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 DrosophilaGenetic 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.