A sperm peptide enhances long-term memory in female Drosophila

Abstract

Can mating influence cognitive functions such as learning and memory in a permanent way? We have addressed this question using a combined behavioral and in vivo imaging approach, finding that aversive long-term memory performance strongly increases in Drosophila females in response to sperm transfer following mating. A peptide in the male sperm, the sex peptide, is known to cause marked changes in female reproductive behavior, as well as other behaviors such as dietary preference. Here, we demonstrate that this sex peptide enhances memory by acting on a single pair of serotonergic brain neurons, in which activation of the sex peptide receptor stimulates the cyclic adenosine monophosphate/protein kinase A pathway. We thus reveal a strong effect of mating on memory via the neuromodulatory action of a sperm peptide on the female brain.

Drosophila seminal sex peptide associates with rival as well as own sperm, providing SP function in polyandrous females

“…SFPs are produced within glandular tissues in the male reproductive tract and are transferred to females along with sperm during mating ( Avila et al, 2010 ; Poiani, 2006 ; Ravi Ram and Wolfner, 2007b ; Ravi Ram et al, 2005 ; Ravi Ram and Wolfner, 2009 ; Wigby et al, 2009 ). Within a mated female, SFPs mediate an array of post-mating responses such as, in insects, changes in egg production, elevated feeding rates, higher activity or reduced sleep levels, long-term memory, activation of the immune system and reduced sexual receptivity ( Avila et al, 2011 ; Bath et al, 2017 ; Scheunemann et al, 2019 ; Isaac et al, 2010 ; Domanitskaya et al, 2007 ; Chapman et al, 2003 ; Schwenke et al, 2016 ).…”

DrosophilaSex Peptide Controls the Assembly of Lipid Microcarriers in Seminal Fluid

“…To assess whether SP is involved in microcarrier assembly, we analysed AGs of males carrying the previously generated SP 0 null allele (12), either as a homozygote or in transheterozygous combination with a small SP deficiency, Df(3L)Δ130 (35, 12). These transheterozygous SP null males have been used to characterise the full range of SP mutant PMR phenotypes (12–21). Unexpectedly, these mutant animals displayed dramatic defects in microcarrier morphology (Fig.…”

“…On transfer to females following mating, SP effects a comprehensive reprogramming of female physiology and behaviour. It promotes long-term increases in egg-laying, reduces female receptivity to remating (11, 12) and affects sperm release (13), diet (14), feeding behaviour (15), water balance (16), defaecation (17), sleep (18), immunity (19), aggression (20) and memory (21).…”

“…In females, the SP receptor (SPR) is required to mediate most of these effects (25). SPR is expressed in specific neurons of the female reproductive tract that have a key role in the SP-dependent PMR (26, 27), and in other neurons in the CNS that are also able to respond to circulating SP (28, 21). In addition, SP appears to produce some SPR-independent post-mating responses in females (29, 20).…”

TheDrosophilaseminal Sex Peptide can associate with rival as well as own sperm and provide function for SP in polyandrous females

“…Ejaculate molecules, particularly the seminal fluid proteins (SFPs) that are received by females during mating, play crucial roles in successful fertilization. In Drosophila they induce striking changes in the physiology and behavior of females, instigating a wide array of post mating responses [6,14,28,29,39–41]. Some of these responses persist long-term, due to binding of a male’s SP to his sperm and gradual release of the SP’s active C-terminal region [19].…”