Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female

Abstract

Quiescence, or a sleep-like state, is a common and important feature of the daily lives of animals from both invertebrate and vertebrate taxa, suggesting that sleep appeared early in animal evolution. Recently, Drosophila melanogaster has been shown to be a relevant and powerful model for the genetic analysis of sleep behaviour. The sleep architecture of D. melanogaster is sexually dimorphic, with females sleeping much less than males during day-time, presumably because reproductive success requires greater foraging activity by the female as well as the search for egg-laying sites. However, this loss of sleep and increase in locomotor activity will heighten the risk for the female from environmental and predator hazards. In this study, we show that virgin females can minimize this risk by behaving like males, with an extended afternoon 'siesta'. Copulation results in the female losing 70 per cent of day-time sleep and becoming more active. This behaviour lasts for at least 8 days after copulation and is abolished if the mating males lack sex peptide (SP), normally present in the seminal fluid. Our results suggest that SP is the molecular switch that promotes wakefulness in the post-mated female, a change of behaviour compatible with increased foraging and egg-laying activity. The stress resulting from SP-dependent sleep deprivation might be an important contribution to the toxic side-effects of male accessory gland products that are known to reduce lifespan in post-mated females.

Figure 1.

Sexually dimorphic locomotor rhythms of Oregon R flies ((a) virgin males; (b) female mated to wild-type male; (c) virgin females; (d) females mated to spermless males) entrained in a 12 : 12 h light : dark cycle. Locomotor activities are expressed as number of beam breaks in 30 min (mean ± s.e.m., n = 22). White and black bars indicate day-time and night-time, respectively. Time is expressed as zeitgeber time with 0 h being the time of lights-on and 12 h being the time of lights-off.

Figure 2.

Mating results in loss of day-time sleep (a,b) and a reduction in sleep onset latency (c) in female Oregon R flies (filled circle, virgin female; open square, mated female; filled triangle, male). White and black bars in (a) and (b) indicate day-time and night-time, respectively. Sleep is expressed as minutes of sleep/hour (mean ± s.e.m., n = 22). *p < 0.0001, statistical significance of the difference in (i) day-time sleep between females mated to wild-type Oregon R males and virgin Oregon R males and females, (ii) sleep latency between virgin females and either females mated to wild-type Oregon R males or virgin Oregon R males (Student's t-test). A sleep period was defined as a 5 min period with no locomotor activity and sleep latency was the time in minutes between lights-off and the first recorded night-time sleep period. Time is expressed as zeitgeber time.

Figure 3.

Mating-induced changes in sleep behaviours of female Oregon R flies are dependent upon male SP. Sleep and sleep latency are defined as in legend to figure 2 (filled circle, virgin; filled triangle, mated to SP⁰ male; open square, mated to wild-type male). Unlike wild-type males (wt, SP⁺), males lacking SP (SP⁰) do not elicit a change in total day-time sleep (a,b) and do not reduce sleep-onset latency (c) of post-mated female flies. White and black bars in (a) and (b) indicate day-time and night-time, respectively. Values are means ± s.e.m., n = 20–23. *p < 0.0002, statistical significance of the differences in sleep and sleep latency between females mated to wild-type males (SP⁺) and either virgin females or females mated to SP⁰ males (Student's t-test). Time is expressed as zeitgeber time.

Figure 4.

SP-dependent loss of total day-time sleep in female (Oregon R) flies persists for 10 days before returning to ‘virgin’ levels by day 14. Data for day 9 were omitted because flies were transferred to fresh food on this day. Values of total day-time sleep are means ± s.e.m., n = 20–23. **p < 0.00 001, *p < 0.05, statistical significances of the differences in daylight sleep between virgin females and females mated to wild-type SP⁺ males (Student's t-test; open bar, virgin; hatched bar, mated to SP⁰ male; dotted bar, mated to wt male).