The Molecular Basis for Nestmate Recognition in the Eusocial Ant Camponotus floridanus

Abstract

BackgroundIn eusocial ants, aggressive behaviors require a sophisticated ability to detect and 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 the recognition of and subsequent aggression between non-nestmates. While several studies have demonstrated that ant chemosensory systems, most notably olfaction, are largely responsible for the decoding of these chemical signatures, a definitive demonstration that odorant receptors are responsible for the detection and processing of the pheromonal signals that regulate nestmate recognition has thus far been lacking. To address this, we have developed an aggression-based bioassay incorporating a suite of highly selective odorant receptor modulators to characterize the role of olfaction in nestmate recognition in the formicine ant Camponotus floridanus.\n\nResultsValidation of our aggression-based behavioral assay was carried out by demonstrating an antennal requirement for nestmate recognition. In order to adapt this bioassay for the volatile delivery of Orco modulators, electroantennography was used to show that both a volatilized Orco antagonist (VUANT1) and an Orco agonist (VUAA4) eliminated or otherwise interfered with the electrophysiological responses to the hydrocarbon decane, respectively. Volatilize administration of these compounds to adult workers significantly reduced aggression between non-nestmates without altering aggression levels between nestmates but did not alter aggressive responses towards a mechanical stimulus.\n\nConclusionsOur studies provide direct evidence that the antennae (as olfactory appendages) and odorant receptors (at the molecular level) are necessary for mediating aggression towards non-nestmates. Furthermore, our observations support a hypothesis in which rejection of non-nestmates depends on the precise detection and decoding of chemical signatures present on non-nestmates as opposed to the absence of any information or the active acceptance of familiar signatures. In addition to describing a novel approach to assess olfactory signaling in genetically intractable insect systems, these studies contribute to a long-standing interest in odor coding and the molecular neuroethology of nestmate recognition.