fornicating female fruitless flies

A male fly's sexual courtship of a female fly is a complicated business of tapping, singing, wing vibration, and licking, but a single gene is all that is needed to produce this complex behavior, according to new research published in this week's issue of the journal Cell.

The gene encodes the Fruitless protein. Male and female flies carry different versions of the fruitless protein, as a result of sex-specific splicing of the mRNA. The male form of Fruitless is critical for the male courtship ritual and males' preference for mating with females, as previous studies have shown.

Now, Barry J. Dickson and Ebru Demir of the Institute of Molecular Biotechnology of the Austrian Academy of Sciences show just how intimately fruitless is linked to these stereotypically male behaviors. They discovered that female flies with the male version of fruitless behave like males, directing at other females a sexual display nearly identical to their male counterparts.

All animals exhibit innate behaviors that are specified during their development. Drosophila melanogaster males (but not females) perform an elaborate and innate courtship ritual directed toward females (but not males). Male courtship requires products of the fruitless (fru) gene, which is spliced differently in males and females. We have generated alleles of fru that are constitutively spliced in either the male or the female mode. We show that male splicing is essential for male courtship behavior and sexual orientation. More importantly, male splicing is also sufficient to generate male behavior in otherwise normal females. These females direct their courtship toward other females (or males engineered to produce female pheromones). The splicing of a single neuronal gene thus specifies essentially all aspects of a complex innate behavior.

Male-specific fruitless (fru) products (FruM) are both necessary and sufficient to “hardwire” the potential for male courtship behavior into the Drosophila nervous system. FruM is expressed in ∼2% of neurons in the male nervous system, but not in the female. We have targeted the insertion of GAL4 into the fru locus, allowing us to visualize and manipulate the FruM-expressing neurons in the male as well as their counterparts in the female. We present evidence that these neurons are directly and specifically involved in male courtship behavior and that at least some of them are interconnected in a circuit. This circuit includes olfactory neurons required for the behavioral response to sex pheromones. Anatomical differences in this circuit that might account for the dramatic differences in male and female sexual behavior are not apparent.