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(Genus: Bombus): from the Organism to the Environment AD UNIVERSITY OF CALIFORNIA RIVERSIDE Feeding and Foraging in Bumble bees (Genus: Bombus): From the Organism to the Environment A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Entomology by Kaleigh Fisher June 2021 Dissertation Committee: Dr. S. Hollis Woodard, Chairperson Dr. Jessica Purcell Dr. Naoki Yamanaka Dr. Anupama Dahanukar Copyright by Kaleigh Fisher 2021 The Dissertation of Kaleigh Fisher is approved: Committee Chairperson University of California, Riverside Acknowledgements I would first like to thank my mentor Dr. S. Hollis Woodard for her exceptional mentorship and friendship over the course of my doctoral studies. Her support has been critical for my success as a scientist and I sincerely value all of the skills that I have developed through her mentorship. I thank her for always believing in my potential, encouraging me to pursue the exciting ideas, and showing me how to be an overall awesome scientist through her example as an amazing role model. I am also grateful for all of the members of my dissertation and qualifying exam committees Dr. Jessica Purcell, Dr. Naoki Yamanaka, Dr. Anupama Dahanukar, Dr. Quinn McFrederick, and Dr. Jason Stajich. I am especially grateful to Dr. Purcell for her encouragement and valuable conversations throughout my doctoral studies. It was such a great experience learning from her in classes as well as collaborating with her on a social insects review. I also thank her for being such an impactful role model for me. I am also especially grateful to Dr. Yamanaka and Dr. Dahanukar for collaborating on the taste projects and always offering their time, encouragement, and feedback on projects. It was such a pleasure to be able to work with such highly esteemed and kind scientists. I would also like to thank members of the Entomology Department in general for fostering such a positive and supportive department to work in, as well as all of the graduate students that I had the pleasure to interact with and work on outreach and departmental events with. I thank all of the staff in the Entomology Department for being so helpful and kind with logistics and administrative tasks. iv I would like to thank all of the members of the Woodard Lab who helped make all of these projects possible: Dr. Michelle Duennes, Kristal Watrous, Alexandra Vanececk, Christie Miranda, Natalie Fischer, Erica Sarro, Dr. Claudineia Costa, Sandara Brasil, Blanca Guillen, Yadira Romero Diaz, Damaris Rodriguez, and Alex Brinkley. Finally, I would like to thank all of my friends and family for their encouragement and support throughout this long process. I would especially like to thank my partner Dr. Aldo de la Mora Rodriguez, for always supporting and encouraging me, and always making me the best, bougiest coffee. I also thank my daughter Rafaela de la Mora Fisher, for always dancing, celebrating, and laughing with me. Chapter One was completed in collaboration with co-authors Blanca Guillen, Dr. Hugh M. Robertson, Dr. Naoki Yamanaka, Dr. Anupama Dahanukar, and Dr. S. Hollis Woodard. Funding for this project came from a U.S.D.A. N.I.F.A. Seed Grant. Chapter Two is currently in review for the Journal of Animal Behavior with Erica Sarro as a co-first author, who was so much fun to collaborate and learn with, as well as co-authors Christie Miranda, Blanca Guillen, and Dr. S. Hollis Woodard. Thank you to all of the amazing undergraduates Damaris Rodriguez-Arellano, Yadira Romero Diaz, Kate Neamsapaya, and Vanessa Uribe who also helped with experimental maintenance and watching videos of bumble bees for this project. Funding for the project came from the US-Israel Binational Science Foundation and the National Science Foundation. Chapter Three was completed in collaboration with Dr. Michelle Duennes and Dr. S. Hollis Woodard. I thank Dr. Jay Kirwood for assisting with metabolomics analysis. v Chapter Four is currently in revision at Ecology and Evolution in collaboration with co-authors Dr. Kristal M. Watrous, Dr. Leif L. Richardson, Dr. Neal M. Williams, and Dr. S. Hollis Woodard. Funding for this project came from U.S.D.A. A.P.H.I.S. I would also like to thank additional funding sources that supported various projects throughout my doctoral studies: UC-MEXUS, NRS Mathias Graduate Student Research Grant, and Shipley-Skinner. vi ABSTRACT OF THE DISSERTATION Feeding and Foraging in Bumble bees (Genus: Bombus): From the Organism to the Environment by Kaleigh Fisher Doctor of Philosophy, Graduate Program in Entomology University of California, Riverside, June 2021 Dr. S. Hollis Woodard, Chairperson Animal survival is dependent on the capacity to effectively find and consume nutritious food resources and avoid harmful components that may be present in food. This fundamental process operates at multiple scales in all animal species. The goal of this dissertation research was to establish a foundation for studying feeding and foraging in bumble bees at the scales of the organism, colony, insect-plant interactions, and the environment. Although bumble bee feeding and foraging behavior have been previously studied at most of these scales, there are several substantial gaps in our knowledge that this dissertation addresses. First, I first identified taste-related genes in Bombus impatiens and characterized the tissues in which these genes are expressed. I then examined how feeding and food-collection tasks are organized amongst workers in bumble bee colonies. Next, I tested whether pollen nutrients impact floral resource visitation in wild bumble bees. Finally, I examined what bumble bee species are present across several ecoregions vii in California. Together, this work provides a foundation to study the ecology and evolution of feeding and foraging in bumble bees. viii Table of Contents Introduction ……………………………………………………………………………...1 References ……………………………………………………………………...…7 Chapter 1: Tissue and caste related gene expression of gustatory receptors in the bumble bee Bombus impatiens Abstract…………………………………………………………………….……...8 Introduction…………………………………………………………………….….9 Materials and Methods…………………………………………………………...12 Results…...…………………………………………………………….…………16 Discussion…...…………………………………………………………….….….31 References...…………………………………………………………….…...…...37 Chapter 2: Worker task organization in incipient bumble bee nests Abstract…………………………………………………………………….…….41 Introduction…………………………………………………………………....…42 Materials and Methods…………………………………………………………...46 Results…...…………………………………………………………….…………61 Discussion…...…………………………………………………………….….….84 References...…………………………………………………………….…...…...94 Chapter 3: Pollen nutrients: a key feature of plant-pollinator interactions Abstract…………………………………………………………………….…...106 Introduction…………………………………………………………………......107 Materials and Methods……………………………………………………….....109 ix Results…...…………………………………………………………….………..115 Discussion…...………………………………………………………………….123 References...…………………………………………………………….…...….130 Chapter 4: A contemporary survey of bumble bee diversity across the state of California Abstract…………………………………………………………………….…...133 Introduction…………………………………………………………………......134 Materials and Methods……………………………………………………….…137 Results…...…………………………………………………………….………..141 Discussion…...………………………………………………………………….150 References...…………………………………………………………….…...….159 Conclusion…………………………………………………………………………......166 x List of Figures Figure 1.1: Gustatory receptor gene tree. Tree was constructed using the neighbor joining method. The tree is rooted at Gr1 and Gr2, which are highly conserved across insects, which suggests they are the more basal gene group…………………………….18 Figure 1.2: Ionotropic receptor gene tree. Tree was constructed using the neighbor joining method. The tree is rooted at IR8a and IR25a, which are highly conserved across insects, which suggests they are the more basal gene group…………………………….20 Figure 1.3: Normalized counts of gustatory receptor gene expression in queens and workers. Points are jittered for easier visualization of overlapping points (width +/- 0.05; height +/- 2)……………………………………………………..……………………….24 Figure 1.4: Non-metric multidimensional scaling of samples based on similarity in GR expression of tissue and caste. Distance between points represents similarity in gene expression. Internal tissues were more similar to each other compared to external tissues. Greater similarity within a caste compared to between castes was not observed………..25 Figure 1.5: Normalized counts of ionotropic receptor gene expression. Points are jittered for easier visualization of overlapping points (width +/- 0.05; height +/- 2)…………….28 Figure 1.6: Non-metric multidimensional scaling of samples based on similarity in IR expression of tissue and caste. Distance between points represents similarity in gene expression. Internal tissues were more similar to each other compared to external tissues. Greater similarity within a caste compared to between castes was not observed. Fat body was dissimilar to brain within the internal tissues………………………………………30 Figure 2.1: Shannon diversity index for tasks in nests. A) Shannon task diversity for each tasks based on social configuration; W3 = Three Workers; W5 = Five Workers; QW3 = Queen + Three Workers; QW5 = Queen + Five Workers. Black dots represent mean Shannon diversity across all groups. Egg laying and pollen collection tasks were performed with more exclusivity (i.e., by fewer observed individuals) than nectar collection and brood feeding tasks (GLMM p < 0.0001). Brood feeding was more exclusive (lower Shannon
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