Shared neural circuitry for female and male sexual behaviours in Drosophila

Sexual reproduction in most species involves innate behaviours that are dramatically distinct in males and females. The different behaviours of males and females are generally thought to reflect the activation of sex-specific neural circuits; however, sex differences could also arise through the sex-specific modulation of circuits that are common to both sexes. Here, we present evidence that the sexspecific reproductive behaviours of females and males of the fruitfly Drosophila melanogaster indeed involve shared neural circuits. Male courtship behaviour is specified in Drosophila by the male-specific products of the fruitless (fru) gene, FruM [1], which are expressed in approximately 2% of the neurons in the male nervous system [2–4]. These neurons can be manipulated using fruGAL4, in which GAL4 coding sequences have been inserted into the fru locus [3,4]. In males, synaptic silencing of these fruGAL4 neurons, with a UAS-shits transgene, inhibits courtship behaviour [3,4] but leaves unrelated behaviours intact [3]. Corresponding neurons are present in females, and express fruGAL4 but not FruM. The functions of these neurons in females are unknown. We tested whether they might mediate female sexual behaviour. A virgin female responds to a male’s courtship song by slowing down and opening her vaginal plates to allow copulation. Virgin females in which the fruGAL4 neurons are synaptically silenced with UAS-shits are largely unreceptive to courting males (Figure 1A): fewer than 10% of fruGAL4 UAS-shits virgin females copulated within a 20 minute observation period (experiment 3), whereas approximately 50% of various control females copulated in the same period (experiments 1, 4, 5 and 10). This was not due to a passive failure to accept the male, but rather an active rejection behaviour in which the female extends her ovipositor to prevent mating (Figure 1B). In addition, we found that silencing the fruGAL4 neurons in virgin females induces them to lay their unfertilized eggs (Figure 1C). These rejection and egg-laying behaviours are characteristic of mated females (Figure 1, experiment 2). Thus, synaptic activity of the fruGAL4 neurons is required in virgin females to promote mating behaviour and to inhibit post-mating reproductive behaviours. We observed that, in females forced to express FruM (fruM females), male courtship behaviour is induced and certain virgin and mated female behaviours are suppressed