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Molecular Phylogenetic Analysis of the Bees (Hymenoptera), with an Emphasis on Apidae and the Evolutionary History of Social and Cleptoparasitic Behavior

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Molecular Phylogenetic Analysis of the Bees (Hymenoptera), with an Emphasis on Apidae and the Evolutionary History of Social and Cleptoparasitic Behavior MOLECULAR PHYLOGENETIC ANALYSIS OF THE BEES (HYMENOPTERA), WITH AN EMPHASIS ON APIDAE AND THE EVOLUTIONARY HISTORY OF SOCIAL AND CLEPTOPARASITIC BEHAVIOR A Dissertation Presented to the Faculty of the Graduate School of Cornell University in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Sophie Carole Cardinal February 2010 © 2010 Sophie Carole Cardinal MOLECULAR PHYLOGENETIC ANALYSIS OF THE BEES (HYMENOPTERA), WITH AN EMPHASIS ON APIDAE AND THE EVOLUTIONARY HISTORY OF SOCIAL AND CLEPTOPARASITIC BEHAVIOR Sophie Carole Cardinal, Ph.D. Cornell University 2010 Apidae (Hymenoptera) is the most speciose family of bees with over 5600 species. The family is notable for having some of the most important pollinators of managed crops, yet also comprises a rich diversity of social and parasitic lifestyles, host plant affinities, and ecosystem services. Despite its importance, relationships among the tribes within Apidae remain unclear. To date, rigorous phylogenetic analysis has been challenged by long-standing assumptions about the relatedness of cleptoparasitic groups in relation to their hosts. I performed the first large-scale phylogenetic study of the family Apidae based on DNA sequence data, including representative taxa from all 33 apid tribes. I then used this phylogeny to investigate the origins and antiquity of cleptoparasitism and sociality. Results indicate that most cleptoparasitic apid bees form a monophyletic group, and therefore stem from a single origin of cleptoparasitism (with two more origins in the Euglossini orchid bees and one in the tribe Ctenoplectrini). Divergence time analysis using a relaxed fossil- calibrated molecular clock model reveals that cleptoparasitism is an ancient behavior in apid bees that first evolved ~100 Ma. Results also indicate that primitive eusociality is the ancestral state for corbiculate Apidae, and that orchid bees represent a reversal from eusociality to solitary, communal, and weakly social behavior. According to my divergence time analysis, eusociality first evolved ~87 Ma in the corbiculates, much earlier than in other groups of bees. To date the origin of bees and their major clades, I performed a phylogenetic analysis of bees including representatives from every subfamily, and almost all tribes, using sequence data from seven genes. I then conducted a fossil-calibrated relaxed clock divergence time analysis. I estimate that bees originated at the start of the Aptian, concurrently with the origin of the eudicot angiosperms. All of the major bee clades are estimated to have originated during the middle to late Cretaceous, which is when angiosperms diversified to becom the dominant group of land plants. This study firmly establishes temporal overlap in the diversification of bees and angiosperms, a necessary precondition for the role of bees in the angiosperms’ rise to dominance during the late Cretaceous. BIOGRAPHICAL SKETCH Sophie grew up in New Liskeard, a small town in northern Ontario. An arch south of town inscribed with “Gateway to the North” declares a certain pride of latitude. Meanwhile, local agricultural pride is expressed by Miss Claybelt, an 18-foot high fiberglass Holstein cow. More important to Sophie however, is the large francophone community found in this area – a community she grew up in, with French as her first language, and that she was proud to be a part of. Nevertheless, like many rebellious teenagers she was inspired to leave the land of Miss Claybelt to study marine biology, attending Dalhousie University in Halifax, Nova Scotia, for the first two years of her B.Sc. (Biology). She then transferred to the University of Toronto to complete her B.Sc. where her interests shifted to entomology. There, she was fortunate to work for Prof. Chris Darling (Royal Ontario Museum/U of T). Long hours spent in the museum pinning and labeling insects from Vietnam is what got her seriously interested in insect systematics. She then attended York University (Toronto) for her M.Sc. (Biology) with Prof. Laurence Packer. Here her interests shifted from parasitoid wasps to bees. At the time she believed that she would one day return to working on parasitoid wasps, but then she discovered cleptoparasitic bees, and she knew that my PhD. would have to focus on them. In 2004, she began her Ph.D. at Cornell University (Ithaca, New York) with Prof. Bryan Danforth. During her dissertation, she has travelled to Arizona, French Guiana, Paraguay and South Africa to collect and study bees. In January 2010, she will continue to work in Dr. Danforth’s lab as a postdoctoral associate. iii ACKNOWLEDGMENTS I am most indebted to my advisor, Bryan N. Danforth, for both accepting me into his lab and, more importantly, for providing me with invaluable support and encouragement throughout my Ph.D. I am also thankful to my committee members, James L. Liebherr and Anurag Agrawal, for their advice, constructive criticism and editing of my dissertation. I also benefitted from participating in classes and discussion groups led by Jim and Anurag during my time at Cornell. Members of the Danforth lab throughout the years have contributed greatly to my professional and personal development. I am thankful to Eduardo Almeida, Jennifer Fang, Neha Bodapati, Kojun Kanda, and Andrew Debevec for assistance in the lab. Over the years, Eduardo, Jesse Litman, and Margarita Lopez-Uribe have not only shared with me their enthusiasm and knowledge about bees and phylogenetics, but more importantly their friendship. I am especially grateful to Jesse and Margarita for their support over the last few years. My family has always supported me unconditionally throughout my life and the time during my dissertation was no exception. They have always made sure that I know that they are proud of me and wish only the best for me. I could also always count on my parents to take care of Chebucto when I had to leave on longer bee- collecting trips. Chebucto is in part to credit for the maintenance of my sanity at times through his constant affection, general excitement and enthusiasm for the simpler things in life (especially cardboard boxes). I am indebted to Chris Darling and Laurence Packer for my time spent in their labs before coming to Cornell. I never would have made it to the point of starting a Ph.D. without the help, encouragement and training that both of them provided for me. iv Some of my most insightful conversations at Cornell have been with Stuart Campbell. His questions and comments have pushed me to better understand the logic behind the work that I do. This dissertation was also greatly improved by comments and careful editing provided by Stuart. His support, encouragement and love during the last few stages of my thesis have convinced me not just to settle for that which is acceptable but to expect more from myself and life. For that, I will always be grateful. The Hortorium Systematics Discussion Group led by Kevin Nixon helped me develop some critical thinking skills and prevented me from becoming overly zealous about molecular phylogenetics. I have also greatly benefited from discussions with people here at Cornell who are too numerous to name. I am grateful to John Ascher for his help with some of the bee identifications and to Jerome G. Rozen, Jr., and Charles D. Michener for discussing my thesis with me and sharing their amazing wealth of knowledge on all that is bees. Most of the funding for the research came from a National Science Foundation Research Grant to B.N. Danforth (DEB- 0412176) and a Doctoral Dissertation Improvement Grant. Funding for the field trips was provided by the Grace Griswold Fund (Cornell University), the A.C. Rawlins Endowment (Cornell University), the Theodore Roosevelt Memorial Fund (AMNH), and The Einaudi Center International Travel Grant (Cornell University). My graduate studies were funded through teaching assistantships in the introductory biology course, research assistantships, the Palmer Fellowship, and the Bradley Fellowship. v TABLE OF CONTENTS Biographical sketch.......................................................................................................iii Acknowledgments.........................................................................................................iv Table of Contents..........................................................................................................vi List of Figures...............................................................................................................vii List of Tables.................................................................................................................ix Chapter 1. Comprehensive phylogeny of apid bees (Apidae: Hymenoptera) reveals the evolutionary origins and antiquity of cleptoparasitism...................................................1 Chapter 2. Phylogeny of apid bees reveals the evolutionary history and antiquity of eusociality...................................................................................................................123 Chapter 3. Simultaneous origins of bees and eudicots: implications for Darwin's abominable mystery....................................................................................................152 vi LIST OF FIGURES Figure 1.1. Known host-parasite relationships of apid cleptoparasites...........................4 Figure 1.2. Previously hypothesized apid relationships..................................................7 Figure 1.3. Bayesian maximum clade credibility tree
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