Substances in the mandibular glands mediate queen effects on larval development and colony organization in an annual bumble bee

Social organization is commonly dynamic, with extreme examples in annual social insects, but little is known about the underlying signals and mechanisms. Bumble bee larvae with close contact to a queen do not differentiate into gynes, pupate at an earlier age, and are commonly smaller than siblings that do not contact a queen. We combined detailed observations, proteomics, microRNA transcriptomics, and gland removal surgery to study the regulation of brood development and division of labor in the annual social bumble bee Bombus terrestris. We found that regurgitates fed to larvae by queens and workers differ in their protein and microRNA composition. The proteome of the regurgitate overlaps significantly with that of the mandibular (MG) and hypopharyngeal glands (HPG), suggesting that these exocrine glands are sources of regurgitate proteins. The proteome of the MG and HPG, but not the salivary glands, differs between queens and workers, with caste-specificity preserved for the MG and regurgitate proteomes. Queens subjected to surgical removal of the MG showed normal behavior, brood care, and weight gain, but failed to shorten larval development. These findings suggest that substances in the queen MG are fed to larvae and influence their developmental program. We suggest that when workers emerge and contribute to larval feeding, they dilute the effects of the queen substances, until she can no longer manipulate the development of all larvae. Longer developmental duration may allow female larvae to differentiate into gynes rather than to workers, mediating the colony transition from the ergonomic to the reproductive phase.