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An olfactory receptor for food-derived odours promotes male courtship in Drosophila

If food be the food of love... Courtship is a costly business in terms of both time and energy, so animals must make sure that they've found a willing partner before making the effort — a job often done through pheromone communication. Now Richard Benton and colleagues have discovered that frui...

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Published in:Nature (London) 2011-10, Vol.478 (7368), p.236-240
Main Authors: Grosjean, Yael, Rytz, Raphael, Farine, Jean-Pierre, Abuin, Liliane, Cortot, Jérôme, Jefferis, Gregory S. X. E., Benton, Richard
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Language:English
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Summary:If food be the food of love... Courtship is a costly business in terms of both time and energy, so animals must make sure that they've found a willing partner before making the effort — a job often done through pheromone communication. Now Richard Benton and colleagues have discovered that fruitfly males also need the proximity of good food before they commit to a courtship routine. They identify a member of a recently described chemosensory ion-channel family — Ionotropic receptor 84a — as key to sensing fruit-derived aromatics and gating pheromone-sensing neuronal pathways that control courtship routines. Such cross-talk between olfactory and pheromonal circuits constitutes a previously unrecognized evolutionary mechanism coupling reproductive behaviour to good feeding and oviposition sites. Many animals attract mating partners through the release of volatile sex pheromones, which can convey information on the species, gender and receptivity of the sender to induce innate courtship and mating behaviours by the receiver 1 . Male Drosophila melanogaster fruitflies display stereotyped reproductive behaviours towards females, and these behaviours are controlled by the neural circuitry expressing male-specific isoforms of the transcription factor Fruitless (FRU M ) 2 , 3 , 4 , 5 . However, the volatile pheromone ligands, receptors and olfactory sensory neurons (OSNs) that promote male courtship have not been identified in this important model organism. Here we describe a novel courtship function of Ionotropic receptor 84a (IR84a), which is a member of the chemosensory ionotropic glutamate receptor family 6 , in a previously uncharacterized population of FRU M -positive OSNs. IR84a-expressing neurons are activated not by fly-derived chemicals but by the aromatic odours phenylacetic acid and phenylacetaldehyde, which are widely found in fruit and other plant tissues 7 that serve as food sources and oviposition sites for drosophilid flies 8 . Mutation of Ir84a abolishes both odour-evoked and spontaneous electrophysiological activity in these neurons and markedly reduces male courtship behaviour. Conversely, male courtship is increased—in an IR84a-dependent manner—in the presence of phenylacetic acid but not in the presence of another fruit odour that does not activate IR84a. Interneurons downstream of IR84a-expressing OSNs innervate a pheromone-processing centre in the brain. Whereas IR84a orthologues and phenylacetic-acid-responsive neurons are present in diver
ISSN:0028-0836
1476-4687
DOI:10.1038/nature10428