Sex Peptide Receptor Research Articles

The Origin and Evolution of Sex Peptide and Sex Peptide Receptor Interactions.

Post-mating responses play a vital role in successful reproduction across diverse species. In fruit flies, sex peptide binds to the sex peptide receptor, triggering a series of post-mating responses. However, the origin of sex peptide receptor predates the emergence of sex peptide. The evolutionary origins of the interactions between sex peptide and sex peptide receptor and the mechanisms by which they interact remain enigmatic. In this study, we used ancestral sequence reconstruction, AlphaFold2 predictions, and molecular dynamics simulations to study sex peptide-sex peptide receptor interactions and their origination. Using AlphaFold2 and long-time molecular dynamics simulations, we predicted the structure and dynamics of sex peptide-sex peptide receptor interactions. We show that sex peptide potentially binds to the ancestral states of Diptera sex peptide receptor. Notably, we found that only a few amino acid changes in sex peptide receptor are sufficient for the formation of sex peptide-sex peptide receptor interactions. Ancestral sequence reconstruction and molecular dynamics simulations further reveal that sex peptide receptor interacts with sex peptide through residues that are mostly involved in the interaction interface of an ancestral ligand, myoinhibitory peptides. We propose a potential mechanism whereby sex peptide-sex peptide receptor interactions arise from the preexisting myoinhibitory peptides-sex peptide receptor interface as well as early chance events both inside and outside the preexisting interface that created novel sex peptide-specific sex peptide-sex peptide receptor interactions. Our findings provide new insights into the origin and evolution of sex peptide-sex peptide receptor interactions and their relationship with myoinhibitory peptides-sex peptide receptor interactions.

Decoupled evolution of the Sex Peptide gene family and Sex Peptide Receptor in Drosophilidae

Across internally fertilising species, males transfer ejaculate proteins that trigger wide-ranging changes in female behaviour and physiology. Much theory has been developed to explore the drivers of ejaculate protein evolution. The accelerating availability of high-quality genomes now allows us to test how these proteins are evolving at fine taxonomic scales. Here, we use genomes from 264 species to chart the evolutionary history of Sex Peptide (SP), a potent regulator of female post-mating responses in Drosophila melanogaster. We infer that SP first evolved in the Drosophilinae subfamily and has since followed markedly different evolutionary trajectories in different lineages. Outside of the Sophophora-Lordiphosa, SP exists largely as a single-copy gene with independent losses in several lineages. Within the Sophophora-Lordiphosa, the SP gene family has repeatedly and independently expanded. Up to seven copies, collectively displaying extensive sequence variation, are present in some species. Despite these changes, SP expression remains restricted to the male reproductive tract. Alongside, we document considerable interspecific variation in the presence and morphology of seminal microcarriers that, despite the critical role SP plays in microcarrier assembly in D. melanogaster, appears to be independent of changes in the presence/absence or sequence of SP. We end by providing evidence that SP's evolution is decoupled from that of its receptor, Sex Peptide Receptor, in which we detect no evidence of correlated diversifying selection. Collectively, our work describes the divergent evolutionary trajectories that a novel gene has taken following its origin and finds a surprisingly weak coevolutionary signal between a supposedly sexually antagonistic protein and its receptor.

Receptivity and Remating Propensity in Female Spodoptera litura (Fabricius) after Mating with an Irradiated Male or Its F1 Male Progeny.

The 'Inherited or F1 sterility technique' (IS), using sub-sterilized male moths, is a widely proposed pest management tool for Lepidoptera pests in general, and the tobacco cutworm Spodoptera litura (Fabr.) in particular. However, the multiple mating tendency of female moths and the ejaculate quality of male moths might influence the efficiency of this technique. Reduced ejaculate quality was observed in irradiated males, as evidenced by radiation's impact on certain bio-parameters, such as the weight of the spermatophores and their protein content, sperm count, the molecular expression of the sex peptide receptor (SPR) and egg fertility, with a greater impact in F1 male progeny. During the remating of females with untreated males, irrespective of the irradiation status of the first male, there was an increase in calling behavior, remating propensity and fertility in females, with a larger time gap between consecutive matings. The ability of F1 male progeny to check remating propensity in females 24 h after the initial mating was lower than that of unirradiated males. Partially sterile (130 Gy) males were as successful as unirradiated males in inducing the level of mating refractoriness in females. Decreased ejaculate quality in F1 male progeny could be associated with increased female receptivity during remating. Understanding the influence of male moth irradiation, insemination quality and post (initial)-mating intervals on the remating behavior of normal female moths and induced sterility might help in simulation modeling and optimizing IS insect programs.

CRISPR/Cas9-induced Mutation of Sex Peptide Receptor Gene Bdspr Affects Ovary, Egg Laying, and Female Fecundity in Bactrocera dorsalis (Hendel) (Diptera: Tephritidae).

The oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), is an invasive and polyphagous pest of horticultural crops, and it can cause huge economic losses in agricultural production. The rapid development of CRISPR/Cas9 gene editing technology has provided new opportunities for the scientific control of agricultural pests. Here, we explore the applicability of the B. dorsalis sex peptide receptor (Bdspr) as a target gene for the CRISPR/Cas9-based sterile insect technique (SIT) in B. dorsalis. We screened two high-efficient single guide RNAs (sgRNAs) for gene editing. The results showed that both mutation efficiency and germline transmission rate were 100% in the surviving G0 females (8/8) from injected embryos, and that 75% of mosaically mutated G0 females (6/8) were sterile. The 50% of heterozygous G1 females (4/8) could not lay eggs; 100% of eggs laid by them could not survive; and 62.5% of individual females (5/8) had abnormal ovaries. These results indicate that Bdspr plays an important role in regulating fertility, egg viability, and ovary development in female B. dorsalis, suggesting that the spr gene can be used for CRISPR/Cas9-based SIT in B. dorsalis.

Mating disrupts morning anticipation in Drosophila melanogaster females.

After mating, the physiology of Drosophila females undergo 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 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 activation of the sex peptide receptor (SPR) mainly on pickpocket (ppk) expressing neurons, since reducing expression of this receptor in these neurons restores the ability to anticipate the LD transition in mated females. Furthermore, we 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, we confirm that 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 reach clock neurons in the fly central nervous system to modulate the temporal organization of circadian behavior according to the needs of the new status.

Response of optic gland pathways to thermal stress in the reproductive phase of female Octopus maya

ABSTRACT The octopus optic glands are the source of multiple signalling molecules that control the transitions through different physiological stages, such as maturation, ageing and death. This study focused on the role of the optic glands during the reproductive phase of Octopus maya, investigating the molecular mechanisms that prevent reproduction at elevated temperatures. RNA sequencing was used to analyse and compare optic gland transcriptomic profiles of female O. maya before, during and after egg-laying under optimal and thermal stress (elevated temperature) conditions. Each stage showed well-defined transcriptomic patterns, and all were strongly affected by thermal stress. At optimal temperature, the optic glands contribute importantly to regulating the energetic balance, as suggested by the expression of genes that modulate the metabolic rate, arterial blood pressure and the management of ATP sources in response to food deprivation. At elevated temperatures, the optic glands of mated females (before egg-laying) showed upregulation of genes encoding neuropeptides (FMRF-amide, APGW-amide, PRQFV-amide, FCAP, buccalin and myomodulin) and the dopamine beta-hydroxylase gene. During egg-laying at elevated temperatures, the neuropeptide receptor capaR and the sex peptide receptor were upregulated whereas homologs of fetuin-B and oviduct-specific glycoprotein genes, crucial for fertilization, were downregulated. These changes in optic gland gene expression in O. maya may be the basis for the high-temperature inhibition of egg-laying, previously observed from this octopus species. Furthermore, after egg-laying, during egg incubation thermal stress affected the expression of genes involved in steroid and thyroid hormone biosynthesis and in inflammatory and apoptotic pathways.

Identification of neuropeptide receptors from the brain of the bean pod borer, Maruca vitrata

• The brain transcriptomes of Maruca vitrata were analyzed. • Twenty neuropeptide receptors exhibited significant expression level in the brain. • The brain expressed various neuropeptide receptors belonging to GPCR family. • Neuropeptide receptors in the brain can be putative control targets. Neuropeptides in the insect brain have been involved in various physiological activities such as circadian rhythm, learning and memory, olfactory processing, feeding behavior, etc. Neuropeptides bind to their receptors which transduce their signals, resulting in behavioral and physiological changes. To identify neuropeptides and examine their diurnal expression from the brain of Maruca vitrata , the brain transcriptomes collected from total RNAs with 4 h interval were analyzed. Total trimmed reads from six brain transcriptomes were 0.69 billion and 40,487 contigs exhibiting significant FPKM value were identified. Twenty contigs showing significant expression level were identified as neuropeptide receptors including tachykinin-like peptide receptor, diuretic hormone receptor, SIFamide receptor, sex peptide receptor, somatostatin receptor, RYamide receptor, etc. These receptors mainly belonged to G protein-coupled receptor family. Relative expressions of neuropeptide receptors were evaluated based on FPKM values. Expressions of various neuropeptide receptors in the brain can provide information on putative control targets for insect pests.

Regulation of Mating-Induced Increase in Female Germline Stem Cells in the Fruit Fly Drosophila melanogaster

In many insect species, mating stimuli can lead to changes in various behavioral and physiological responses, including feeding, mating refusal, egg-laying behavior, energy demand, and organ remodeling, which are collectively known as the post-mating response. Recently, an increase in germline stem cells (GSCs) has been identified as a new post-mating response in both males and females of the fruit fly, Drosophila melanogaster. We have extensively studied mating-induced increase in female GSCs of D. melanogaster at the molecular, cellular, and systemic levels. After mating, the male seminal fluid peptide [e.g. sex peptide (SP)] is transferred to the female uterus. This is followed by binding to the sex peptide receptor (SPR), which evokes post-mating responses, including increase in number of female GSCs. Downstream of SP-SPR signaling, the following three hormones and neurotransmitters have been found to act on female GSC niche cells to regulate mating-induced increase in female GSCs: (1) neuropeptide F, a peptide hormone produced in enteroendocrine cells; (2) octopamine, a monoaminergic neurotransmitter synthesized in ovary-projecting neurons; and (3) ecdysone, a steroid hormone produced in ovarian follicular cells. These humoral factors are secreted from each organ and are received by ovarian somatic cells and regulate the strength of niche signaling in female GSCs. This review provides an overview of the latest findings on the inter-organ relationship to regulate mating-induced female GSC increase in D. melanogaster as a model. We also discuss the remaining issues that should be addressed in the future.

The sex peptide receptor in the Asian gypsy moth, Lymantria dispar, is involved in development and stress resistance

The G protein-coupled receptor (GPCR) regulates downstream genes by binding to a heterotrimeric G protein. However, the function of sex peptide receptor (SPR) in lepidopteran species is mostly unknown. Understanding the physiological functions of SPR in insects is essential for exploring new insecticidal targets. In the present study, the functions of an SPR in Lymantria dispar (Asian gypsy moth; LdSPR) were investigated. The expression of LdSPR was the highest in the 6th instar larval stage, and there was a large difference in expression between male and female adults. After LdSPR gene silencing, L. dispar larvae showed increased sensitivity to high temperature, starvation, and oxidative stress, indicating that LdSPR enhances stress resistance. These results enrich our knowledge of the function of the insect SPRs, which will lead to a better understanding of other insect GPCR family members and the identification of new targets for the development of environmentally friendly pesticides.

Sex peptide receptor mediates the post‐mating switch in Helicoverpa armigera (Lepidoptera: Noctuidae) female reproductive behavior

In Drosophila, the sex peptide receptor (SPR) in females to detect male sex peptide (SP) and trigger changes in female behavior including mating rejection and oviposition. In moths, the SPR had been identified and investigated the limited function by using RNA interference (RNAi). However, the detailed function of SPR after a normal mating in moths, especially the role in female sexual receptivity, remains to be elucidated. In this study, we use Helicoverpa armigera, an economically important pest worldwide, as a case study to verify the function of SPR in vivo by CRISPR/Cas9 gene editing system. Analyzing the post-mating behaviors in mutant females, we investigated that HarmSPR could mediate the long-term sexual receptivity (remating, sex pheromone production and calling behavior) switch in female, but not affect the short-term sexual receptivity and the duration time of remating. The oviposition of mated HarmSPR-/- females was significantly decreased by ~70% comparing to wild-type (WT) mated females and there were more eggs staying in the ovary of mutant females. SPR also showed effect on female longevity, which is that the mated HarmSPR-/- females showed longer longevity than mated WT females. The results detailedly demonstrated the functional role of SPR in female post-mating behaviors and we could propose a pest control strategy in which developing an antagonist of SPR to reduce the oviposition of female. © 2021 Society of Chemical Industry.

Drosophila Sex Peptide controls the assembly of lipid microcarriers in seminal fluid

Seminal fluid plays an essential role in promoting male reproductive success and modulating female physiology and behavior. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterized protein mediator of these effects. It is secreted from the paired male accessory glands (AGs), which, like the mammalian prostate and seminal vesicles, generate most of the seminal fluid contents. After mating, SP binds to spermatozoa and is retained in the female sperm storage organs. It is gradually released by proteolytic cleavage and induces several long-term postmating responses, including increased ovulation, elevated feeding, and reduced receptivity to remating, primarily signaling through the SP receptor (SPR). Here, we demonstrate a previously unsuspected SPR-independent function for SP. We show that, in the AG lumen, SP and secreted proteins with membrane-binding anchors are carried on abundant, large neutral lipid-containing microcarriers, also found in other SP-expressing Drosophila species. These microcarriers are transferred to females during mating where they rapidly disassemble. Remarkably, SP is a key microcarrier assembly and disassembly factor. Its absence leads to major changes in the seminal proteome transferred to females upon mating. Males expressing nonfunctional SP mutant proteins that affect SP's binding to and release from sperm in females also do not produce normal microcarriers, suggesting that this male-specific defect contributes to the resulting widespread abnormalities in ejaculate function. Our data therefore reveal a role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species that lack the signaling functions seen in Dmelanogaster.

Drosophila melanogaster sex peptide regulates mated female midgut morphology and physiology

Drosophila melanogaster females experience a large shift in energy homeostasis after mating to compensate for nutrient investment in egg production. To cope with this change in metabolism, mated females undergo widespread physiological and behavioral changes, including increased food intake and altered digestive processes. The mechanisms by which the female digestive system responds to mating remain poorly characterized. Here, we demonstrate that the seminal fluid protein Sex Peptide (SP) is a key modulator of female post-mating midgut growth and gene expression. SP is both necessary and sufficient to trigger post-mating midgut growth in females under normal nutrient conditions, and likely acting via its receptor, Sex Peptide Receptor (SPR). Moreover, SP is responsible for almost the totality of midgut transcriptomic changes following mating, including up-regulation of protein and lipid metabolism genes and down-regulation of carbohydrate metabolism genes. These changes in metabolism may help supply the female with the nutrients required to sustain egg production. Thus, we report a role for SP in altering female physiology to enhance reproductive output: Namely, SP triggers the switch from virgin to mated midgut state.

Molecular characterization of ligand selectivity of the sex peptide receptors of Drosophila melanogaster and Aedes aegypti

Drosophila melanogaster sex peptide receptor (DrmSPR) is a G protein-coupled receptor (GPCR) with ‘dual ligand selectivity’ towards sex peptide (SP) and myoinhibitory peptides (MIPs), which are only remotely related to one another. SPR is conserved in almost all the sequenced lophotrochozoan and ecdysozoan genomes. SPRs from non-drosophilid taxa, such as those from the mosquitoes Aedes aegypti (AeaSPR), Anopheles gambiae (AngSPR), and the sea slug Aplysia californica (ApcSPR), are highly sensitive to MIP, but not to SP. To understand how Drosophila SPRs evolved their SP sensitivity while maintaining MIP sensitivity, we examined ligand selectivity in a series of chimeric GPCRs that combine domains from the SP-sensitive DrmSPR and the SP-insensitive AeaSPR. We found replacement of Pro 238 (P238) in DrmSPR with the corresponding residue from AeaSPR (L310) reduced its SP sensitivity 2.7 fold without altering its MIP sensitivity. The P238 residue located in the third extracellular loop (ECL3) is conserved in Drosophila SPRs and in SPR from the moth Bombyx mori (BomSPR), which is considerably more sensitive to SP than AeaSPR, AngSPR, or ApcSPR. We found, however, that rather than improving AeaSPR's sensitivity to SP, replacement of L310 in AeaSPR with Pro significantly reduces its MIP sensitivity. Thus, our identification of a single amino acid residue critical for SP sensitivity, but not for MIP sensitivity is an important step in clarifying how DrmSPR evolved the ability to detect SP.

Anxiety-like behaviour is regulated independently from sex, mating status and the sex peptide receptor in Drosophila melanogaster

Sex differences in anxiety-related behaviours have been documented in many animals and are notable in human populations. A major goal in behaviour research is to understand why and how sex differences in cognitive-emotional states like anxiety arise and are regulated throughout life. Anxiety allows individuals to detect and respond to threats. Mating is a candidate regulator for anxiety because threats are likely to change, often in sex-specific ways, when individuals shift to a postmating reproductive state. However, we know little about how mating mediates anxiety-related behaviour in males and females, or about how males might influence female anxiety via seminal proteins transferred during mating. To address this gap, we examined anxiety-related behaviour in the fruit fly Drosophila melanogaster , an emerging model animal for anxiety, with respect to sex, mating and sex peptide, a seminal protein known to modulate a host of female postmating responses in fruit flies. We assayed anxiety-like behaviour using the open-field assay to assess individual avoidance of the interior of an arena (‘wall-following’ behaviour). We found sex differences in activity level, but no evidence for sex differences in wall-following behaviour. We found no effects of mating in either sex, or of the presence of the sex peptide receptor in females, on wall following. Our results suggest that anxiety is not one of the cognitive-emotional states regulated by mating and sex peptide in fruit flies, and that researchers need an alternative model for sex differences in anxiety. • Many animals display anxiety, but few studies have compared males and females. • In fruit flies, we found no sex differences in anxiety-like behaviour. • Mating could modulate anxiety, directly or via male ejaculate proteins. • We found that anxiety was independent from mating and the sex peptide protein. • Anxiety is not part of the postmating behavioural shift in fruit flies.

Knocking down the sex peptide receptor by dsRNA feeding results in reduced oviposition rate in olive fruit flies.

Insect pests can cause crop damage in yield or quality, resulting in profit losses for farmers. The primary approach to control them is still the use of chemical pesticides resulting in significant hazards to the environment and human health. Biological control and the sterile insect technique are alternative strategies to improve agriculture protection. However, both strategies have significant limitations. A newly introduced approach that could be both effective and species-specific is the RNA interference mechanism. One key point for the success of this strategy is the delivery method of double-strand RNA (dsRNA) to the insects. A method of dsRNA delivery to insects with potential use in the field is the oral delivery, feeding the insects engineered microorganisms that produce dsRNA. Here, we present the first protocol for dsRNA feeding using modified bacteria, in the olive fruit fly, the most important insect pest of cultivated olives. We chose to target the sex peptide receptor gene. The sex peptide receptor interacts with the sex peptide, a peptide that is responsible for the postmating behavior in the model organism, Drosophila melanogaster. Feeding the female olive fruit fly with bacteria that produced dsRNA for the sex peptide receptor gene resulted in the development of female insects with significantly lower oviposition rates. Administration of dsRNA producing bacteria in insect diet against target genes that lead to genetic sexing or female-specific lethality could be added in the armory of control methods.

A sperm peptide enhances long-term memory in female Drosophila.

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.

Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development

BackgroundThe black-lip rock oyster (Saccostrea echinata) has considerable potential for aquaculture throughout the tropics. Previous attempts to farm S. echinata failed due to an insufficient supply of wild spat; however, the prospect of hatchery-based aquaculture has stimulated renewed interest, and small-scale farming is underway across northern Australia and in New Caledonia. The absence of knowledge surrounding the population genetic structure of this species has raised concerns about the genetic impacts of this emerging aquaculture industry. This study is the first to examine population genetics of S. echinata and employs both mitochondrial cytochrome c oxidase subunit I gene (COI) and single nucleotide polymorphism (SNP) markers.ResultsThe mitochondrial COI data set included 273 sequences of 594 base pair length, which comprised 74 haplotypes. The SNP data set included 27,887 filtered SNPs for 272 oysters and of these 31 SNPs were identified as candidate adaptive loci. Data from the mitochondrial COI analyses, supports a broad tropical Indo-Pacific distribution of S. echinata, and showed high haplotype and nucleotide diversities (0.887–1.000 and 0.005–0.008, respectively). Mitochondrial COI analyses also revealed a ‘star-like’ haplotype network, and significant and negative neutrality tests (Tajima’s D = − 2.030, Fu’s Fs = − 25.638, P < 0.001) support a recent population expansion after a bottleneck. The SNP analyses showed significant levels of population subdivision and four genetic clusters were identified: (1) the Noumea (New Caledonia) sample location; (2) the Bowen (north Queensland, Australia) sample location, and remaining sample locations in the Northern Territory, Australia (n = 8) were differentiated into two genetic clusters. These occurred at either side of the Wessel Islands and were termed (3) ‘west’ and (4) ‘east’ clusters, and two migrant individuals were detected between them. The SNP data showed a significant positive correlation between genetic and geographic distance (Mantel test, P < 0.001, R2 = 0.798) and supported isolation by distance. Three candidate adaptive SNPs were identified as occurring within known genes and gene ontology was well described for the sex peptide receptor gene.ConclusionsData supports the existence of genetically distinct populations of S. echinata, suggesting that management of wild and farmed stocks should be based upon multiple management units. This research has made information on population genetic structure and connectivity available for a new aquaculture species.

Tango knock-ins visualize endogenous activity of G protein-coupled receptors in Drosophila

G protein-coupled receptors (GPCRs) represent a family of seven-pass transmembrane protein receptors whose ligands include neuropeptides and small-molecule neuromodulators such as dopamine and serotonin. These neurotransmitters act at long distances and are proposed to define the ground state of the nervous system. The Drosophila genome encodes approximately 50 neuropeptides and their functions in physiology and behavior are now under intensive studies. Key information currently lacking in the field is the spatiotemporal activation patterns of endogenous GPCRs. Here we report application of the Tango system, a reporter assay to detect GPCR activity, to endogenous GPCRs in the fly genome. We developed a method to integrate the sensor component of the Tango system to the C-terminus of endogenous genes by using genome editing techniques. We demonstrate that Tango sensors in the Sex-peptide receptor (SPR) locus allow sensitive detection of mating-dependent SPR activity in the female reproductive organ. The method is easily applicable to any GPCR and will provide a way to systematically characterize GPCRs in the fly brain.

Sex peptide receptor-regulated polyandry modulates the balance of pre- and post-copulatory sexual selection in Drosophila

Polyandry prolongs sexual selection on males by forcing ejaculates to compete for fertilisation. Recent theory predicts that increasing polyandry may weaken pre-copulatory sexual selection on males and increase the relative importance of post-copulatory sexual selection, but experimental tests of this prediction are lacking. Here, we manipulate the polyandry levels in groups of Drosophila melanogaster by deletion of the female sex peptide receptor. We show that groups in which the sex-peptide-receptor is absent in females (SPR-) have higher polyandry, and – as a result – weaker pre-copulatory sexual selection on male mating success, compared to controls. Post-copulatory selection on male paternity share is relatively more important in SPR- groups, where males gain additional paternity by mating repeatedly with the same females. These results provide experimental evidence that elevated polyandry weakens pre-copulatory sexual selection on males, shifts selection to post-copulatory events, and that the sex peptide pathway can play a key role in modulating this process in Drosophila.

Divergence in sex peptide-mediated female post-mating responses in Drosophila melanogaster.

Transfer and receipt of seminal fluid proteins crucially affect reproductive processes in animals. Evolution in these male ejaculatory proteins is explained with post-mating sexual selection, but we lack a good understanding of the evolution of female post-mating responses (PMRs) to these proteins. Some of these proteins are expected to mediate sexually antagonistic coevolution generating the expectation that females evolve resistance. One candidate in Drosophila melanogaster is the sex peptide (SP) which confers cost of mating in females. In this paper, we compared female SP-induced PMRs across three D. melanogaster wild-type populations after mating with SP-lacking versus control males including fitness measures. Surprisingly, we did not find any evidence for SP-mediated fitness costs in any of the populations. However, female lifetime reproductive success and lifespan were differently affected by SP receipt indicating that female PMRs diverged among populations. Injection of synthetic SP into virgin females further supported these findings and suggests that females from different populations require different amounts of SP to effectively initiate PMRs. Molecular analyses of the SP receptor suggest that genetic differences might explain the observed phenotypical divergence. We discuss the evolutionary processes that might have caused this divergence in female PMRs.