Exposure to males, but not receipt of sex peptide, accelerates functional ageing in female fruit flies

Abstract

Increased exposure to males can affect females negatively, reducing female life span and fitness. These costs could derive from increased mating rate and also harassment by males. Additionally, early investment in reproduction can increase the onset or rate of senescence in reproductive traits. Hence, there is a tight link between reproduction and ageing. Here, we assess how mating and encounter rate with males impacts declines in female functional traits that are not directly involved in reproduction. In Drosophila melanogaster fruit flies, exposure to males and mating reduces female life span through harassment and receipt of seminal proteins, including sex peptide (SP). We manipulated the intensity of female exposure to males and regularly assessed female stress responses and recorded physiological traits over her lifetime. Both mating itself and increased exposure to males accelerate declines in female climbing ability and starvation resistance. However, this is not related to changes in female body mass or fat storage. Moreover, these declines are not driven by the receipt of SP. Our results suggest some synchrony in senescence across traits in response to female exposure to males; however, this is not universal, as we did not find this for physiological traits. Synchrony in senescence has been theorized but little supported in the literature. It is clear that ageing is a multifaceted trait; to understand environmental impacts on ageing rates, we must measure more than life span and indeed measure senescence in multiple traits. Specifically, our work shows that we must identify which female traits are sensitive to elevated mating activity to understand the impact of antagonistic interactions between the sexes on female ageing patterns. A plain language summary is available for this article.