The control of sexual receptivity in female Drosophila

144

During mating, male Drosophila melanogaster transfer to the female's cuticle a compound (7-tricosene) that is almost absent from virgin females but is the major hydrocarbon component of the male's cuticle. During the first 3 hr after mating, the amount of7-tricosene on a female decreases sharply but remains significantly above virgin levels. By 6 hr after mating, female synthesis of 7-tricosene has increased, and females release it when they are exposed to courting males. Transfer of 7-tricosene to immature virgin females by courting males significantly decreases their attractiveness, so 7-tricosene has demonstrable antiaphrodisiac properties. Thus, mated D. melanogaster females appear to mimic males by releasing during courtship, an antiasphrodisiac pheromone that is almost absent from virgin females but is the most prominent hydrocarbon of the male cuticle.Mature virgin Drosophila melanogaster females are highly attractive (elicit high levels ofcourtship from males), but after mating, female attractiveness quickly decreases by half or more (1, 2). A complete mating, which normally lasts about 20 min, is not necessary for this initial decrease. Copulations interrupted after 3 min effect nearly the entire reduction in female attractiveness, and some reduction occurs after copulations lasting only 1 min (2). Production of female-specific courtship-stimulating compounds remains near virgin levels for about the first 3 days after mating (3), so loss of sex stimulants does not contribute to the initial decrease in female attractiveness. By 24 hr after a complete mating, females release an aversive chemical cue when they are courted (4-7). This cue probably helps maintain lower female attractiveness after the initial decrease (see ref. 8).During mating, the male-specific lipid cis-vaccenyl acetate (cVAc: cis-11-octadecen-1-yl acetate) is transferred to females (3, 9-12). Topical application ofcVAc to virgin females inhibits male courtship and mating (1,13), which suggests that cVAc could be involved in the regulation of matedfemale attractiveness (1,8,13,14). However, most of the cVAc in mated females is lost during the first 4-6 hr after mating (12,13,15). Further, the primary antiaphrodisiac of mated females is probably not the male-derived cVAc but rather a compound produced by females themselves (14). Mane et al. (1) proposed that cVAc in mated females was hydrolyzed to cis-vaccenol (cVOH) by esterase 6, another component of the male ejaculate (16). Production of cVOH could then lead to a reduction in female attractiveness beyond that due to cVAc alone (1). This hypothesis accounted for both the rapid loss of cVAc from the female and the appearance of a female-produced antiaphrodisiac. However, subsequent experiments showed that the loss of cVAc from mated females is independent of Esterase 6 transfer and that hydrolysis of cVAc to cVOH does not occur in vivo (12).Instead, cVAc lost from mated females' reproductive tracts is deposited onto the substrate, where it interacts with food odors as an aggregati...

Section: Discussionmentioning

confidence: 99%

Sexual mimicry regulates the attractiveness of mated Drosophila melanogaster females.

Scott¹

1986

144

“…Based on these results, it has been proposed that both responses are composed of two phases: a short-term phase lasting for 1 day and a long-term phase persisting for an additional 8-10 days (20). The short-term phase is thought to be activated only by seminal fluid (''seminal effect'') (14,(16)(17)(18)(19) and the long-term phase, only by sperm (''sperm effect'') (13). According to this model, when males producing sperm, but no accessory gland secretions, are mated, the recipient females are expected to display both responses only with a long-term phase.…”

mentioning

confidence: 99%

“…However, earlier matings counteract this effect in females by drastically enhancing egg laying (oviposition) and repressing sexual receptivity, i.e., the acceptance of males for remating, and thus maximize the number of eggs fertilized by sperm before the next mating (9)(10)(11). Both behavioral responses can persist for 9-11 days after a single mating event (12,13) and require, in addition to sperm, the transfer during copulation of components secreted by the male accessory glands (9-11, 14, 15). XO males, which produce accessory gland secretions (seminal fluid) but no sperm, induce in their mates a transient increase in oviposition and a decrease in receptivity for only 1 day (14).…”

mentioning

confidence: 99%

Drosophila female sexual behavior induced by sterile males showing copulation complementation

Xue

Noll

2000

122

Females of most animal species are usually inseminated by more than one male, which allows sperm from different males to compete for fertilization. To prevent invasion of sperm from other males, Drosophila males elicit a rejection behavior in their mates after copulation. Using paired mutant males that, for the lack of accessory glands, are sterile, we show that this rejection behavior is induced exclusively by the secreted accessory gland products transferred to the female during copulation. Moreover, the activities of sperm and accessory gland products are complementary and interdependent: both sperm fertility and rejection behavior depend on accessory gland products whose prolonged activities, in turn, require the presence of sperm. Fertility of sperm from paired males can be restored by accessory gland products of spermless males in ''copulation complementation'' experiments. Our observations may have important implications for the role of sexual behavior in evolution and for the treatment of male sexual dysfunction in humans.

“…Manning (19,20) has shown that sperm is required for the persistence of both responses (sperm effect). Lack of sperm transfer results in a short-term response of 1 day as also observed after injection of physiological amounts of SP or DUP99B (12, 13).…”

mentioning

confidence: 99%

Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster

Liu

Kubli

2003

482

535

Mating elicits two major changes in the reproductive behavior of many insect females. The egg-laying rate increases and the readiness to accept males (receptivity) is reduced. These postmating responses last Ϸ1 week in Drosophila melanogaster. Males that do not transfer sperm but transfer seminal fluid during mating induce a short-term response of 1 day. The long-term response of 1 week requires the presence of sperm (sperm effect). Hence, sperm is essential for the long-term persistence of the postmating responses. Three seminal fluid peptides elicit postmating responses: ovulin, sex-peptide (SP), and DUP99B. Using the technique of targeted mutagenesis by homologous recombination, we have produced males with mutant SP genes. Here, we report that males lacking functional SP elicit only a weak short-term response. However, these males do transfer sperm. Thus, (i) SP is the major agent eliciting the short-term and the long-term postmating responses and (ii) sperm is merely the carrier for SP. The second conclusion is supported by the finding that SP binds to sperm. The 36-aa-encoding SP gene is the first small Drosophila gene knocked out with the method of homologous recombination. I n many insect species, the reproductive behavior of females drastically changes after mating (1, 2). Egg laying is increased and receptivity is reduced. These female postmating responses are elicited by seminal fluid and sperm transferred during copulation. In most species, the virgin state is achieved again after some time (2). The egg-laying rate decreases to a virgin level and the female accepts courting males again. The coordination of egg production and egg laying with the presence of sperm in the female genital tract is largely in the interest of both sexes. However, it may be advantageous for a female to mate with more than one male to enhance the genetic diversity of her offspring. Female promiscuity can reduce the partner's fitness through sperm competition. As countermeasures, males have evolved mechanisms that reduce the females' tendency to remate (2-4). In some species, this may even lead to a reduced female lifespan (5). Experimental approaches have yielded insights into the nature of these sexual conflicts (6-11), but the molecular mechanisms involved remain largely unknown.In Drosophila melanogaster, two male peptides induce the postmating responses when injected into virgin females: sexpeptide (SP, ACP70A) and ductus ejaculatorius peptide 99B (DUP99B; 99B stands for the cytological localization of the gene at position 99B; refs. 12 and 13). They are synthesized in the accessory glands and the ductus ejaculatorius, respectively. Both are transferred into the female during mating (3, 13). After entering the female genital tract, the two peptides are believed to be transferred into the hemolymph where they reach their targets (3,(13)(14)(15). This view is supported by ectopic, constitutive expression of SP in the fat body of females, leading to a continuous induction of the postmating responses (16). Although both peptid...