Changes in Female Drosophila Sleep following Mating Are Mediated by SPSN-SAG Neurons

Abstract

Female Drosophila melanogaster, like many other organisms, exhibit different behavioral repertoires after mating with a male. These postmating responses (PMRs) include increased egg production and laying, increased rejection behavior (avoiding further male advances), decreased longevity, altered gustation and decreased sleep. Sex Peptide (SP), a protein transferred from the male during copulation, is largely responsible for many of these behavioral responses, and acts through a specific circuit to induce rejection behavior and alter dietary preference. However, less is known about the mechanisms and neurons that influence sleep in mated females. In this study, we investigated postmating changes in female sleep across strains and ages and on different media, and report that these changes are robust and relatively consistent under a variety of conditions. We find that female sleep is reduced by male-derived SP acting through the canonical sex peptide receptor (SPR) within the same neurons responsible for altering other PMRs. This circuit includes the SPSN-SAG neurons, whose silencing by DREADD induces postmating behaviors including sleep. Our data are consistent with the idea that mating status is communicated to the central brain through a common circuit that diverges in higher brain centers to modify a collection of postmating sensorimotor processes.

TheDrosophilaPost-mating Response: Gene Expression and Behavioral Changes Reveal Perdurance and Variation in Cross-Tissue Interactions

“…We discover that both daytime and nighttime sleep are increased post-mating in tud progeny females without a germline, whereas nighttime sleep is decreased post-mating in control tud progeny females with a germline. This sleep result is distinct from previous studies that found daytime post-mating sleep decreased in all strains but white Berlin (Isaac et al 2010;Garbe et al 2016;Dove et al 2017). We find that the female post-mating preference for yeast-containing media is independent of presence of eggs and receipt of sperm.…”

“…Sleep: We examine differences in sleep post-mating, as to our knowledge, sleep has not been assayed in females lacking a germline (Table S1 for publication summary; for sleep statistical tests see Figure S6 and Table S5). Previous work has shown that mating results in decreased daytime sleep, across multiple strains, including CS, Oregon R, iso 31 , and w 1118 , but not white Berlin (see Table S1; Isaac et al 2010;Garbe et al 2016;Dove et al 2017). In female strains with a germline (CS, Berlin and tud/+), we confirm that CS has a significant post-mating reduction in daytime sleep, whereas Berlin had a significant increase in daytime sleep ( Figure S6A and B and Table S5).…”

“…These signaling pathway interactions are also important for the female post-mating response (PMR), which includes increased egg laying (Chen et al 1988) and feeding (Carvalho et al 2006), a preference for both yeast and salt instead of carbohydrates (Ribeiro and Dickson 2010;Vargas et al 2010;Walker et al 2015), decreased intestinal transit (Cognigni et al 2011;Apger-Mcglaughon and Wolfner 2013), decreased receptivity to mating (Manning 1962;Chen et al 1988;Aigaki et al 1991;Chapman et al 2003), decreased daytime sleep (Isaac et al 2010;Garbe et al 2016;Dove et al 2017) and lowered immune response (Fedorka et al 2007;Short and Lazzaro 2010;Short et al 2012). During copulation, peptides are transferred to the female in the male seminal fluid that induce the PMR (reviewed in Wolfner 1997;Wolfner 2002;Avila et al 2011;Sirot et al 2014).…”

The Effect of Mating and the Male Sex Peptide on Group Behaviour of Post-mated Female Drosophila melanogaster

“…SP appears to be the molecular switch that changes the behavior of post-mated females by increasing locomotor activity and reducing sleep [33]. A similar response to mating by female D. melanogaster was also observed in other studies and in the related fruit fly D. suzukii, which also receives SP in the male seminal fluid [46,20,47]. showed that a 5-day enriched social experience amongst same and mixed sex adults can substantially increase the amount and quality of sleep of individuals compared to flies that have been deprived of any social interactions from eclosion [48].…”

Most sleep does not serve a vital function. Evidence from Drosophila melanogaster

“…3B) and the strong increase in micro-movements (Fig. 3C) are likely to represent an increase in food intake and egg-laying activity and may explain why such a strong decline in sleep amount was never identified using different tools (27,43,44). Interestingly, four-dimensional behavioural fingerprinting showed that the short sleep phenotype observed upon mating is qualitatively different from the one observed as natural variation in the CantonS population ( …”