Honey bee retinue workers respond similarly to queens despite seasonal differences in Queen Mandibular Pheromone (QMP) signaling

Authors: Carroll, Mark; Brown, Nicholas; Ruetz, Zachary; Ricigliano, Vincent; Anderson, Kirk

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/4/2023
Publication Date: 9/28/2023
Citation: Carroll, M.J., Brown, N.J., Ruetz, Z.J., Ricigliano, V.A., Anderson, K.E. 2023. Honey bee retinue workers respond similarly to queens despite seasonal differences in Queen Mandibular Pheromone (QMP) signaling. PLOS ONE. 18(9). Article e0291710. https://doi.org/10.1371/journal.pone.0291710.
DOI: https://doi.org/10.1371/journal.pone.0291710

Interpretive Summary: Worker honey bees are able to detect the presence and quality of their queen through her release of Queen Mandibular Pheromone (QMP) pheromone chemicals. QMP pheromones attract workers to feed and take care of the queen (retinue worker behavior) and prevent workers from rearing new replacement queens. Retinue workers remove QMP pheromones from the queen’s body and spread it by contact to other worker bees in the colony. Poor quality queens (injured, sick, starving, old, pesticide-exposed, or poorly-mated) usually release less QMP pheromones than higher quality queens.When QMP levels are low, workers often rear a new replacement queen. However, the effects of common colony stressors (overwintering, poor nutrition, disease, parasites, and pesticides) on this system (QMP signaling and worker responses) are poorly understood. We examined the effects of seasonal changes (July to January overwintering) on queen releases of four QMP pheromones. The colonies used here were from a warm subtropical location where brood rearing and queen egg-laying do not stop in winter (Imperial Valley of California, USA). We also examined seasonal changes in queen care and feeding of queens by retinue workers. We determined whether queen QMP releases reflected queen reproductive quality (“matedness” - amount of stored sperm left in the queen and queen ovary nutrient quality) and whether worker retinue responses reflected queen QMP releases. Queen releases of all QMP compounds changed from summer to mid-winter. Queen releases of three QMP compounds (HOB, 9-HDA, and 9-ODA) decreased from July to January while queen releases of one QMP compound (HVA) increased in January. Despite these seasonal differences in queen QMP releases, retinue workers fed and tended queens in similar numbers through the study. Queens did not vary by month in matedness or physiological age, but queens differed in how much nutrients they had in their ovaries. Queen ovaries contained more protein in September than in November or January, and more lipids in July and September than in November and January. Surprisingly, queen QMP compound releases did not vary with the queen’s reproductive quality (QMP was not an “honest signal” of queen quality) and retinue worker number did not vary with queen QMP release levels. These results show that factors other than queen QMP signaling alone are responsible for retinue worker behaviors. These results also suggest that queen QMP release levels may not be good predictors of queen care by retinue workers in colonies during seasonal stress.

Technical Abstract: Honey bee colonies maintain viable queens in part through communication with Queen Mandibular Pheromone (QMP), a mixture that signals the queen’s presence and reproductive quality to workers. In turn, workers are thought to provide retinue queen care or replace queens partially based on QMP profiles. We examined the effects of seasonal dearth (overwintering in a warm subtropical location) on queen-worker interactions. Retinue worker responses to continuously ovipositing queens were considered in view of QMP signaling and queen reproductive quality. QMP signaling was estimated from QMP residues recovered from nest worker bodies, which is the primary mode of QMP transfer from the queen to the colony at large. QMP residues varied seasonally but not at all with queen reproductive quality (spermatheca sperm storage, ovary protein and lipid contents). 9-HDA and 9-ODA were lower in January than other months. HOB decreased from July to January, while HVA, a component associated with mated queens, increased sharply in January. Despite these seasonal signaling differences, retinue workers attended queens at similar levels through the months. In terms of reproductive quality, queens did not differ over the months in matedness (spermatheca sperm storage) or physiological age (protein carbonyl content), but varied in nutrient allocation to reproductive and non-reproductive tissues. Queen ovaries contained more protein in September than in November, and more lipid in July and September than in November and January. Queen fat bodies had more protein in July than September or November, but less lipid in July and September than November or January. Retinue worker responses did not vary with seasonal QMP changes, but reflected overall continuous brood rearing efforts and queen matedness throughout the year. The absence of seasonal differences in worker responses to QMP should be considered in the broader context of continuous reproductive efforts in warm subtropical colonies.