Division of labor is a central facet of complex societies. Task specialization by individual members of the society (theoretically) increases the overall productivity and the fitness of the group. The work presented in this dissertation extends existing knowledge about the regulation of task-related behavioral states at the level of the individual and social group by using the honeybee as a model organism. Chapter 1 reviews the extensive literature regarding the contribution of endocrine signaling (including endocrine-mediated transcriptional cascades) to division of labor in the social Hymenoptera. It also presents a theoretical framework for the evolution of division of labor via the cooption and neofunctionalization of endocrine-mediated signaling and transcription and suggests future lines of research to investigate these phenomena. Chapter 2 investigates the transcriptomic architecture underlying two of the tasks associated with division of labor (broodcare and foraging) using a novel combination of RNA sequencing and informatic analyses. In addition to identifying a key set of transcription factors (TFs) as putative regulators of broodcare or foraging behavior, it presents findings that suggest that coherent modules of coregulated genes are critical for task-related behavioral states. It thereby extends our understanding of how division of labor might be regulated at the transcriptomic level. Chapter 3 probes the regulatory logic underlying this architecture by investigating whether connections between TFs and their targets are labile. Using both bioinformatic analyses and RNAi coupled to behavioral assays and endocrine treatments, it presents significant evidence that the TF-target connectivity can be rewired as a function of behavioral state, social context and neuroendocrine state. This demonstrates how behavioral plasticity related to division of labor can arise at the transcriptomic level. Finally, Chapter 4 links division of labor to social networks involving trophallaxis (exchange of oral secretions and food). It shows that not only are task-related behaviors associated with differences in social interactivity, but that group-level social properties can be altered by hormone treatments that shift division of labor. Chapter 4 also demonstrates that certain emergent properties (such as information flow) are unaffected by such treatments and may represent core features of trophallactic communication in bees. As such, the findings presented in this chapter represent an important first step toward deciphering the role of direct communication in mediating division of labor
