Identification of an ant queen pheromone regulating worker sterility

Abstract

The selective forces that shape and maintain eusocial societies are an enduring puzzle in evolutionary biology. Ordinarily sterile workers can usually reproduce given the right conditions, so the factors regulating reproductive division of labour may provide insight into why eusociality has persisted over evolutionary time. Queen-produced pheromones that affect worker reproduction have been implicated in diverse taxa, including ants, termites, wasps and possibly mole rats, but to date have only been definitively identified in the honeybee. Using the black garden ant Lasius niger, we isolate the first sterility-regulating ant queen pheromone. The pheromone is a cuticular hydrocarbon that comprises the majority of the chemical profile of queens and their eggs, and also affects worker behaviour, by reducing aggression towards objects bearing the pheromone. We further show that the pheromone elicits a strong response in worker antennae and that its production by queens is selectively reduced following an immune challenge. These results suggest that the pheromone has a central role in colony organization and support the hypothesis that worker sterility represents altruistic self-restraint in response to an honest quality signal.

Figure 1.

3-MeC₃₁ is a condition-dependent queen pheromone that affects worker physiology and behaviour in L. niger. (a) The cuticular hydrocarbon profile of queens contains a 6 times higher proportion of 3-MeC₃₁ than that of a worker, while the egg profile has 9 times more; see also electronic supplementary material, table S1. (b) Supplementation of queenless groups of workers with synthetic 3-MeC₃₁ negatively affected ovarian activation relative to controls. Bars show the frequency distributions of ovary activation on a categorical scale from 1 (no activation) to 4 (highest activation). (c) Glass model queens coated with 3-MeC₃₁ were attacked by workers less often than controls. (d) A lipopolysaccharide immune challenge reduced the proportion of 3-MeC₃₁ on the cuticle of queens. (a,c,d) Means ± 1 s.e.; shared letters indicate that two groups are not significantly different. Sample size is shown inside the bars.

Figure 2.

The queen pheromone 3-MeC₃₁ elicits a strong response in worker antennae. Response of worker antennae (n = 25) to the five treatment solutions, relative to the pentane control. The plots show the estimated effect ±1 s.e. from contrasts of a mixed model with antenna as a random factor and treatment order as a covariate; a value of zero indicates an antennal response equal to that of the control (pentane only) stimulus. Only 3-MeC₃₁ produced a significantly higher (starred; p < 0.05) electrophysiological response than the control.