The making of a queen: Hormonal regulation of female caste in the social bee Bombus impatiens

The process of queen production is unique to social insects which exhibit reproductive division of labor between non-reproductive workers and fecund queens that differ in behavior, physiology, and morphology. This phenotypic plasticity is regulated by both environmental and genetic factors, often during larval development, leading to the production of two female castes. Mechanistically, external factors are thought to translate into hormonal changes affecting molting and body mass, but detailed regulation is known for only a handful of species. The bumblebee Bombus impatiens is an important model for understanding sociality, yet how long-lived, fecund queens, which are three times larger than workers, develop from the same totipotent egg remains unknown. Here, we examine the role of juvenile hormone in caste differentiation by directly manipulating exogenous JH during larval development. We found that JH influences larval fate indirectly through JH-treated workers, leading to queen differentiation within a narrow critical period toward the end of larval development. Using labeled JH, we further showed that JH applied to workers is incorporated into larval provisioning and ultimately detected in larval bodies. In addition, exogenous JH application reduced endogenous JH titers, indicating a feedback loop between hemolymph levels and hormone synthesis. These findings demonstrate that caste differentiation in B. impatiens is hormonally regulated through socially mediated JH transfer by workers, providing a mechanistic framework for understanding endocrine regulation of social morph differentiation.