Bumble bee queens initiate nests solitarily and transition to living socially once they successfully rear their first cohort of offspring. Bumble bees are disproportionately important for early season pollination, and many populations are experiencing dramatic declines. In this system, the onset of the social stage is critical for nest survival, yet the mechanisms that facilitate this transition remain understudied. Further, the majority of conservation efforts target the social stage of the bumble bee life cycle and do not address the solitary founding stage. We experimentally manipulated the timing of worker emergence in young nests of bumble bee (Bombus impatiens) queens to determine whether and how queen fecundity and survival are impacted by the emergence of workers in the nest. We found that queens with workers added to the nest exhibit increased ovary activation, accelerated egg laying, elevated juvenile hormone (JH) titres and also lower mortality relative to solitary queens. We also show that JH is more strongly impacted by the social environment than associated with queen reproductive state, suggesting that this key regulator of insect reproduction has expanded its function in bumble bees to also influence social organization. We further demonstrate that these effects are independent of queen social history, suggesting that this underlying mechanism promoting queen fecundity is reversible and short lived. Synchronization between queen reproductive status and emergence of workers in the nest may ultimately increase the likelihood of early nesting success in social systems with solitary nest founding. Given that bumble bee workers regulate queen physiology as we have demonstrated, the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories and ultimately nesting success. Collectively, our findings underline the importance of conservation interventions for bumble bees that support the early nesting period and facilitate the production and maintenance of workers in young nests.

Studies on the physiological states of wild-caught organisms are essential to uncovering the links between ecological and physiological processes. Bumble bee queens emerge from overwintering in the spring. At this time, queens develop their ovaries and search for a nest site in which to start a colony. Whether these two processes, ovary development and nest-searching, interact with or influence one another remains an unresolved question in behavioral physiology. We explored the hypothesis that ovary development and nest-searching might be mechanistically connected, by testing whether (1) ovary development precedes nest-searching behavior; (2) nest occupation precedes ovary development; or (3) ovary development and nest-searching occur independently, in bumble bee (Bombus vosnesenskii) queens. We collected queens either nest-searching (and thus prior to occupying a nest) or pollen-collecting (and thus provisioning an occupied nest) and measured their degree of ovary activation. We further screened these queens for parasites or other symbionts, to identify additional factors that may impact their reproductive success at this time. We found that queens searched for and occupied nests at all stages of ovary development, indicating that these processes occur independently in this system. Nest-searching queens were more likely to have substantial mite loads than pollen-collecting queens, who had already located and occupied a nest. However, mite loads did not significantly predict ovary developmental status. Collectively, our work shows that nesting status and symbionts alone are insufficient to explain the variation in spring bumble bee queen ovary development. We propose that ovary development and nest-searching occur opportunistically, which may enable queens to begin laying eggs earlier in the season than if these processes occurred in discrete succession.

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