Odor coding of nestmate recognition in the eusocial ant Camponotus floridanus

Abstract

In eusocial ants, aggressive behaviors require the ability to discriminate between chemical signatures such as cuticular hydrocarbons that distinguish nestmate friends from non-nestmate foes. It has been suggested that a mismatch between a chemical signature (label) and the internal, neuronal representation of the colony odor (template) leads to aggression between non-nestmates. Moreover, a definitive demonstration that odorant receptors are responsible for the processing of the chemical signals that regulate nestmate recognition has thus far been lacking. To address these issues, we have developed an aggression-based bioassay incorporating highly selective modulators that target odorant receptor functionality to characterize their role in nestmate recognition in the formicine ant Camponotus floridanus . Electrophysiological studies were used to show that exposure to either a volatilized antagonist or an agonist eliminated or dramatically altered signaling, respectively. Administration of these compounds to adult workers significantly reduced aggression between non-nestmates without altering aggression levels between nestmates. These studies provide direct evidence that odorant receptors are indeed necessary and sufficient for mediating aggression towards non-nestmates. Furthermore, our observations support a hypothesis in which rejection of non-nestmates depends on the precise decoding of chemical signatures present on non-nestmates as opposed to the absence of any information or the active acceptance of familiar signatures. Summary: Broad inhibition as well as activation of peripheral odorant receptor signaling decreases aggression between non-nestmate ants consistent with a ‘lock-and-key’ model that requires OR-based detection of unambiguous non-nestmate chemical labels.