A Common Regulatory Architecture Shapes Queen Chemical Signals Across Multiple Exocrine Sites.

Abstract

Insects communicate identity, health, and reproductive state through diverse chemicals secreted from multiple glands and production sites. Although these exocrine sites often contain a similar profile of compounds, they are usually studied in isolation. Here, we tested the hypothesis that changes in the identity and abundance of chemical signals from different exocrine sites within the same individual are coordinated, suggesting they may be governed by shared regulatory processes. To do so, we quantified the cuticular lipids and the glandular secretion of three exocrine glands in bumble bee queens across three key life stages: unmated newly-emerged queen (gynes), young founders shortly after nest initiation and old founders towards the end of the life cycle. We found that as queens aged and transitioned into reproduction, they produced hydrocarbons and esters with shorter chain length and shifted toward a greater investment in alkenes over alkanes across several exocrine sites. Terpenoid-, acetate- and wax-esters were produced across multiple exocrine sites with partially overlapping patterns. These remarkably coordinated shifts across glands that differ in both function and anatomical origin suggest that the overall chemical profile of an insect is coordinated across glandular sites and may convey more biologically relevant information than any single glandular secretion alone. Insect chemical communication is likely shaped by a shared regulatory architecture or coordinated responses to environmental conditions, highlighting a unifying mechanism underlying complex social signals.