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The Pennsylvania State University the Graduate School The Pennsylvania State University The Graduate School EVOLUTIONARY AND ECOLOGICAL PATTERNS IN BUMBLE BEES (Bombus spp.): FROM MIMETIC COLORATION TO EPIDEMIOLOGICAL DYNAMICS A Dissertation in Entomology by Briana D. Ezray Ó 2019 Briana D. Ezray Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy August 2019 ii The dissertation of Briana D. Ezray was reviewed and approved* by the following: Heather Hines Associate Professor of Biology and Entomology Dissertation Advisor Chair of Committee Christina Grozinger Distinguished Professor of Entomology Director of Center for Pollinator Research Diana Cox-Foster Adjunct Professor of Entomology, Penn State University Research Leader USDA-ARS-PWA Pollinating Insect – Biological Management Systems – Research Unit Utah State University, Department of Biology Margarita López-Uribe Lorenzo L. Langstroth Early Career Professor, Assistant Professor of Entomology Erica Smithwick Professor of Geography Director of Center for Landscape Dynamics Gary Felton Professor of Entomology Department Head - Entomology *Signatures are on file in the Graduate School iii ABSTRACT The formation and maintenance of biodiversity patterns are driven by the interplay between ecology and evolution. Globally, biodiversity loss is occurring among numerous organisms ranging from mammals to invertebrates. Bees, for instance, are experiencing drastic population declines and range reductions. These declines have been attributed to reduced genetic diversity, agricultural intensification, pesticides, pathogens, and parasites. To conserve bee populations, a thorough understanding of how various ecological and evolutionary factors interact to drive organismal and community diversity and distribution is necessary. Here, I examine both mimetic and epidemiological dynamics with the goal of determining the spatial distribution, temporal changes, and ecological and evolutionary selective factors involved in the establishment of geographic and phylogenetic patterns. To advance the understanding of the evolutionary and ecological processes that drive mimetic color distribution in bumble bees, I utilized an innovative, machine learning method to quantify color pattern perception. I then applied these perceptual values to both spatial and phylogenetic analyses. To further examine the processes driving patterns and distributions of a polymorphic bumble bee, Bombus melanopygus, I employed COI barcoding to detect patterns of historical biogeography and selection. To improve the understanding of the epidemiological dynamics of bee communities, I conducted a longitudinal survey of pathogen and parasite seasonality across honey bees (Apis mellifera) and the common eastern bumble bee (Bombus impatiens). I further explored the dynamics surrounding cross-species horizontal transmission by determining the persistence of Deformed Wing Virus (DWV) particles, outside of a host, in the environment. Ultimately, I found that (1) bumble bees are continuously converging on a local, average color pattern, (2) historical events may have driven the distribution of color patterns of a dimorphic species, B. melanopygus, (3) pathogens and parasites display unique seasonal trends with honey bees iv maintaining and bumble bees purging pathogens through the overwintering period, and (4) DWV viral particles may be able to survive outside the host for greater than 2 months. Together, these results enhance knowledge regarding the influence of various evolutionary and ecological dynamics on the community composition of bumble bee species themselves as well as the pathogens and parasites they harbor. v TABLE OF CONTENTS LIST OF FIGURES............................................................................................................. vii LIST OF TABLES .............................................................................................................. xii ACKNOWLEDGEMENTS ................................................................................................. xiv Chapter 1 ................................................................................................................... Introduction ................................................................................................................. 1 References ........................................................................................................... 5 Chapter 2 Unsupervised machine learning reveals mimicry complexes in bumble bees occur along a perceptual continuum ............................................................................. 8 Abstract ............................................................................................................... 8 Introduction ......................................................................................................... 9 Materials and Methods ......................................................................................... 11 Results ................................................................................................................. 18 Discussion............................................................................................................ 23 Conclusions ......................................................................................................... 28 References ........................................................................................................... 30 Supplemental References ..................................................................................... 52 Chapter 3 Phylogeographic analysis reveals geographic discordance between phenotypic and mitochondrial transition zones in the bumble bee, Bombus melanopygus ............... 53 Abstract ............................................................................................................... 53 Introduction ......................................................................................................... 54 Methods ............................................................................................................... 57 Results ................................................................................................................. 62 Discussion............................................................................................................ 64 Conclusions ......................................................................................................... 69 References ........................................................................................................... 70 Chapter 4 Seasonal variation, overwintering behaviors, and foraging dynamics as indicators of pathogen prevalence in bee communities ................................................. 87 Abstract ............................................................................................................... 87 Introduction ......................................................................................................... 88 Methods ............................................................................................................... 91 Results ................................................................................................................. 97 Discussion............................................................................................................ 101 Conclusions ......................................................................................................... 110 References ........................................................................................................... 111 Chapter 5 Environmental persistence of Deformed Wing Virus .......................................... 139 vi Abstract ............................................................................................................... 139 Introduction ......................................................................................................... 140 Methods ............................................................................................................... 143 Results ................................................................................................................. 148 Discussion............................................................................................................ 152 References ........................................................................................................... 158 Chapter 6 Summary and Conclusions ................................................................................. 169 References ........................................................................................................... 176 vii LIST OF FIGURES Figure 2-1: Quantification of mimetic patterns among bumble bee species of the United States. (a) t-SNE plot of perceptual color embedding values. (b) Topology of color similarity (left) compared to phylogenetic history [Hines 2008] (right) with color from the t-SNE for each taxon and tanglegram lines connecting the same taxon. (c) Fine-scale depiction of perceptual averages calculated by averaging the t-SNE positions of all bumble bee specimens contained within each grid cell. (d) The same analysis, but excluding species in decline (B. affinis, B. pensylvanicus/B. sonorus, and B. terricola/B. occidentalis). (e) Average color embedded score by species/color form. (f) The most frequent species colored as in the t-SNE. ........................................ 38 Figure 2-2: Mimetic transition
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