Social and physical environment independently affect oviposition decisions in Drosophila.

In response to environmental stimuli, including variation in the presence of conspecifics, genotypes show highly plastic responses in behavioral and physiological traits influencing reproduction. Although extensively documented in males, such female responses are rather less studied. We expect females to be highly responsive to environmental variation and to differentially allocate resources to increase offspring fitness, given the major contribution of mothers to offspring number, size, and developmental conditions. Using Drosophila melanogaster, we (a) manipulate exposure to conspecific females, which mothers could use to anticipate the number of potential mates and larval density, and; (b) test how this interacts with the spatial distribution of potential oviposition sites, with females from higher densities expected to prefer clustered resources that can support a larger number of larvae. We found that high density females were slower to start copulating and reduced their copulation duration, the opposite effect to that observed in males. There was a parallel, perhaps related, effect on egg production: females previously housed in groups laid fewer eggs than those housed in solitude. Resource patchiness also influenced oviposition behavior: females preferred aggregated substrate, which attracted more females to lay eggs. However, we found no interaction between prior housing conditions and resource patchiness, indicating that females did not perceive the value of different resource distributions differently when exposed to environments that could signal expected levels of larval competition. We show that, although exposure to consexual competition changes copulatory behaviors of females, the distribution of oviposition resources has a greater effect on oviposition decisions.

Differing effects of age and starvation on reproductive performance in Drosophila melanogaster.

Successful reproduction requires the completion of many, often condition-dependent, stages, from mate searching and courtship through to sperm transfer, fertilisation and offspring production. Animals can plastically adjust their investment in each stage according to the physical and social environment, their own condition, their future reproductive potential, and the condition of their partner. Here we manipulate age and condition, through a nutritional challenge early or late in life, of both male and female Drosophila melanogaster and measure the effects on courtship, mating, and fitness when paired with a standardized (unmanipulated) partner. Older males were slower to start courting and mating, and courted at a slower rate, but males were indifferent to female age or condition despite older females laying and hatching fewer eggs. Female condition had a substantial effect on mating acceptance rate, which dropped dramatically after starvation, and particularly recent starvation experience. In contrast, male condition had little effect on any of the components of reproductive performance we measured. Intriguingly, we found no evidence for additive or multiplicative effects of ageing and starvation: the only significant interaction between these variables was on male latency to initiate courtship - older males were slower to start courting unless they had experienced starvation early in life. These results indicate that the immediate costs of mating differ between males and females, and that the sexes differ in their perception of the opportunity cost sustained by refusing a mating opportunity. Our results support the idea that ageing has more wide-ranging impact on reproductive behaviours than does nutritional challenge.

Sperm production responds to perceived sperm competition risk in male Drosophila melanogaster.

Postcopulatory sexual selection arising from female multiple mating leads to the evolution of ejaculates that maximize a male's reproductive success under sperm competition. Where the risk of sperm competition is variable, optimal fitness may be achieved by plastically altering ejaculate characteristics in response to the prevailing sperm competition environment. In the model species Drosophila melanogaster, males expecting to encounter sperm competition mate for longer and transfer more accessory proteins and sperm. Here we show that after being housed with a single rival for one week, the seminal vesicles of male D. melanogaster contain a significantly greater proportion of live sperm than those of males maintained alone, indicating adaptive adjustment of sperm quality in response to the perceived risk of sperm competition. This effect is due to an increase in the number of live sperm produced, indicating that males upregulate sperm production in response to the presence of rivals. Our data suggest that males show plasticity in the rate of spermatogenesis that is adaptive in the context of a fluctuating sperm competition environment.

Baculum morphology predicts reproductive success of male house mice under sexual selection.

BACKGROUND: Diversity in penile morphology is characterised by extraordinary variation in the size and shape of the baculum (penis bone) found in many mammals. Although functionally enigmatic, diversity in baculum form is hypothesised to result from sexual selection. According to this hypothesis, the baculum should influence the outcome of reproductive competition among males within promiscuous mating systems. However, a test of this key prediction is currently lacking. RESULTS: Here we show that baculum size explains significant variation in the reproductive success of male house mice under competitive conditions. After controlling for body size and other reproductive traits, the width (but not length) of the house mouse baculum predicts both the mean number of offspring sired per litter and total number of offspring sired. CONCLUSIONS: By providing the first evidence linking baculum morphology to male reproductive success, our results support the hypothesis that evolutionary diversity in baculum form is driven by sexual selection.

Exposure to sperm competition risk improves survival of virgin males.

Sperm competition between the ejaculates of multiple males for the fertilization of a given set of ova is taxonomically widespread. Males have evolved remarkable adaptations to increase their reproductive success under postcopulatory sexual selection, which in many species includes the ability to modify behaviour and ejaculate characteristics plastically to match the perceived level of sperm competition. Males of the model species Drosophila melanogaster increase mating duration and modify seminal fluid composition in response to short-term changes in sperm competition risk. If these responses increase a male's total investment in reproduction, he must either trade-off this cost against other life-history traits or suffer reduced survival. We tested whether mounting a plastic sperm competition response bears an instantaneous survival cost, and instead found that male D. melanogaster exposed to a high risk of sperm competition survive 12 per cent longer than those at low risk, equating to a 49 per cent reduction in the hourly hazard of death. This striking effect was found only among virgins: the high cost of mating in this species eliminates any such benefit among non-virgin males. Our results suggest that the improvement in survival found among virgins may be a product of males' tactical responses to sperm competition.

Female choosiness leads to the evolution of individually distinctive males.

Individual recognition is a taxonomically widespread ability that underlies a diverse suite of behaviors including the identification of individual nest-mates, agonistic opponents, and mating partners. However, as yet relatively little is known about the circumstances under which the requisite signal diversity can evolve. Here, we develop a model describing a novel mechanism of individual identity evolution via sexual selection. Females choose among a subset of males, but can select the most attractive male only when he bears a unique identity signal. This mimics a species in which mate assessment and choice are temporally separate, such as when females observe males in direct conflict and must subsequently locate the winner. When females in our model are choosy at least 10% of the time, diversity at individuality signaling loci evolves as a by-product of selection on male attractiveness more rapidly than does diversity at equivalent loci evolving only under neutral processes. Even at lower discrimination rates, drifting signal diversity gives the female choice mechanism sufficient traction to drive up average male attractiveness. The mechanism we describe here can significantly increase signal diversity at even low rates of discrimination by females.