Molecular Mechanisms of Phenotypic Variation in Honey Bees (Apis mellifera)

A Dissertation in Molecular, Cellular, and Integrative Biosciences, in partial fulfillment of the requirements for the degree of Doctor of Philosophy (PhD) from The Graduate School at The Pennsylvania State University.

May 30th, 2024, 12-1pm (EST), W-203 Millennium Science Complex, University Park, PA, 16803

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Dissertation Committee

  • Christina Grozinger - Publius Vergilius Maro Professor, Department of Entomology, Director of Center for Pollinator Research, Dissertation Co-Advisor, Co-Chair of Committee
  • Michael Axtell - Professor, Department of Biology, Louis and Hedwig Sternberg Chair in Plant Biology, Dissertation Co-Advisor, Co-Chair of Committee
  • Shaun Mahony - Associate Professor, Department of Biochemistry and Molecular Biology
  • Heather Hines - Associate Professor, Department of Biology
  • Amro Zayed - Professor, Department of Biology, York University, Toronto, Ontario, Canada, York Research Chair in Genomics


Phenotypic variation is essential for evolution—it is the raw material on which natural selection acts—and has been demonstrated for numerous traits, including behavior in animals. Behaviors are among the most plastic of phenotypes, and individuals from the same population often vary substantially and consistently in their behavioral responses to the same stimuli. In social groups, behavioral variation underlies the flexible task repertoires which facilitate collective responses to changing environments. Studying the proximate and ultimate mechanisms underlying variation in complex behaviors can shed light on the adaptive significance of these traits, how they arise and why and how they persist in different populations. In this dissertation, I evaluate the molecular mechanisms of phenotypic variation in the honey bee (Apis mellifera), which exhibits extreme examples of behavioral variation between nestmates. In chapter 1, I evaluate variation in tissue-specific transcriptional profiles associated with seasonal differences in behavior and physiology between summer and winter bees. In chapters 2-4, I examine multiple behavioral contexts (worker aggression, receptivity to queen pheromone, ovary activation, and queen-worker caste determination during larval development) in which parent-of-origin intragenomic conflicts are predicted to arise and contribute to phenotypic variation. I test predictions of the Kinship Theory of Intragenomic Conflict, which proposes that alleles derived from the mother (matrigenes) versus the father (patrigenes) can have different strategies for maximizing their reproductive fitness—with conflicting effects on development and behavior—and these different selective pressures lead to opposite expression patterns of matrigenes and patrigenes. Since these selective advantages and expression differences arise from the origin of the gene (whether it is derived from the mother or the father) and not the gene sequence, understanding how these parent- of-origin expression differences are regulated and selected for provides a fascinating framework in which to uncover principles of gene regulation, and examine how proximate and ultimate mechanisms interact to influence gene expression and phenotypic outcomes. To this end, chapters 2-4 also evaluate multiple mechanisms of gene regulation that may drive parent-of-origin expression differences in this species, including piRNAs, RNA methylation, and histone post-translational modifications.