Honeybee communication during collective defence is shaped by predation

Abstract

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.

Extracting individual characteristics from population data reveals a negative social effect during honeybee defence

“…With this methodology, we obtained results consistent with previous findings on how stinging likelihood varies depending on the SAP concentration, based on individual measurements [ 21 ]. Furthermore, we validated our prediction by demonstrating that individual bees become less likely to sting as the group grows larger, for any given SAP concentration.…”

“…Notice that rewriting the stinging condition in this form (stinging condition A j > θ k ) may suggest an interpretation that the aggressiveness is fixed and the stinging threshold changes in response to the concentration level k . Such an interpretation is different from the one the model is originally built upon (stinging condition A j + Δ k > θ 0 ), that aggressiveness changes with stinging events, as this is the known action of the alarm pheromone at a large range of concentration levels [ 21 ]. Since the two interpretations are mathematically equivalent, for the purpose of presentation clarity, we will further represent the stinging condition by A j > θ k .…”

“…Second, model selection is performed between two biologically plausible hypotheses. In particular, we explore whether the parameters follow either a linear or a sigmoidal trend [ 21 ].…”

From inter-group conflict to inter-group cooperation: insights from social insects

“…Indeed, the above examples notwithstanding, group-level combat among conspecifics is relatively rare in the social insects. The weaponry borne by social insect workers is primarily used to defend their resources (stored food and vulnerable proteinrich brood) from heterospecific predators and kleptoparasites, rather than from conspecifics [22,25,26]. Many conspicuous colony-level conflicts are in fact attempts to withstand heterospecific robbing [22,27,28].…”

Olfactory Strategies in the Defensive Behaviour of Insects

“…A recent study on honeybees shows that they become more likely to sting as the alarm pheromone concentration increases, however, this aggressive response drops back when very high concentrations of alarm pheromone are reached. This mechanism may help to prevent a disproportionate defensive response [ 84 ]. In another study, it was shown that the concentration of the alarm pheromone component varied between exotic species of fire ants ( Solenopsis richteri , S. invicta , and their hybrid S. richteri × S. invicta ) and the native Solenopsis geminata —thus suggesting a potential link between alarm pheromone production and invasion success [ 85 ].…”