................................................................................................................. 8 Materials and Methods ............................................................................................. 11 Results ....................................................................................................................... 18 Discussion ................................................................................................................. 24 3 A MULTI-POPULATION ANALYSIS OF SOCIAL VARIATION, GENETIC STRUCTURE, AND ECOLOGY IN MYRMECOCYSTUS MENDAX ............. 39 Introduction ................................................................................................................ 39 Materials and Methods .............................................................................................. 40 Results ........................................................................................................................ 45 Discussion .................................................................................................................. 51 4 THE RELATIONSHIP BETWEEN PHYLOGEOGRAPHY AND POLYMORPHISM IN MYRMECOCYSTUS MENDAX ..................................... 71 Introduction ................................................................................................................ 71 Materials and Methods .............................................................................................. 73 Results ........................................................................................................................ 82 v CHAPTER Page Discussion .................................................................................................................. 91 5 CONCLUSION .................................................................................................... 125 REFERENCES ........................................................................................................................ 133 APPENDIX A. MULTI-LOCUS MICROSATELLITE GENOTYPES OF MYRMECOCYSTUS MENDAX SPECIMENS FROM CHAPTER TWO ................................................ 147 B. ANALYSIS CONDITIONS AND TECHNICAL RESULTS FOR MATESOFT AND COLONY ......................................................................................................... 164 C. MULTI-LOCUS MICROSATELLITE GENOTYPES OF MYRMECOCYSTUS MENDAX SPECIMENS FROM CHAPTER THREE ............................................ 168 vi LIST OF TABLES Table Page 2.1. Microsatellite Statistics of Sierra Ancha and Chiricahua Populations ............ 35 2.2. Summary of Experiments and Sample Sizes .................................................... 36 2.3. Social Structure Inferences of Sierra Ancha and Chiricahua Populations ...... 37 2.4. Reproductive Allocation in Sierra Ancha Fused Colonies .............................. 38 3.1. Descriptions of 15 Populations .......................................................................... 65 3.2. Microsatellite Statistics of 15 Populations ........................................................ 66 3.3. Social Structure Inferences of 15 Populations .................................................. 67 3.4. Pairwise θ Estimates ........................................................................................... 68 3.5. Pairwise G"ST Estimates...................................................................................... 69 3.6. Pairwise Nm Estimates ....................................................................................... 70 4.1. Sample Summary .............................................................................................. 114 4.2. Sequence Descriptions ...................................................................................... 116 4.3. Summary of Colonies With Both mtDNA and UCE Data ............................ 117 4.4. K2P Distance Within Inferred Clades ............................................................. 119 4.5. K2P Distance Between Inferred Clades Estimated From mtDNA ..............
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