NATURAL HISTORY AND SOCIOGENETIC ORGANIZATION OF THE BEE HALICTUS FARINOSUS (HYMENOPTERA: HALICTIDAE) IN NORTHERN UTAH JENNIFER ALBERT A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE GRADUATE PROGRAM IN BIOLOGY YORK UNIVERSITY TORONTO, ONTARIO AUGUST 2012 ©JENNIFER ALBERT, 2012 Library and Archives Bibliotheque et Canada Archives Canada Published Heritage Direction du Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington Ottawa ON K1A0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-90067-3 Our file Notre reference ISBN: 978-0-494-90067-3 NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliotheque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par I'lnternet, preter, telecommunication or on the Internet, distribuer et vendre des theses partout dans le loan, distrbute and sell theses monde, a des fins commerciales ou autres, sur worldwide, for commercial or non­ support microforme, papier, electronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. 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Canada Abstract Nesting biology, phenology and sociobiology were studied in an aggregation of the primitively eusocial ground-nesting bee Halictus farinosus in Northern Utah. Nest architecture was typical of the genus but key phenological events were delayed up to two weeks when compared to earlier studies of the same population. Bees were genotyped at six variable microsatellite loci to reveal kin structure within each nest. Polyandry was uncommon in H. farinosus queens whose population wide effective mating frequency was 1.07. The queen produced the vast majority of the brood (98%) while she was present and workers took over reproduction upon being orphaned. There were significant differences in sex ratios between female-biased queenright and male- biased queenless nests (t = -3.72, p = 0.003). Together these results generally agree with the predictions of inclusive fitness theory and support the view that haplodiploidy is important in the evolution of eusociality. ii Acknowledgements This work was funded by an NSERC discovery grant awarded to Dr. Laurence Packer. I would like to sincerely thank a number of people for their contribution to the project. I am grateful to Terry Griswold for sharing his expertise and helping me initiate my field study. He and his wife Rhonda also graciously welcomed me into their home during my field season. I would like to thank David Trew for his help with nest excavations and for answering my many questions over the last few years. I am grateful to Dr. Scott Tarof, Dr. Amro Zayed, Dr. Robert Paxton and Pat Kramer for their lab related advice and assistance and to Dr. Cory Sheffield for his assistance with the analysis. A special thanks to Stefanie Cargnelii for all of her hard work assisting me in the lab. My thanks also go to Jessica Albert, whose skillful editing has vastly improved the work. Finally, I am ever grateful to my supervisor Dr. Laurence Packer for his help with my field study and for his comments on the many versions of my thesis. His advice, encouragement and guidance over the years have been invaluable to me. To Mom, Dad and Tom who supported me emotionally and financially during this process, I dedicate this thesis to you. iii Table of Contents Abstract ii Acknowledgements iii Table of Contents Iv List of Tables v List of Figures vi Chapter One: Introduction 1 Chapter Two: Nesting biology and phenology of Halictus farinosus (Hymenoptera: Halictidae) in Northern Utah 12 Abstract 13 Introduction 13 Methods 16 Results 20 Discussion 26 Tables and Figures 31 Chapter Three: Sociogenetic organization in the primitively eusocial bee Halictus farinosus (Hymenoptera: Halictidae) 50 Abstract 51 Introduction 51 Methods 55 Results 60 Discussion 66 Conclusion 73 Tables and Figures 75 References 82 iv List of Tables Table 2-1: List of all excavated nests 31 Table 2-2: Comparison of phenological events between years of study 33 Table 2-3: Comparison of H.farinosus nest sizes between 2002 and 2012 34 Table 2-4: Ovary development and matedness in queens and workers 35 Table 2-5: Comparison of social and life history traits between social Halictus 36 Table 3-1: Microsatellite primers and variability in H.farinosus 75 Table 3-2: Estimates of relatedness in worker and reproductive brood 76 Table 3-3: Summary of kin structure in reproductive brood nests 77 Table 3-4: Sociobiological data in all excavated nests 78 v List of Figures Figure 2-1: Percentage of brood in different developmental stages 37 Figure 2-2: Halictus farinosus nests (external) 38 Figure 2-3: Internal structure of a typical H. farinosus nest (Or4b) 39 Figure 2-4: Proportion of nests where the queen was present at excavation 40 Figure 2-5: Head widths of H. farinosus workers and queens 41 Figure 2-6: Wing lengths of H. farinosus workers and queens 42 Figure 2-7: Head width vs. wing length in adult females 43 Figure 2-8: Difference in mandible and wing wear between each queen and her workers 44 Figure 2-9: Mandible wear in queens and workers 45 Figure 2-10: Wing wear in queens and workers 46 Figure 2-11: Average daily maximum and minimum temperatures in the summer months for the years of study in Logan, Utah 47 Figure 2-12: Total rainfall per summer month for the years of study in Logan Utah 48 Figure 2-13: Cumulative degree days between March and August in years of study with key phenological markers 49 Figure 3-1: Genetic relatedness among females in all genotyped nests 80 Figure 3-2: Size difference between replacement queen and workers 81 vi Chapter One: Introduction 1 In nature there are numerous examples of cooperation among individuals, including altruistic behaviour. An action is considered altruistic when it comes at the expense of the actor's personal fitness in terms of breeding potential but enhances the fitness of another individual. Eusociality is essentially an extreme example of altruism. A eusocial society is defined by three characteristics: a reproductive division of labour between members, overlapping generations, and intergenerational help with rearing the brood (Wilson, 1971). In eusocial societies the helpers often form a sterile worker caste that exist to help the queen produce the brood by provisioning resources and helping to construct and defend the nest. Within the context of Darwin's theory of evolution by natural selection the origin of a sterile caste that does not contribute directly to the next generation becomes all the more difficult to explain: how do some individuals forgo reproduction if it is through reproducing that the genes for such behaviour would be passed on? Darwin himself recognized this problem, admitting that it initially seems "insuperable and actually fatal to the whole theory" (Darwin, 1859). There are two essential difficulties with the evolution of sterility in workers. First is the paradox of the inheritance of sterility when the trait is necessarily carried by individuals who do not produce progeny. Secondly, it seems that sterility would never be selectively advantageous (Crozier, 2008). Darwin attempts to explain inheritance of the trait, saying that "selection may be applied to the family as well as the individual" (Darwin, 1859) indicating that selection can occur on multiple levels, not just at the level of the individual but at the colony level as well. Modern group selection emphasizes the 2 competition between groups as a more significant driving force in selection than the competition between members of the group (Wilson and Holldobler, 2005; Nowak at al., 2010). Group selection theory stands in opposition to kin selection theory, which is discussed further in this review, although it has been suggested that the two do not differ empirically in their expectations or mathematical framework (Queller, 1992; Gardiner et al., 2007; West et al., 2007a). In 1964 William D. Hamilton published two papers that contained the first mathematical proof that altruism can be explained by evolutionary theory without invoking selection operating at a level "above" the individual (Hamilton, 1964 a, b). Hamilton's rule states that a particular behaviour is selectively favoured when it leads to a net increase in the inclusive fitness of the actor. Mathematically it is represented as follows: br — c > 0. Where c is the lifetime cost to the productivity of the actor behaving altruistically, b is the lifetime benefit of the behaviour to the recipient and r is the coefficient of relatedness between the two individuals. This statistic describes in genetic terms how closely related the actor is to the beneficiary relative to the genetic similarity in the general population (Frank, 1998; West et al., 2007b).