Resource limitation and responses to rivals in males of the fruit fly Drosophila melanogaster

Diet has a profound direct and indirect effect on reproductive success in both sexes. Variation in diet quality and quantity can significantly alter the capacity of females to lay eggs and of males to deliver courtship. Here we tested the effect of dietary resource limitation on the ability of male D. melanogaster to respond adaptively to rivals by extending their mating duration. Previous work done under ad libitum diet conditions showed that males exposed to rivals prior to mating significantly extend mating duration, transfer more ejaculate proteins and achieve higher reproductive success. Such adaptive responses are predicted to occur because male ejaculate production may be limited and hence ejaculate resources require allocation across different reproductive bouts, to balance current versus future reproductive success. However, when males suffer dietary limitation, and potentially have fewer reproductive resources to apportion, we expect adaptive allocation of responses to rivals to be minimised. We tested this prediction and found that males held on agar-only diets for 5-7 days lost the ability to extend mating following exposure to rivals. Interestingly, extended mating was retained in males held on low yeast/sugar: no sugar/yeast diet treatments, but was mostly lost when males were maintained on ‘imbalanced’ diets in which there was high yeast: no sugar and vice versa. Overall, the results show that males exhibit adaptive responses to rivals according to the degree of dietary resource limitation and to the ratio of individual diet components

Resource-dependent evolution of female resistance responses to sexual conflict

Sexual conflict can promote the evolution of dramatic reproductive adaptations as well as resistance to its potentially costly effects. Theory predicts that responses to sexual conflict will vary significantly with resource levels-when scant, responses should be constrained by trade-offs, when abundant, they should not. However, this can be difficult to test because the evolutionary interests of the sexes align upon short-term exposure to novel environments, swamping any selection due to sexual conflict. What is needed are investigations of populations that are well adapted to both differing levels of sexual conflict and resources. Here, we used this approach in a long-term experimental evolution study to track the evolution of female resistance to sexual conflict in the fruit fly Drosophila melanogaster. In resource-rich regimes, high-conflict females evolved resistance to continual exposure to males. There was no difference in baseline survival, consistent with the idea that responses evolving under nutritional abundance experienced no trade-offs with resistance. In the poor resource regimes, the ability of high-conflict females to evolve resistance to males was severely compromised and they also showed lower baseline survival than low-conflict females. This suggested high-conflict females traded off somatic maintenance against any limited resistance they had evolved in response to sexual conflict. Overall, these findings provide experimental support for the hypothesis that evolutionary responses to sexual conflict are critically dependent upon resource levels

Satyrization in Drosophila fruitflies

The satyr of Greek mythology was half-man, half-goat, with an animal persona signifying immoderate sexual appetites. In biology, satyrization is the disruption of reproduction in matings between closely related species. Interestingly, its effects are often reciprocally asymmetric, manifesting more strongly in one direction of heterospecific mating than the other. Heterospecific matings are well known to result in female fitness costs due to the production of sterile or inviable hybrid offspring and can also occur due to reduced female sexual receptivity, lowering the likelihood of any subsequent conspecific matings. Here we investigated the costs and mechanisms of satyrization in the Drosophila melanogaster species subgroup of fruitflies. The results showed that D. simulans females experienced higher fitness costs from a loss of remating opportunities due to significantly reduced post-mating sexual receptivity than did D. melanogaster females, as a result of reciprocal heterospecific matings. Reciprocal tests of the effects of male reproductive accessory gland protein (Acp) injections on female receptivity in pairwise comparisons between D. melanogaster and five other species within the melanogaster species subgroup revealed significant post-mating receptivity asymmetries. This was due to variation in the effects of heterospecific Acps within species with which D. melanogaster can mate, and significant but nonasymmetric Acp effects in species with which it cannot. We conclude that asymmetric satyrization due to post-mating effects of Acps may be common among diverging and hybridising species. The findings are of interest in understanding the evolution of reproductive isolation and species divergence

Plastic male mating behavior evolves in response to the competitive environment

Male reproductive phenotypes can evolve in response to the social and sexual environment. The expression of many such phenotypes may also be plastic within an individual's lifetime. For example, male Drosophila melanogaster show significantly extended mating duration following a period of exposure to conspecific male rivals. The costs and benefits of reproductive investment, and plasticity itself, can be shaped by the prevailing sociosexual environment and by resource availability. We investigated these ideas using experimental evolution lines of D. melanogaster evolving under three fixed sex ratios (high, medium, and low male-male competition) on either rich or poor adult diets. We found that males evolving in high-competition environments evolved longer mating durations overall. In addition, these males expressed a novel type of plastic behavioral response following exposure to rival males: they both significantly reduced and showed altered courtship delivery, and exhibited significantly longer mating latencies. Plasticity in male mating duration in response to rivals was maintained in all of the lines, suggesting that the costs of plasticity were minimal. None of the evolutionary responses tested were consistently affected by dietary resource regimes. Collectively, the results show that fixed behavioral changes and new augmentations to the repertoire of reproductive behaviors can evolve rapidly

Sex ratio and the evolution of aggression in fruit flies

Aggressive behaviours are among the most striking displayed by animals, and aggression strongly impacts fitness in many species. Aggression varies plastically in response to the social environment, but we lack direct tests of how aggression evolves in response to intra-sexual competition. We investigated how aggression in both sexes evolves in response to the competitive environment, using populations of Drosophila melanogaster that we experimentally evolved under female-biased, equal, and male-biased sex ratios. We found that after evolution in a female-biased environment—with less male competition for mates—males fought less often on food patches, although the total frequency and duration of aggressive behaviour did not change. In females, evolution in a female-biased environment—where female competition for resources is higher—resulted in more frequent aggressive interactions among mated females, along with a greater increase in post-mating aggression. These changes in female aggression could not be attributed solely to evolution either in females or in male stimulation of female aggression, suggesting that coevolved interactions between the sexes determine female post-mating aggression. We found evidence consistent with a positive genetic correlation for aggression between males and females, suggesting a shared genetic basis. This study demonstrates the experimental evolution of a behaviour strongly linked to fitness, and the potential for the social environment to shape the evolution of contest behaviours

Sexual conflict maintains variation at an insecticide resistance locus

Background: The maintenance of genetic variation through sexually antagonistic selection is controversial, partly because specific sexually-antagonistic alleles have not been identified. The Drosophila DDT resistance allele (DDT-R) is an exception. This allele increases female fitness, but simultaneously decreases male fitness, and it has been suggested that this sexual antagonism could explain why polymorphism was maintained at the locus prior to DDT use. We tested this possibility using a genetic model and then used evolving fly populations to test model predictions. Results: Theory predicted that sexual antagonism is able to maintain genetic variation at this locus, hence explaining why DDT-R did not fix prior to DDT use despite increasing female fitness, and experimentally evolving fly populations verified theoretical predictions. Conclusions: This demonstrates that sexually antagonistic selection can maintain genetic variation and explains the DDT-R frequencies observed in nature

Pleiotropic Effects of DDT Resistance on Male Size and Behaviour

Understanding the evolution and spread of insecticide resistance requires knowing the relative fitness of resistant organisms. In the absence of insecticides, resistance is predicted to be costly. The Drosophila melanogaster DDT resistance allele (DDT-R) is associated with a male mating cost. This could be because resistant males are generally smaller, but DDT-R may also alter courtship behaviours. Here we tested for body size and courtship effects of DDT-R on mating success in competitive and non-competitive mating trials respectively. We also assessed relative aggression in resistant and susceptible males because aggression can also influence mating success. While the effect of DDT-R on male size partly contributed to reduced mating success, resistant males also had lower rates of courtship and were less aggressive than susceptible males. These differences contribute to the observed DDT-R mating costs. Additionally, these pleiotropic effects of DDT-R are consistent with the history and spread of resistance alleles in nature

Methanethiol-dependent dimethylsulfide production in soil environments

Dimethylsulfide (DMS) is an environmentally important trace gas with roles in sulfur cycling, signalling to higher organisms and in atmospheric chemistry. DMS is believed to be predominantly produced in marine environments via microbial degradation of the osmolyte dimethylsulfoniopropionate (DMSP). However, significant amounts of DMS are also generated from terrestrial environments, for example, peat bogs can emit ~6 μmol DMS m−2 per day, likely via the methylation of methanethiol (MeSH). A methyltransferase enzyme termed ‘MddA’, which catalyses the methylation of MeSH, generating DMS, in a wide range of bacteria and some cyanobacteria, may mediate this process, as the mddA gene is abundant in terrestrial metagenomes. This is the first study investigating the functionality of MeSH-dependent DMS production (Mdd) in a wide range of aerobic environments. All soils and marine sediment samples tested produced DMS when incubated with MeSH. Cultivation-dependent and cultivation-independent methods were used to assess microbial community changes in response to MeSH addition in a grassland soil where 35.9% of the bacteria were predicted to contain mddA. Bacteria of the genus Methylotenera were enriched in the presence of MeSH. Furthermore, many novel Mdd+ bacterial strains were isolated. Despite the abundance of mddA in the grassland soil, the Mdd pathway may not be a significant source of DMS in this environment as MeSH addition was required to detect DMS at only very low conversion rates

Data from: Manipulation of feeding regime alters sexual dimorphism for lifespan and reduces sexual conflict in Drosophila melanogaster

Sexual dimorphism for lifespan (SDL) is widespread, but poorly understood. A leading hypothesis, which we test here, is that strong SDL can reduce sexual conflict by allowing each sex to maximize its sex-specific fitness. We used replicated experimental evolution lines of the fruit fly, Drosophila melanogaster, which had been maintained for over 360 generations on either unpredictable ‘Random’ or predictable ‘Regular’ feeding regimes. This evolutionary manipulation of feeding regime led to robust, enhanced SDL in Random over control, Regular lines. Enhanced SDL was associated with a significant increase in the fitness of focal males, tested with wild-type (WT) females. This was due to sex-specific changes to male life history, manifested as increased early reproductive output and reduced survival. In contrast, focal female fitness, tested with WT males, did not differ across regimes. Hence increased SDL was associated with a reduction in sexual conflict, which increased male fitness and maintained fitness in females. Differences in SDL were not associated with developmental time or developmental survival. Overall, the results showed that the expression of enhanced SDL, resulting from experimental evolution of feeding regimes, was associated with male-specific changes in life history, leading to increased fitness and reduced sexual conflict