Reproductive Conflicts and Signal Evolution in Social Wasps and Bees 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 Kevin Joseph Loope August 2015 © 2015 Kevin Joseph Loope REPRODUCTIVE CONFLICTS AND SIGNAL EVOLUTION IN SOCIAL WASPS AND BEES Kevin Joseph Loope, Ph. D. Cornell University 2015 Chapter 1 (published in Naturwissenshaften) is a side project on honeybee behavior. We showed that honeybee colonies that are headed by queens who are artificially inseminated with the sperm of a single drone have egg-eating policing behavior, just like colonies with naturally mated, highly polyandrous queens. Chapter 2 is an ESS-style model of worker reproduction in honeybee colonies, suggesting that workers may invest in selfish reproduction if they sense the queen may be about to die. Chapter 3 (published in BMC Evolutionary Biology) addresses the evolution of multiple mating in the Vespine wasps. First, I used microsatellite markers to describe how many patrilines are present in colonies of five wasp species, four of which are in the enigmatic Vespula rufa species group, and the last a facultative social parasite of another species of yellowjacket. I also performed a comparative analysis of paternity number and paternity skew across 21 species of yellowjacket wasps and hornets (Vespidae: Vespinae). Species with larger colonies have higher average paternity frequencies and lower average paternity skew, with interesting implications for the evolution of polyandry in this group. Chapters 4 and 5 focus on the adaptive significance of matricide in Dolichovespula arenaria, an aerially nesting yellowjacket wasp. I describe matricide for the first time in this species, and use experiments and genetic analyses to show that in natural and lab colonies, queens that are killed are typically those who have mated few times, or who use sperm in a strongly biased way, resulting in high worker relatedness. Queens who have mated multiply and use sperm evenly are rarely killed, supporting the hypothesis that workers kill queens as a result of conflict over the production of males. Experiments suggested that queens laying only male eggs do not trigger matricide, nor does an abrupt drop in queen fecundity, contrary to theoretical predictions. Chapter 6 examines the evolution of cuticular hydrocarbon diversity across the polistine wasps, and provides evidence that the diversity of recognition compounds correlates with social organization, suggesting that these compounds have evolved in response to their function in recognition behavior. BIOGRAPHICAL SKETCH Kevin was born and raised in Lincoln, Nebraska in a family who loves the natural world. Frequent trips to the American West and abroad almost certainly bent him toward biology and graduate school. He attended the Lincoln Public Schools, with two years at “Zoo School”, the science focus program housed at the Lincoln Children’s Zoo. He left Nebraska for the University of Wisconsin, Madison, graduating in 2007 with degrees in Mathematics and Zoology. Most influential was the time spent in Costa Rica in 2006: a semester in Monteverde with CIEE, followed by a summer near Cañas, collecting data for a senior thesis project on nest construction in a social wasp. Here and afterward he was inspired by his advisor, Bob Jeanne, to take a stab at a career studying the social behavior of insects, particularly social wasps. But the reason he went to Costa Rica in the first place was the rave review from Elizabeth Hunter, his future spouse, who he met in Madison in 2005. After graduating, they spent a whirlwind year traveling, working field jobs in the west, and volunteering in Costa Rica, before moving to Ithaca, NY where he started grad school in 2008After several early field seasons working with tropical wasps in Costa Rica, he switched to projects in Ithaca with honey bees and local yellowjacket wasps. Along the way he spent considerable time in Syracuse, where Elizabeth lived during her Masters, and Athens, GA, where she is working on a PhD. Next, they move to Riverside, CA, for a postdoc with Erin Wilson Rankin. vi ACKNOWLEDGMENTS This dissertation was the result of seven years of support, discussion, collaboration and encouragement from many, many mentors, collaborators, friends and family members. First, I am indebted to my committee who gave me the freedom to explore the questions I wanted with the organisms I chose. Tom Seeley was a supportive advisor who let me figure out what I wanted to study, and made sure I had what I needed to make fieldwork a success at Liddell and elsewhere. Without his support and patience, my various projects may have been cut short before the exciting results turned up. It was also wonderful to spend a summer learning honey bees with Tom. Heather Mattila was also very generous and fun to work with that summer, hosting me at Wellseley and providing advice and encouragement later on. Kern Reeve shares my fascination with conflict within cooperative groups, and was at the center of the group of students and postdocs working on this topic when I first got to Cornell. His modeling advice, excitement, and typically brilliant suggestions about additional analyses or overlooked connections to previous work made meetings valuable and fun. Although Paul Sherman was only around for half of my time at Cornell, he was very encouraging of my work on matricide and pushed me to test my hypotheses more directly. Cole Gilbert was a phenomenal outside committee member. He helped me develop surgical methods, was always happy to chat about my work and about science in general, and he gave great comments on drafts of this manuscript. I must also express great gratitude to several non-committee faculty. First, I thank Rob Raguso, for training me in GC-MS methods and for helping me with so much of my methodology. Rob was generous with his lab space, his knowledge and his time. I regret that the CHC project didn’t end up being a collaboration with him, but I always very much appreciated our conversations, and his voluminous advice. Conversations with Kerry Shaw in my last year at Cornell really opened my eyes to the wider field of evolutionary biology and the different approaches to tackling evolutionary questions. Her friendship and mentorship were an unforeseen but extremely valuable part of my time at Cornell. Finally, Patrizia D’Ettorre, at U. Paris 13, generously trained me in CHC analysis methods, hosted me in Paris, and has been a vii great collaborator. For my comparative analysis in Chapter 6, Rick Hoebeke, Jason Dombroskie, Jim Carpenter, Jim Hunt and especially Joan Strassmann were extremely generous with their time and specimens. The vast majority of my training and support came from other graduate students and postdocs. Martin von Arx generously trained me to do EAG recordings. Julian Kapoor taught me microsatellite data collection and analysis, and most of my results would not exist were it not for his generosity. Julian has been a phenomenal sounding board for ideas and an inspirational field biologist, engineer, programmer, chef and friend. Julie Miller, Jessie Barker, Caitlin Stern all share my passion for the evolution of cooperation and conflict, and provided the core group I could always rely on for feedback and interesting discussion. They are also great friends. Michael Smith is a logistical genius, a great sounding board and collaborator, and a creepy but good friend. David Peck provided great conversations about parasites, social insects, experimental design and many other things. Paul Shamble made me understand how amazing mimicry is, and how curious naturalists should think. Becky Cramer is/was a great role model for productivity, curiosity and work/life balance. Barrett Klein provided great advice and was a wonderful role model and friend during our shared summer at Liddell. Gil Menda has been a great friend and fellow bee and wasp enthusiast. Shinichi Asao, Patty Jones, Susan Whitehead, Bonnie Waring, Kellie Kuhn, Bernal Matarrita and Danilo Brenes made La Selva fun, despite my experimental woes. Ben Freeman, Nick Mason, and Jake Berv helped me understand phylogenetics and comparative analyses. Shane Peace is an invaluable friend who helped me stay sane. Matt Lewis provided excellent rants. My parents have always been encouraging, supportive and proud of me. I’m grateful to my brother, Garrison, for his help and his patience putting up with my tropical flailing during a season in Costa Rica. Finally, and most of all, I thank Elizabeth Hunter, for helping me appreciate my successes, get over my failures, learn statistics, think about ecology, and live a happier and more balanced life. viii TABLE OF CONTENTS Biographical Sketch ....................................................................................................................... vi Acknowledgements ....................................................................................................................... vii Chapter 1. No facultative worker policing in the honey bee (Apis Mellifera L.) .......................... 1 References ................................................................................................................................. 11 ! ! Chapter 2. Queen loss and worker reproduction in honey bees and other social insects ............ 14 References ................................................................................................................................