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Phylogenetic Systematics and the Evolution of Nesting PHYLOGENETIC SYSTEMATICS AND THE EVOLUTION OF NESTING BEHAVIOR, HOST-PLANT PREFERENCE, AND CLEPTOPARASITISM IN THE BEE FAMILY MEGACHILIDAE (HYMENOPTERA, APOIDEA) A Thesis 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 Jessica Randi Litman January 2012 ! ! ! ! ! ! ! ! © 2012 Jessica Randi Litman ! PHYLOGENETIC SYSTEMATICS AND THE EVOLUTION OF NESTING BEHAVIOR, HOST-PLANT PREFERENCE, AND CLEPTOPARASITISM IN THE BEE FAMILY MEGACHILIDAE (HYMENOPTERA, APOIDEA) Jessica Randi Litman, Ph.D. Cornell University 2012 Members of the bee family Megachilidae exhibit fascinating behavior related to nesting, floral preference, and cleptoparasitic strategy. In order to explore the evolution of these behaviors, I assembled a large, multi-locus molecular data set for the bee family Megachilidae and used maximum likelihood-, Bayesian-, and maximum parsimony-based analytical methods to trace the evolutionary history of the family. I present the first molecular-based phylogenetic hypotheses of relationships within Megachilidae and use biogeographic analyses, ancestral state reconstructions, and divergence dating and diversification rate analyses to date the antiquity of Megachilidae and to explore patterns of diversification, nesting behavior and floral preferences in the family. I find that two ancient lineages of megachilid bees exhibit behavior and biology which reflect those of the earliest bees: they are solitary, restricted to deserts, build unlined nests, and are host-plant specialists. I suggest that the use of foreign material in nest construction allowed early megachilid bees to escape their ancestral desert habitat and colonize temperate, previously uninhabitable areas. In order to further examine phylogenetic relationships among tribes of the family Megachilidae, I develop a novel bootstrapping algorithm designed to balance the signal from combined molecular-morphological datasets; I use the results of all phylogenetic analyses to propose a new subfamilial- and tribal-level classification for Megachilidae and present a revised key to the tribes of Megachilidae. I also reconstruct the evolutionary history of the tribe Anthidiini and offer the first molecular-based phylogenetic hypothesis of the generic and suprageneric relationships within Anthidiini based on maximum likelihood and Bayesian phylogenetic analyses. I trace the evolutionary history of nesting behavior, the origins of cleptoparasitism, and the evolution of cleptoparasitic strategy in the megachilid tribe Anthidiini using Bayesian ancestral state reconstructions. Our results indicate three suprageneric clades within Anthidiini: the Trachusa group, the Anthidium group, and the Dianthidium group; each of these groups shows a distinct preference for either plant fibers or plant resins as a primary nest-building material. Our phylogeny supports two origins of cleptoparasitism in Anthidiini and also supports the hypothesis that cleptoparasitic lineages with hospicidal adults are an evolutionary intermediate between nest-building bees and cleptoparasitic lineages with hospicidal larvae. BIOGRAPHICAL SKETCH Jessica Randi Litman was born on July 30, 1975 in Brooklyn, NY. She attended high school at Phillips Exeter Academy in Exeter, NH and graduated in 1993. Jessica received a BSc in biology from McGill University in Montreal, Quebec in 1998. After spending several years in South America, she attended Rutgers University in New Brunswick, NJ, where she received an MS in entomology in 2006. ! """! for christophe “...and this is the wonder that's keeping the stars apart...” ! "#! ACKNOWLEDGEMENTS First and foremost, I would like to thank my advisor, Bryan Danforth: for spending months reading papers with me at the beginning of my studies at Cornell until we put together the perfect project; for having the brilliant idea of studying a small tribe of desert-dwelling bees found only in the deserts of Africa and Chile and for encouraging me to travel to collect them; for patience, understanding and a rational voice in moments of academic anxiety; for his enthusiasm for unexpected things, like Jean-Henri Fabre and Weetabix, some of which I came to love (Fabre), and others of which I did not (Weetabix); for understanding when I spent the last year of my Ph.D. away from Ithaca; and finally for being a good advisor and a good friend. Many thanks to the other members of my special committee, Brian Lazzaro and Jeff Doyle, for all of their support and constructive feedback during my studies at Cornell. Many generous agencies supplied funding for my projects. Many thanks to the National Science Foundation (grant DEB-0742998, awarded to Bryan Danforth and Terry Griswold); the National Geographic Society (grant 8448-08, awarded to Bryan Danforth); the Mario Einaudi Center at Cornell University; the Graduate School at Cornell University; the Griswold Endowment, awarded through the Cornell University Department of Entomology; the Rawlins Endowment, awarded through the Cornell University Department of Entomology; and the Linnean Society of London and the Systematics Association. I would like to thank the people with whom I went on bee collecting trips while at Cornell: Bryan Danforth, Terry Griswold, and Connal Eardley, for a fantastic first-ever collecting trip to South Africa to hunt for Fidelia; Sophie Cardinal, with whom I returned to ! #! South Africa to collect more Fidelia and with whom I saw my first warthog; and Jason Gibbs, who went with me to Chile to collect Neofidelia and who remained cheerful despite an unfortunate robbery on our first day in Santiago. Many people provided specimens that I was unable to collect myself and which were invaluable to my thesis. Thank you to Werner Arens, Sophie Cardinal, Victor Gonzalez, Terry Griswold, Michael Kuhlmann, Denis Michez, Andreas Müller, Laurence Packer, Sebastien Patiny, Christophe Praz, Jerry Rozen, Maximilian Schwarz and Claudio Sedivy. Many thanks also to Robert Paxton, Antonella Soro, and Andreas Müller, who provided valuable feedback on manuscripts, to Maximilian Schwarz, who provided helpful correspondence on Trachusa, and to Jim Liebherr, who provided helpful counsel on the naming of suprageneric anthidiine groups. I would like to express a million thanks to my family, for their love and unflagging support, especially to my parents and to Eric and Rachel. While at Cornell I made three wonderful friends who were more supportive of me than I ever deserved: Sophie Cardinal, who always knew when something wasn’t quite right, even when I was tucked away at my makeshift desk at the back of the lab; Margarita Lopez Uribe, who always listened and always understood; and Jacob Crawford, who always reminded me that there was more going on outside of lab than inside and with whom I spent many of my best hours in Ithaca. Special thanks also to Stuart Campbell, Sara DeLeon, Deb Leddy, and Luis Duque for awesomeness, love, and support. Thanks also to Gaylord Desurmont, Antonella Soro, Robert Paxton, Giulia Paxton, Laura Paxton, and Melanie Sifton for their good energy, support and loyal friendship. Finally, all of my love and gratitude to my husband, Christophe Praz, who shared his love of bees with me, who gave me thoughtful feedback on each chapter of my thesis, who was ceaselessly attentive and ! #"! supportive during these last months, and who was (and remains) my primary source of inspiration. ! #""! TABLE OF CONTENTS BIOGRAPHICAL SKETCH..........................................................................................................iii DEDICATION................................................................................................................................iv ACKNOWLEDGEMENTS.............................................................................................................v LIST OF FIGURES........................................................................................................................ix LIST OF TABLES......................................................................................................................... .x CHAPTER 1: A REVIEW OF THE BIOLOGY OF THE BEE FAMILY MEGACHILIDAE (HYMENOPTERA), WITH A FOCUS ON THE EVOLUTION OF NESTING BEHAVIOR, HOST-PLANT PREFERENCE, AND CLEPTOPARASITISM ..........................................................................................................................................................1 CHAPTER 2: WHY DO LEAFCUTTER BEES CUT LEAVES? NEW INSIGHTS INTO THE * EARLY EVOLUTION OF BEES ..............................................................................................59 CHAPTER 3: PHYLOGENETIC SYSTEMATICS OF THE BEE FAMILY MEGACHILIDAE, INCLUDING A NOVEL METHOD FOR BOOTSTRAPPING COMBINED MOLECULAR AND MORPHOLOGICAL DATA.............................................................................................110 CHAPTER 4: THE EVOLUTION OF NESTING BEHAVIOR AND CLEPTOPARASITISM IN THE BEE TRIBE ANTHIDIINI (HYMENOPTERA: MEGACHILIDAE)...............................154 !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! * This chapter has been published as: Litman J.R., Danforth B.N., Eardley C.D., Praz C.J. 2011. Why do leafcutter bees cut leaves? New insights into the early evolution of bees. Proceedings of the Royal Society B - Biological Sciences 278: 3593-3600. Reproduced with permission from Proceedings of the Royal Society B - Biological Sciences.! ! #"""! LIST OF FIGURES Figure 2.1 Maximum clade credibility
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