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.

The hidden ageing costs of sperm competition

“…The female-specific deleterious effects of male sex peptide on lifespan and late-life reproductive success are mediated by several physiological pathways, notably through a rise in the release of juvenile hormones (Edward and Chapman, 2011). Strikingly, it has been recently shown thatindependently of the transfer of sex peptideboth mating and the amount of exposure to males not only decrease female survival but also increase the degree of physiological ageing (measured by the age-specific decline in climbing activity and starvation resistance; Bretman and Fricke, 2019). These results strongly emphasise the complexity of the interactions between mating rates, physiological processes and both reproductive and survival ageing in females.…”

Interactive effects of social environment, age and sex on immune responses in Drosophila melanogaster

“…Such factors could help to explain the widely observed social impacts on ageing (Steptoe, Shankar, Demakakos, & Wardle, ), especially as ageing and immunity share common mechanistic pathways (Carnes et al., ). However, a further consideration is that responses of males and females are likely to differ between social environments, for example because male–male aggression is generally responsive to population density (Knell, ), whereas for females interactions with males are stressful and ultimately increase their rate of senescence (Bretman & Fricke, ).…”

Plasticity in male mating behavior modulates female life history in fruit flies

“…; Wigby and Chapman ). A potential mechanism is that the increased investment into early reproduction results in an increased rate of senescence (Bretman and Fricke ). In fruit flies, females that have a genetic propensity to mate more produce more offspring early in life and die younger (Chapman et al.…”

“…The shorter lifespan of females mated to males exposed to rivals may be explained by a larger donation of Acps during matings from these males, as it is well known that exposure to Acps is associated with reduced longevity in female fruit flies (Chapman et al 1995;Wigby and Chapman 2005). A potential mechanism is that the increased investment into early reproduction results in an increased rate of senescence (Bretman and Fricke 2019). In fruit flies, females that have a genetic propensity to mate more produce more offspring early in life and die younger (Chapman et al 1995;Travers et al 2015), and lineages of the IV population that were artificially selected for increased longevity displayed a decreased investment into early-life offspring production and increased late-life production compared to the base population (i.e., a trend similar to the IV population in Fig.…”

“…5C). Bretman and Fricke () reported that female longevity and the onset of senescence is not influenced by the receipt of sex peptide, but females with more exposure to males (i.e., more matings) have reduced longevity and an accelerated expression of senescent decline in traits such as climbing speed and starvation resistance. Although sex peptide on its own appeared to have no detectable effect on female longevity, it may be that other Acps transferred during mating mediate the harmful effects of mating such as those related to stimulating reproduction (Bretman and Fricke ).…”