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.

A social insect fertility signal is dependent on chemical context

“…This result contrasts with other primer-effect experiments, wherein a compound presented without the normal chemical background inhibited worker ovarian development [11][12][13].…”

“…This hypothesis remains largely untested owing to the small number of experimentally identified signals of caste or reproductive status. Experimental studies identifying the primer effect of queen hydrocarbon fertility signals in which a single compound is introduced to workers suggest that compounds without chemical background can mimic the presence of a queen by inhibiting worker ovarian development [11][12][13]. However, these compounds occur naturally only in the context of the entire chemical profile of an individual or an egg.…”

The origin and dynamic evolution of chemical information transfer

“…sex, age and fertility; e.g. [52][53][54]) than chemicals with low molecular weight, but they are less conspicuous to receivers. We, therefore, propose that in this situation selection for more effective communication will primarily result in adding signal components to the informative but inconspicuous substances.…”

Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

“…Chemical signals are for example used in ant nestmate recognition (Lahav et al, 1999), which is crucial for the colony cohesion and inclusive fitness benefits, directing the altruistic behavior to colony mates. Furthermore, chemical signals (pheromones) are used to control and suppress reproduction by other queens or workers and to stimulate specific worker tasks, for example to make them take care of larvae (Holman et al, 2010). Thus, social life involves unique long-lasting selection pressures.…”