What doesn’t kill you makes you stronger? Effects of paternal age at conception on fathers and sons

Abstract

Advancing male age is often hypothesised to reduce both male fertility and offspring quality through reproductive senescence. However, the effects of advancing male age on reproductive output and offspring quality need not always be deleterious. For example, older fathers might compensate for reproductive senescence by terminally investing in reproduction. Similarly, males that survive to reproduce at an old age, might carry alleles that confer high viability (viability selection) which are then inherited by offspring, or might have high reproductive potential (selective disappearance). Differentiating these mechanisms requires an integrated experimental study of paternal survival and reproductive performance, as well as offspring quality, which is currently lacking. UsingDrosophila melanogaster, we test the effects of paternal age at conception (PAC) on paternal survival and reproductive success, and the lifespans of sons. We discover that mating at an old age is temporarily linked with decreased future male survival, suggesting that mating-induced mortality is possibly due to old fathers being frail. We also find a quadratic reproductive ageing pattern, with an onset of senescence in late-life. We discover no evidence for terminal investment, and instead discover positive covariances between a father’s lifespan and his probability of siring offspring, for older PAC groups. Lastly, we show that sons born to older fathers live longer than those born to younger fathers, due to viability selection. Collectively, our results suggest that effects of advancing PAC need not be deleterious for fathers or offspring, and can increase fitness if older fathers produce more viable offspring.Lay summaryIt’s often assumed that old fathers have fewer or lower-quality offspring than young fathers. However, old fathers have on average, usually survived to and reproduced at an older age than young fathers, which might be signals of high quality of old fathers, and benefit offspring. These opposing predictions have rarely been tested, and it’s unclear what their combined influence is, in determining the father’s and offspring’s fitness. Using fruit flies, we explored how old paternal age affects a father’s reproduction and his sons’ lifespans. We find evidence for age-related reproductive decline in fathers. However, we also discover that fathers who mate at an older age live longer than fathers who mate at a younger age, and subsequently, the sons of older fathers live longer than sons of younger fathers. We suggest that the relationship between paternal age, paternal reproduction and lifespan, and offspring quality, is more complex than previously assumed, and that old fathers might provide benefits to their offspring that future studies need to consider.Teaser textIs an old dad really that bad? While old fathers might in some cases produce fewer offspring or offspring of worse quality than young fathers, they have also survived to an older age, thus might be of higher quality. We test how reproducing at an old age affects a father and his son’s fitness. We show that old fathers show evidence of reproductive senescence, but, surprisingly, produce sons that are longer lived than the sons of young fathers. This effect is driven largely by old fathers themselves living longer than young fathers, thus possibly passing alleles conferring higher viability to their sons. Our research is important because it reveals specific mechanisms that drive multifaceted effects of age on fitness.

Reproductive output of old polygynous males is limited by seminal fluid, not sperm number

“…All females used in our experiments were young (3-4 days old) and of dah background. Across all experiments, male flies between 3 to 11 days of age were considered young, and between 37 to 46 days as old, based on previous studies (Aguilar et al, 2023; Sanghvi et al, 2023; Sepil et al, 2020; Snoke and Promislow, 2003; Ruhmann et al, 2018; Turnell and Reinhardt, 2020).…”

“…Experimental virgin males were transferred onto new food once a week. Virgin males in our lab usually have a median and maximum lifespan of 50 and 90 days respectively (Sanghvi et al, 2023; Sepil et al 2020; also see Figure S7). Sample sizes across the three experiments are provided in Table S8.…”

“…Fruit flies have been used extensively for reproductive ageing research. Previous studies show that old males have lower quality and quantity of sperm (Sepil et al, 2020; Turnell and Reinhardt, 2020) and seminal fluid (reviewed in Fricke et al, 2023), and lower reproductive success (Sanghvi et al, 2023; Snoke and Promislow, 2003) than young males. Male fruit flies are polygynous (Hopkins et al, 2019b), and due to a low sperm to egg number ratio (Bjork and Pitnick, 2006), can become ejaculate depleted after few matings (Pitnick and Markow, 1994; Hopkins et al, 2019b).…”