Mechanisms of sleep plasticity due to sexual experience in Drosophila melanogaster

Abstract

Sleep can be altered by an organism's previous experience. For instance, female Drosophila melanogaster experience a post-mating reduction in daytime sleep that is purportedly mediated by sex peptide (SP), one of many seminal fluid proteins (SFPs) transferred from male to female during mating. In the present study, we first characterized this mating effect on sleep more fully, as it had previously only been tested in young flies under 12h light/12h dark conditions. We found that mating reduced sleep equivalently in 3-day-old or 14-day-old females, and could even occur in females who had been mated previously, suggesting that there is not a developmental critical period for the suppression of sleep by mating. In conditions of constant darkness, circadian rhythms were not affected by prior mating. In either constant darkness or constant light, the sleep reduction due to mating was no longer confined to the subjective day but could be observed throughout the 24-hour period. This suggests that the endogenous clock may dictate the timing of when the mating effect on sleep is expressed.We recently reported that genetic elimination of SP only partially blocked the post-mating female siesta sleep reduction, suggesting that the effect was unlikely to be governed solely by SP. We found here that the daytime sleep reduction was also reduced but not eliminated in females mated to mutant males lacking the vast majority of SFPs. This suggested that SFPs other than SP play a minimal role in the mating effect on sleep, and that additional non-SFP signals from the male might be involved. Males lacking sperm were able to induce a normal initial mating effect on female sleep, although the effect declined more rapidly in these females. This result indicated that neither the presence of sperm within the female reproductive tract nor female impregnation are required for the initial mating effect on sleep to occur, although sperm may serve to prolong the effect.Finally, we tested for contributions from other aspects of the mating experience. NorpA and eya2 mutants with disrupted vision showed normal mating effects on sleep. By separating males from females with a mesh, we found that visual and olfactory stimuli from male exposure, in the absence of physical contact, could not replicate the mating effect. Further, in ken/barbie male flies lacking external genitalia, courtship and physical contact without ejaculation were also unable to replicate the mating effect. These findings confirmed that the influence of mating on sleep does in fact require male/female contact including copulation, but may not be mediated exclusively by SP transfer.