Honeybee communication during collective defence is shaped by predation

BACKGROUND: Social insect colonies routinely face large vertebrate predators, against which they need to mount a collective defence. To do so, honeybees use an alarm pheromone that recruits nearby bees into mass stinging of the perceived threat. This alarm pheromone is carried directly on the stinger; hence, its concentration builds up during the course of the attack. We investigate how bees react to different alarm pheromone concentrations and how this evolved response pattern leads to better coordination at the group level. RESULTS: We first present a dose-response curve to the alarm pheromone, obtained experimentally. This data reveals two phases in the bees’ response: initially, bees become more likely to sting as the alarm pheromone concentration increases, but aggressiveness drops back when very high concentrations are reached. Second, we apply Projective Simulation to model each bee as an artificial learning agent that relies on the pheromone concentration to decide whether to sting or not. Individuals are rewarded based on the collective performance, thus emulating natural selection in these complex societies. By also modelling predators in a detailed way, we are able to identify the main selection pressures that shaped the response pattern observed experimentally. In particular, the likelihood to sting in the absence of alarm pheromone (starting point of the dose-response curve) is inversely related to the rate of false alarms, such that bees in environments with low predator density are less likely to waste efforts responding to irrelevant stimuli. This is compensated for by a steep increase in aggressiveness when the alarm pheromone concentration starts rising. The later decay in aggressiveness may be explained as a curbing mechanism preventing worker loss. CONCLUSIONS: Our work provides a detailed understanding of alarm pheromone responses in honeybees and sheds light on the selection pressures that brought them about. In addition, it establishes our approach as a powerful tool to explore how selection based on a collective outcome shapes individual responses, which remains a challenging issue in the field of evolutionary biology. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at (10.1186/s12915-021-01028-x).