Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila

Abstract

<jats:p>Declining ejaculate performance with male age is taxonomically widespread and has broad fitness consequences. Ejaculate success requires fully functional germline (sperm) and soma (seminal fluid) components. However, some aging theories predict that resources should be preferentially diverted to the germline at the expense of the soma, suggesting differential impacts of aging on sperm and seminal fluid and trade-offs between them or, more broadly, between reproduction and lifespan. While harmful effects of male age on sperm are well known, we do not know how much seminal fluid deteriorates in comparison. Moreover, given the predicted trade-offs, it remains unclear whether systemic lifespan-extending interventions could ameliorate the declining performance of the ejaculate as a whole. Here, we address these problems using <jats:italic>Drosophila melanogaster.</jats:italic> We demonstrate that seminal fluid deterioration contributes to male reproductive decline via mating-dependent mechanisms that include posttranslational modifications to seminal proteins and altered seminal proteome composition and transfer. Additionally, we find that sperm production declines chronologically with age, invariant to mating activity such that older multiply mated males become infertile principally via reduced sperm transfer and viability. Our data, therefore, support the idea that both germline and soma components of the ejaculate contribute to male reproductive aging but reveal a mismatch in their aging patterns. Our data do not generally support the idea that the germline is prioritized over soma, at least, within the ejaculate. Moreover, we find that lifespan-extending systemic down-regulation of insulin signaling results in improved late-life ejaculate performance, indicating simultaneous amelioration of both somatic and reproductive aging.</jats:p>

The hidden ageing costs of sperm competition

“…However, Koppik and colleagues (2018) recently discovered that, at old ages, sexually active male D. melanogaster display shorter mating, resulting in a lower number of eggs laid by females than following mating with virgin males. However, this pattern might be more likely due to a decrease in sperm number rather than in the quantity of seminal fluid proteins delivered to females, when sexually active males are reaching old ages (see Sepil et al 2020).…”

Influences of male age, mating history and starvation on female post mating aggression and feeding inDrosophila

“…A male’s individual condition is also critical for determining males’ ability to produce and transfer ejaculates. Intrinsic factors such as age, mating activity, and diet have all been shown to influence male ejaculate quality, quantity and composition, impacting both male and female fitness (Fricke, Bretman, & Chapman, 2008; Macartney et al, 2019; Sepil et al, 2020). In both vertebrate and invertebrate taxa, older males tend to transfer smaller or lower quality ejaculates, leading to a decline in fertility or offspring fitness (Dean et al, 2010; Preston, Saint Jalme, Hingrat, Lacroix, & Sorci, 2015; Ruhmann, Koppik, Wolfner, & Fricke, 2018).…”

“…Here we use the fruit fly Drosophila melanogaster to test how variation in three male traits known to influence ejaculate characteristics affect an important female post-mating behaviour – female aggression. We chose male age, mating history, and adult feeding status as our male traits, as all three characters are related to male condition and have been shown to strongly influence some aspect of the ejaculate in D. melanogaster and other species (Fricke et al, 2008; Macartney et al, 2019; Sepil et al, 2020). In D. melanogaster , male reproductive function declines with age, but this is heavily dependent on male sexual activity and differs for different ejaculate components.…”

“…In D. melanogaster , male reproductive function declines with age, but this is heavily dependent on male sexual activity and differs for different ejaculate components. Sperm production declines with age, regardless of mating history, and old sexually active males transfer fewer sperm to females, leading to severe reductions in fecundity and reproductive success (Koppik & Fricke, 2017; Koppik et al, 2018; Sepil et al, 2020). Surprisingly, sexually active males show no change in their Sfp production and transfer with age.…”

“…Surprisingly, sexually active males show no change in their Sfp production and transfer with age. Instead old sexually inactive males transfer a lower abundance of Sfps to females, but their mates show no change in their fecundity or reproductive success (Sepil et al, 2020). Finally, for some Sfps, protein quality declines with age, partly explaining the age-related reduction in male reproductive function.…”