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Wigby, S.

Publications and source records attributed to Wigby, S..

11 recordsLinked to original sources

Sperm length ornamentation associates with survival and sterility after heatwaves among Drosophila species

Whether sexual selection facilitates or hinders adaptation to novel environments is a question of fundamental importance due to current rapid environmental change. Using phylogenetic comparative analysis in 42 Drosophila species, we found that sperm length - a sexually selected ornament - positively associates with the ability of males to survive high temperatures. However, the ability to remain fertile does not increase with sperm length to the same extent, meaning that longer sperm species experience a larger gap between temperatures that kill and temperatures that sterilize males. The findings are consistent with the idea that strong sexual selection on condition-dependent exaggerated traits may facilitate somatic resilience to environmental stressors, but that susceptibility to heat-induced infertility may be a cost of extreme sperm ornamentation. Overall, the data suggests multifaceted links between postcopulatory sexual selection and climate change.

evolutionary biology↗

Chilling out or heating up? Thermal plasticity of seminal fluid proteins in Drosophila melanogaster

Seminal fluid proteins (SFPs) play crucial roles in reproduction by shaping female post-mating physiology and behaviour, male sperm competition, and sexual conflict between the sexes. However, we mostly ignore how abiotic ecological factors regulate SFP expression and transfer. Here, we use quantitative proteomics in adult flies from a wild Drosophila melanogaster population to test how exposure to natural temperature variation (20{degrees}C, 24{degrees}C and 28{degrees}C) across two-time scales (48h and 13d), and under either no or high sperm competition risk, interact to shape SFP production and transfer. We show that both production and transfer of SFPs was reduced after long-term (13d) exposure to low (20{degrees}C) and high (28{degrees}C) temperatures, including in key proteins (sex peptide and ovulin networks) mediating female post-copulatory responses, sperm competition and sexual conflict. Our results show that natural temperature fluctuations can have a strong effect on SFP production and transfer, and thus on post-copulatory sexual selection dynamics.

evolutionary biology↗

The developmental environment mediates adult seminal proteome allocation in male Drosophila melanogaster

Early life conditions can have long-lasting fitness effects on organisms. In insects, crowding during larval stages impose a significant constraint on adult phenotypes due to increased intraspecific competition for resources, which can modulate males success in pre- and post-mating competition in adulthood. Evidence for larval crowding effects on male seminal fluid allocation exists but is limited to a small subset of well-known seminal fluid proteins (Sfps), and often overlooks the interactions between male and female phenotypes. We currently lack a comprehensive understanding of how male and female larval crowding interact to affect production, composition, and transfer of the wider seminal proteome. Here, we manipulated Drosophila melanogaster larval crowding (low versus high) of males and females to generate individuals with large and small body size, respectively. We mated individuals in a fully factorial design, and measured the abundance, composition, and transfer of Sfps. Large males produced Sfps in significantly higher abundances, yet this difference was marginal and not detected when Sfps were analysed individually. Conversely, small males transferred greater quantities of much of their seminal proteome to females than did large males. When analysing proteins individually, 10 Sfps were transferred in significantly higher abundances by small males than large males. Our results suggest that small males invest more on each mating opportunity, potentially as a response of overall fewer mating opportunities due to their reduced size, or due to the larval cues of high population density. This work provides an insight into early life effects on ejaculate allocation in D. melanogaster and sheds light on the physiological and behavioural responses to developmental conditions in insects.

evolutionary biology↗

Experimental evolution under varying sex ratio and nutrient availability modulates male mating success in Drosophila melanogaster

Biased population sex ratios can alter optimal male mating strategies, and allocation to reproductive traits depends on nutrient availability. However, there is little information on how nutrition interacts with sex ratio to influence the evolution of pre-copulatory and post-copulatory traits separately. To address this omission, here we test how male mating success and reproductive investment evolve under varying sex ratios and adult diet in Drosophila melanogaster using an experimental evolution approach. We found that sex ratio and nutrient availability interacted to determine male pre-copulatory performance. Males from female-biased populations were slow to mate when they evolved on a protein-restricted diet. On the other hand, we found direct and non-interacting effects of sex ratio and nutrient availability on post-copulatory success, without interactions between them. Males that evolved on a protein-restricted diet were poor at suppressing female remating. Males that evolved under equal sex ratios fathered more offspring and were better at supressing female remating, relative to males from male-biased or female-biased populations. These results support the idea that sex ratios and nutrition interact to determine the evolution of pre-copulatory mating traits, but independently influence the evolution of post-copulatory traits.

evolutionary biology↗

Influences of male age, mating history and starvation on female post mating aggression and feeding in Drosophila

O_LIMating changes female behaviour and physiology across a wide range of taxa, with important effects for male and female fitness. These changes are often induced by components of the male ejaculate, such as sperm and seminal fluid proteins. C_LIO_LIHowever, males can vary significantly in their ejaculates, due to factors such as age, mating history, or nutritional status. This male variation may therefore lead to variation in the strength of responses males can stimulate in females, with alterations in fitness outcomes for both sexes. C_LIO_LIUsing the fruit fly, Drosophila melanogaster, we tested whether three aspects of male condition shape an important, but understudied, post-mating response - increased female-female aggression. C_LIO_LIWe found that females mated to old males fought less than females mated to young males. This effect was exacerbated in mates of old, sexually active males, but there was no effect of male starvation status on mating-induced female aggression. There was also a significant effect of age and mating history on female post-mating feeding duration. C_LIO_LIOur results add to a growing body of literature that variation in male condition can shape sexual selection through post-mating responses in females, including female-female interactions. Studying such variation may therefore be useful for understanding how the condition of sex affects the behaviour of the other. C_LI

animal behavior and cognition↗

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 behaviour. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterised 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 post-mating responses including ovulation, elevated feeding and reduced receptivity to remating, primarily signalling 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 assembly factor for microcarriers and is also required for the female disassembly process to occur normally. Males expressing non-functional SP mutant proteins that affect SPs 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 defects in ejaculate function. Our data therefore reveal a novel role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species, which lack the signalling functions seen in D. melanogaster. Significance StatementSeminal fluid plays a critical role in reprogramming female physiology and behaviour to promote male reproductive success. We show in the fruit fly that specific seminal proteins, including the archetypal female-reprogramming molecule Sex Peptide, are stored in male seminal secretions in association with large neutral lipid-containing microcarriers, which rapidly disperse in females. Related structures are also observed in other Sex Peptide-expressing Drosophila species. Males lacking Sex Peptide have structurally defective microcarriers, leading to abnormal cargo loading and transfer to females. Our data reveal that this key signalling molecule in Drosophila seminal fluid is also a microcarrier assembly factor that controls transfer of other seminal factors, and that this may be a more evolutionarily ancient role of this protein.

cell biology↗

Temporal and genetic variation in female aggression after mating

Aggression between individuals of the same sex is almost ubiquitous across the animal kingdom. Winners of intrasexual contests often garner considerable fitness benefits, through greater access to mates, food, or social dominance. In females, aggression is often tightly linked to reproduction, with females displaying increases in aggressive behavior when mated, gestating or lactating, or when protecting dependent offspring. In the fruit fly, Drosophila melanogaster, females spend twice as long fighting over food after mating as when they are virgins. However, it is unknown when this increase in aggression begins or whether it is consistent across genotypes. Here we show that aggression in females increases between 2 to 4 hours after mating and remains elevated for at least a week after a single mating. In addition, this increase in aggression 24 hours after mating is consistent across three diverse genotypes, suggesting this may be a universal response to mating in the species. We also report here the first use of automated tracking and classification software to study female aggression in Drosophila and assess its accuracy for this behavior. Dissecting the genetic diversity and temporal patterns of female aggression assists us in better understanding its generality and adaptive function, and will facilitate the identification of its underlying mechanisms.

animal behavior and cognition↗

Structural variation in Drosophila melanogaster spermathecal ducts and its association with sperm competition dynamics

The ability of female insects to retain and use sperm for days, months, or even years after mating requires specialised storage organs in the reproductive tract. In most orders these organs include a pair of sclerotised capsules known as spermathecae. Here, we report that some Drosophila melanogaster females exhibit previously uncharacterised structures within the distal portion of the muscular duct that links a spermatheca to the uterus. We find that these spermathecal duct presences (SDPs) may form in either or both ducts and can extend from the duct into the sperm-storing capsule itself. We further find that the incidence of SDPs varies significantly between genotypes, but does not change significantly with the age or mating status of females, the latter indicating that SDPs are not composed of or stimulated by sperm or male seminal proteins. We show that SDPs affect neither the number of first male sperm held in a spermatheca nor the number of offspring produced after a single mating. However, we find evidence that SDPs are associated with a lack of second male sperm in the spermathecae after females remate. This raises the possibility that SDPs provide a mechanism for variation in sperm competition outcome among females.

evolutionary biology↗

BMP-signalling inhibition in Drosophila secondary cells remodels the seminal proteome, and self and rival ejaculate functions

Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of [~]1000 fertility-enhancing main cells and [~]40, more functionally cryptic, secondary cells. Inhibition of BMP-signalling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female post-mating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary cell secretions might therefore make a highly specific contribution to the seminal proteome and ejaculate function; alternatively, they might regulate more global - but hitherto-undiscovered - SFP functions and proteome composition. Here, we present data that supports the latter model. We show that in addition to previously reported phenotypes, secondary cell-specific BMP-signalling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a novel constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal a mix of specific and widespread changes to the seminal proteome that surprisingly encompass alterations to main cell-derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell-types suggesting that modification to the cellular make-up of seminal fluid-producing tissues is an important factor in ejaculate evolution.

evolutionary biology↗

An exposition of ejaculate senescence and its inhibition in Drosophila

Declining ejaculate performance with male age is taxonomically widespread and has broad ramifications for fertility and fitness. However, we have a poor understanding of age-related changes to specific ejaculate components, how they cause reduced performance, and whether the decline is ameliorable. Here, we show that, in Drosophila, sperm production chronologically declines with age, invariant to mating activity, while repeated mating causes infertility via reduced sperm stores and viability. However, changes to sperm do not fully explain ejaculate deterioration: impacts on seminal fluid contribute to aspects of reduced ejaculate performance, associated with shifts in proteome abundance and quality. We show that ablation of insulin-like peptide-producing cells in males ameliorates aspects of ejaculate performance loss, suggesting that anti-ageing interventions can be coopted to benefit male reproductive health.\n\nOne Sentence SummaryEjaculate performance declines with male age via mating-dependent sperm and seminal protein deterioration, but it can be ameliorated.

evolutionary biology↗

Quantitative proteomics identification of seminal fluid proteins in male Drosophila melanogaster

Seminal fluid contains some of the fastest evolving proteins currently known. These seminal fluid proteins (Sfps) play crucial roles in reproduction, such as supporting sperm function, and - particularly in insects - modifying female physiology and behaviour. Identification of Sfps in small animals is challenging, and often relies on samples taken from the female reproductive tract after mating. A key pitfall of this method is that it might miss Sfps that are of low abundance due to dilution in the female-derived sample or rapid processing in females. Here we present a new and complimentary method, which provides added sensitivity to Sfp identification. We applied label-free quantitative proteomics to Drosophila melanogaster male reproductive tissue - where Sfps are unprocessed, and highly abundant - and quantified Sfps before and immediately after mating, to infer those transferred during copulation. We also analysed female reproductive tracts immediately before and after copulation to confirm the presence and abundance of known and candidate Sfps, where possible. Results were cross-referenced with transcriptomic and sequence databases to improve confidence in Sfp detection. Our data was consistent with 124 previously reported Sfps. We found 8 high-confidence novel candidate Sfps, which were both depleted in mated versus unmated males and identified within the reproductive tract of mated but not virgin females. We also identified 31 more candidates that are likely Sfps based on their abundance, known expression and predicted characteristics, and revealed that four proteins previously identified as Sfps are at best minor contributors to the ejaculate. The estimated copy numbers for our candidate Sfps were lower than for previously identified Sfps, supporting the idea that our technique provides a deeper analysis of the Sfp proteome than previous studies. Our results demonstrate a novel, high-sensitivity approach to the analysis of seminal fluid proteomes, whose application will further our understanding of reproductive biology.

genomics↗