Mating disrupts morning anticipation inDrosophila melanogasterfemales

Abstract

After mating, the physiology of Drosophila females undergoes several important changes, some of which are reflected in their rest-activity cycles. To explore the hypothesis that mating modifies the temporal organization of locomotor activity patterns, we recorded the fly activity by a video tracking method. Monitoring rest-activity patterns under light/dark (LD) cycles indicated that mated females lose their ability to anticipate the night-day transition, in stark contrast to males and virgins; this postmating response is mediated by the sex peptide (SP) acting mainly on pickpocket (ppk) expressing neurons, since reducing expression of the SP receptor (SPR) in these neurons restores the ability to anticipate the LD transition in mated females. We further provide evidence of connectivity between PPK+ neurons and the pigment-dispersing factor (PDF)-positive ventral lateral neurons (sLNv), which play a central role in the temporal organization of daily activity. Since PDF has been associated to the generation of the morning activity peak, we hypothesized that the mating signal could modulate PDF levels. Indeed, mated females have reduced PDF levels at the dorsal protocerebrum; moreover, SPR downregulation in PPK+ neurons mimics PDF levels observed in males. In sum, our results are consistent with a model whereby mating-triggered signals reaches clock neurons in the fly central nervous system to modulate the temporal organization of circadian behavior according to the needs of the new status.Author SummaryAfter mating, Drosophila females undergoes striking behavioral changes, specially in their activity patterns. Despite some of the circuits that deliver mating signals to the female brain are known the connection with the circadian network has not been explored in detail. Here, we show that mating changes the onset of daily activity, masking a central function of the clock. This modulation is mediated by the sex peptide (transferred during courtship) acting on PPK+ neurons, which, in turn, directly contact PDF+ neurons, responsible for the increase of the activity that precedes dawn. Thus, our work identifies a postmating response directly related to the circadian clock, and begins to unravel the underlying neuronal circuit.

Time series transcriptome analysis implicates the circadian clock in the Drosophila melanogaster female’s response to sex peptide

“…So far our analysis identified networks that respond to SP, but it did not give information about how SP coordinates changes across networks. Because a non-SP aspect of mating (in the first 4 h postmating) and SP (after 4 h) up-regulated the expression of Clk, and because SP influences behaviors that are under circadian control ( 16 , 17 ), we investigated whether additional features with circadian rhythms were differentially expressed after mating. We found that of the 1,305 differentially expressed features from the network analysis, 18% (232 features) follow a circadian rhythm in V females ( q-value <0.3, Fig.…”

“…Since synaptic connections exist between pC1 neurons and clock neurons, there is a possibility for SP to directly modulate the female’s clock, thereby allowing SP to control many different postmating responses at once. Through ppk+ neurons that express SPR, SP alters neurotransmitter release from central clock ventral lateral (LNv) neurons, leading to loss of predawn elevated activity in mated females ( 17 ). LNv are called “morning neurons”, and LNd (for which we found a direct connection with pC1) are called “evening neurons” ( 106 ).…”

“…SP-mediated responses include increased egg laying and reduced receptivity to additional matings ( 5 , 6 ), and SP is needed to release sperm from storage organs ( 7 , 8 ). SP leads to an increase in juvenile hormone titers ( 9 , 10 ), immunity changes ( 11 , 12 ), alterations to the female’s metabolism, gut morphology and excretion ( 13 – 15 ), changes in activity levels ( 16 , 17 ), an increased appetite, with a preference for high-protein food ( 18 – 21 ), increased aggression ( 22 ), and an enhanced long-term memory ( 23 ). Many of these responses extend long-term due to SP’s ability to bind to stored sperm, followed by its gradual release via active proteolytic cleavage.…”