No abstract

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.

In Drosophila melanogaster, prolonged exposure to males reduces the longevity and fecundity of females. This harm arises from the effects of male courtship behaviours and the toxic side effects of the accessory gland proteins (Acps) in their seminal fluids. Here, we examine the relationship between male exposure and its harmful effect on the lifetime fitness of his mates, and quantify the genetic basis for this variation. We found significant additive genetic variation in the magnitude of harm that males impose on females by exposing females to males from a variety of hemiclonal backgrounds for either a brief or prolonged period of time and measuring their fecundity, a meaningful fitness index. Furthermore, we discovered a strong negative correlation between the magnitude of harm and the short-term effects of male exposure on female fitness. We discuss the evolutionary significance of these results with regards to potential life-history trade-offs in females, and its relationship to male body size.

Female mate choice is a complex decision‐making process that involves many context‐dependent factors. In Drosophila melanogaster, a model species for the study of sexual selection, indirect genetic effects (IGEs) of general social interactions can influence female mate choice behaviors, but the potential impacts of IGEs associated with mating experiences are poorly understood. Here, we examined whether the IGEs associated with a previous mating experience had an effect on subsequent female mate choice behaviors and quantified the degree of additive genetic variation associated with this effect. Females from 21 different genetic backgrounds were housed with males from one of two distinct genetic backgrounds for either a short (3 hr) or long (48 hr) exposure period and their subsequent mate choice behaviors were scored. We found that the genetic identity of a previous mate significantly influenced a female's subsequent interest in males and preference of males. Additionally, a hemiclonal analysis revealed significant additive genetic variation associated with experience‐dependent mate choice behaviors, indicating a genotype‐by‐environment interaction for both of these parameters. We discuss the significance of these results with regard to the evolution of plasticity in female mate choice behaviors and the maintenance of variation in harmful male traits.

In many species, intense male‐male competition for the opportunity to sire offspring has led to the evolution of selfish reproductive traits that are harmful to the females they mate with. In the fruit fly, Drosophila melanogaster, males modulate their reproductive behavior based on the perceived intensity of competition in their premating environment. Specifically, males housed with other males subsequently transfer a larger ejaculate during a longer mating compared to males housed alone. Although the potential fitness benefits to males from such plasticity are clear, its effects on females are mostly unknown. Hence, we tested the long‐term consequences to females from mating with males with distinct social experiences. First, we verified that competitive experience influences male mating behavior and found that males housed with rivals subsequently have shorter mating latencies and longer mating durations. Then, we exposed females every other day for 20 days to males that were either housed alone or with rivals, and subsequently measured their fitness. We found that females mated to males housed with rivals produce more offspring early in life but fewer offspring later in life and have shorter lifespans but similar intrinsic population growth rates. These results indicate that plasticity in male mating behavior can influence female life histories by altering females’ relative allocation to early versus late investment in reproduction and survival.