The possible role of ritualized aggression in the vibration signal of the honeybee, Apis mellifera

•We explored the evolution of the honeybee vibration signal through ritualized aggression.•Queenless vibrators had active ovaries and performed aggressive mauling.•Vibrators had greater expression of aggression-related genes compared to recipients.•Signal performance may involve a genetic module associated with aggression.

Cooperative activities in advanced insect societies are organized by complex systems of communication signals that may have evolved from interactions among nestmates in primitively social ancestors. Primitively social colonies are organized by dominance and aggression, which suggests that some communication signals in advanced societies may have evolved through ritualized aggression. For example, many primitively social insects perform repetitive body movements during aggressive encounters and such movements in ancestral species may have become ritualized into vibratory signals, such as ‘abdominal wagging’ in Polistes wasps, and the ‘vibration signal’ of the honeybee Apis mellifera. We explored this possibility by examining the performance of the vibration signal by queenless honeybee workers. Under typical colony conditions, the vibration signal helps to coordinate cooperative labour; however, the function of the signal under queenless conditions is poorly understood. When a colony is permanently queenless, the ovaries of some workers activate and there is a pronounced increase in overt aggression, expressed as ‘mauling’, in which workers attack nestmates with greater ovarian activation. Here, we show that workers that performed vibration signals throughout their adult lifetimes had greater ovarian activation and an increased tendency to perform mauling. These results suggest that vibration signal performance is associated with the reproductive competition that characterizes queenless colonies. We next compared brain–gene expression patterns in persistent queenless vibrators, persistent recipients and nonvibrating control bees, for eight candidate genes associated with aggressive nest defence in honeybees and dominance in the primitively social wasp Polistes metricus. Five of the eight genes were upregulated in persistent vibrators compared to recipients and controls. Our results are consistent with the idea that the vibration signal of the honeybee evolved from repetitive aggressive movements, perhaps by co-opting components of a conserved genetic module associated with aggression.