During mating season, love can literally be in the air. Many animals communicate about reproduction using pheromones. Male Drosophila produce the pheromone 11-cis-vaccenyl acetate (cVA). Food smelling of cVA attracts Drosophila, but females smelling of cVA inhibit male sexual advances. How are these signals transduced? Kurtovic et al. report that cVA acts at a single type of neuron to mediate opposite behaviors in male and female Drosophila in a recent article in Nature.
Each of the approximately 1300 Drosophila olfactory receptor neurons (ORNs) expresses one olfactory receptor. Of the roughly 60 G-protein-coupled olfactory receptors in Drosophila, indirect evidence from previous studies suggests that cVA acts at Or67d.
To determine the importance of Or67d in cVA response, the authors knocked the yeast transcription factor GAL4 into the Or67d locus and recorded cellular responses in T1 sensory units, or sensilla, which contain only Or67d ORNs. Treatment with cVA increased ORN firing in T1 sensilla from male and female control but not Or67d mutant Drosophila, suggesting that cVA specifically activates Or67d ORNs in both males and females.
Removal of the Or67d receptor made courtship behavior less discriminating in males and decreased courtship in females. Male Or67d mutant and control Drosophila courted wild-type females for similar lengths of time. However, Or67d mutant males courted wild-type males more than did control males. Or67d mutant males courted wild-type females rubbed with cVA, but control males did not, suggesting that Or67d signaling inhibits courtship behavior in male Drosophila. Although wild-type male Drosophila courted Or67d mutant and control females similarly, Or67d mutant females showed less receptivity to wild-type males than did control females, suggesting that Or67d signaling promotes sex behavior in female Drosophila. Together, these data indicate that cVA secreted by amorous males activates Or67d ORNs to promote mating behavior in females and inhibit mating behavior in competing males.
According to the authors, most odors act at a combination of different ORNs, but odors that are biologically important might act at a single type of ORN to communicate vital information quickly and without confusion. To determine whether pheromone detection involves the integration of multiple signals from combinations of ORN or dedicated activation of Or67d ORNs, the authors artificially activated Or67d ORNs. Female silkmoths release pheromones to attract males. The authors knocked the gene encoding the silkmoth pheromone receptor into the Or67d locus. Male Drosophila expressing the silkmoth receptor courted control females, but not females rubbed with silkmoth pheromone. In contrast, control and Or67d mutant male Drosophila courted wild-type and pheromone-rubbed females similarly. Therefore, specific activation of Or67d ORNs suppresses male courtship behavior, consistent with the 'labeled line' hypothesis of unambiguous communication of reproductive information.
How does activation of
ORNs in male and female
cause opposing behavioral responses? Signals from
ORNs terminate in two regions of the
brain that process sex pheromone signals. One of these regions is enlarged in males, and the other region is enlarged in females. According to the authors, differing synaptic connections may mediate sex-specific responses to cVA in male and female
.