Female-limited X-chromosome evolution effects on male pre- and post-copulatory success

Intralocus sexual conflict arises when the expression of shared alleles at a single locus generates opposite fitness effects in each sex (i.e. sexually antagonistic alleles), preventing each sex from reaching its sex-specific optimum. Despite its importance to reproductive success, the relative contribution of intralocus sexual conflict to male pre- and post-copulatory success is not well-understood. Here, we used a female-limited X-chromosome (FLX) evolution experiment in Drosophila melanogaster to limit the inheritance of the X-chromosome to the matriline, eliminating possible counter-selection in males and allowing the X-chromosome to accumulate female-benefit alleles. After more than 100 generations of FLX evolution, we studied the effect of the evolved X-chromosome on male attractiveness and sperm competitiveness. We found a non-significant increase in attractiveness and decrease in sperm offence ability in males expressing the evolved X-chromosomes, but a significant increase in their ability to avoid displacement by other males' sperm. This is consistent with a trade-off between these traits, perhaps mediated by differences in body size, causing a small net reduction in overall male fitness in the FLX lines. These results indicate that the X-chromosome in D. melanogaster is subject to selection via intralocus sexual conflict in males.

Maintenance of fertility in the face of meiotic drive

Selfish genetic elements that gain a transmission advantage through the destruction of sperm have grave implications for drive male fertility. In the X-linked SR meiotic drive system of a stalk-eyed fly, we found that drive males have greatly enlarged testes and maintain high fertility despite the destruction of half their sperm, even when challenged with fertilising large numbers of females. Conversely, we observed reduced allocation of resources to the accessory glands that probably explains the lower mating frequency of SR males. Body size and eyespan were also reduced, which are likely to impair viability and pre-copulatory success. We discuss the potential evolutionary causes of these differences between drive and standard males.

Winners have higher pre-copulatory mating success but losers have better post-copulatory outcomes

In many animals, the outcomes of competitive interactions can have lasting effects that influence an individual's reproductive success and have important consequences for the strength and direction of evolution via sexual selection. In the fruit fly, Drosophila melanogaster , males that have won previous contests are more likely to win in subsequent conflicts and losers are more likely to lose (winner–loser effects), but the direct fitness consequences and genetic underpinnings of this plasticity are poorly understood. Here, we tested how male genotype and the outcomes of previous male–male conflicts influence male pre- and post-copulatory success. We quantified pre-copulatory success in a choice and no-choice context, and post-copulatory success by quantifying ejaculate offensive and defensive ability. We found that winners have higher reproductive success compared to losers in both pre-copulatory scenarios. However, losers consistently mated for a longer duration, boosted female fecundity and had an increased paternity share when they were the first males to mate, suggesting increased investment into post-copulatory mechanisms. Finally, by using clonal hybrids from the Drosophila Genetic Reference Panel, we documented that genetic variation explained a sizeable proportion of the observed differences between lines, and of the interaction between line and winner and loser effects. Our results place the behavioural data on winner–loser effects in an evolutionary context by documenting the potential fitness gain to males from altering their reproductive strategy based on fighting experience. Our data may also explain the presence and maintenance of trade-offs between different male reproductive strategies.

Lek Behavior of Mediterranean Fruit Flies: An Experimental Analysis

The Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae), is a ubiquitous pest of fruit trees, causing significant economic damage both in the U.S. and in Israel. Control efforts in the future will rely heavily on the sterile insect technique (SIT). Success of such operations hinges on the competitive ability of released males. The mating system of the medfly is based on leks. These are aggregations of sexually signaling males that attract females (who then select and copulate a courting male). A major component of male competitiveness is their ability to join existing leks or establish leks that are attractive to wild females. Accordingly, we identified leks and the behaviors associated with them as critical for the success of SIT operations. The objectives of this proposal were to determine 1. what makes a good lek site, 2. what are the energetic costs of lekking, 3. how females choose leks, and finally 4. whether the copulatory success of sterile males may be manipulated by particular pre-release diets and judicious spatial dispersal. We established that males choose lek sites according to their spatial location and penological status, that they avoid predators, and within the lek tree choose the perch that affords a compromise between optimal signalling, micro-climatic conditions and predation risk (Kaspi & Yuval 1999 a&b; Field et al 2000; Kaspi & Yuval submitted). We were able to show that leks are exclusive, and that only males with adequate protein and carbohydrate reserves can participate (Yuval et al 1998; Kaspi et al 2000; Shelly et al 2000). We determined that females prefer leks formed by protein fed, sexually experienced males (Shelly 2000). Finally, we demonstrated that adding protein to the diet of sterile males significantly enhances their probability of participating in leks and copulating wild females (Kaspi & Yuval 2000).