Abstract
A male-specific component, 11-cis-vaccenyl acetate (cVA) works as an anti-aphrodisiac pheromone in Drosophila melanogaster. The presence of cVA on a male suppresses the courtship motivation of other males and contributes to suppression of male-male homosexual courtship, while the absence of cVA on a female stimulates the sexual motivation of nearby males and enhances the male-female interaction. However, little is known how a male distinguishes the presence or absence of cVA on a target fly from either self-produced cVA or secondhand cVA from other males in the vicinity. In this study, we demonstrate that male flies have keen sensitivity to cVA; therefore, the presence of another male in the area reduces courtship toward a female. This reduced level of sexual motivation, however, could be overcome by pretest odor exposure via olfactory habituation to cVA. Real-time imaging of cVA-responsive sensory neurons using the neural activity sensor revealed that prolonged exposure to cVA decreased the levels of cVA responses in the primary olfactory center. Pharmacological and genetic screening revealed that signal transduction via GABAA receptors contributed to this olfactory habituation. We also found that the habituation experience increased the copulation success of wild-type males in a group. In contrast, transgenic males, in which GABA input in a small subset of local neurons was blocked by RNAi, failed to acquire the sexual advantage conferred by habituation. Thus, we illustrate a novel phenomenon in which olfactory habituation positively affects sexual capability in a competitive environment.
Highlights
To determine the anti-aphrodisiac potency of cis-vaccenyl acetate (cVA), we performed a behavioral assay using a double-layered chamber (Fig 1A) in which a naïve male housed in the upper cell was exposed to various amounts of cVA in the lower cell under the mesh barrier and examined for its behavior toward a virgin female as a courtship target housed in the upper cell
We found that virgin females with no or as little as 0.02 ng cVA elicited high levels of courtship behavior from the males, while the presence of cVA over the mesh barrier decreased the courtship level of the males (Fig 1B)
Habituation is defined as decrement of behavioral response to an iterative stimulus and is considered as the simplest form of learning and memory; it allows animals to filter out irrelevant stimuli of diminishing relevance and focus selectively on important stimuli [40,41,42,43,44]
Summary
11-cis-vaccenyl acetate (cVA) is a volatile male pheromone component of the fruit fly Drosophila melanogaster. Since a mated female will not accept a second courting male and avoids further copulation, it is feasible for a male to judge the partner's mating status by the presence or absence of cVA and adjust his courtship activity . It has been unclear how male flies distinguish presence or absence of a tiny amount of cVA on the female target fly from other nearby males in a complex olfactory environment and make an appropriate courtship decision. We found that the presence of another male or cVA in the area reduces the courtship motivation of a male toward a female This inhibition could be overcome by pretest odor exposure and olfactory habituation to cVA or male odor. We discovered that habituation allowed wild-type males to gain a sexual advantage in a competitive courtship environment that GABAA mutant males failed to acquire
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