The male-specific fly courtship song is thought to be generated by neurons in the thoracic ganglion, which are in turn controlled by descending neurons from the brain. However, the neural circuitry of these regions is anatomically very similar in males and females, so it was puzzling why females do not also sing for sex. Much of the reproductive behaviour of D. melanogaster stems from the actions of the various transcription-factor products of the fruitless (fru) gene, which is expressed only in neurons. Owing to alternative mRNA splicing, some of these proteins are gender-specific — the male-specific fru products are collectively known as FruM. Miesenböck and Clyne therefore investigated whether the lack of singing in females might be due to the gender-specific differences in Fru-protein-containing neurons.
They engineered flies that expressed a light-activatable cation channel under the control of the fru gene, and then exposed these flies' thoracic neurons to light. They found that photoactivation of these fru-expressing neurons readily induced singing in males. Remarkably, singing could also be induced in this manner in females, but only when a fourfold higher light intensity was used. This showed that the motor programme for singing can be turned on artificially in females, albeit at a higher activation threshold than is required for males.
Why, then, do females not normally sing? To investigate this matter, the authors generated FruM-expressing female flies. These FruM females, which have a largely male nervous system but an otherwise female physiology, could be induced to sing by the same light intensity as male flies. Furthermore, an analysis of the songs themselves revealed that, whereas the songs of the FruF female flies were off key, those of the FruM females were very similar to the true courtship song of normal male flies. Thus, neural components or properties that are specifically imparted by the actions of FruM are needed to activate the thoracic motor programme and control the execution of the courtship song.
This study shows that female D. melanogaster possess the motor programme that allows males to generate the courtship song, but that Fru-expression-dependent differences from the male neural circuitry prevent the programme being activated in females.