Biology subjects

Pizzari, T.

Publications and source records attributed to Pizzari, T..

4 recordsLinked to original sources

bioRxiv2024

No evidence for paternal age effects on sons or daughters, when accounting for paternal sperm storage

O_LIThe age at which a father reproduces is predicted to affect not only his own fertility but also the fitness of his offspring. Specifically, offspring born to old fathers are assumed to be of a lower quality than those conceived by young fathers. However, when fathers have low mating rates, paternal age might be confounded with the duration for which mature sperm are stored in fathers prior to ejaculation. C_LIO_LIStudies that disentangle the confounding effects of paternal sperm storage duration from those of paternal age, on offspring, are lacking. We use Drosophila melanogaster to test the separate and interactive effects of paternal age and sperm storage duration (sexual rest) on the survival and lifetime reproduction of offspring. C_LIO_LIAs expected, old fathers produce fewer offspring than young fathers. But surprisingly, paternal age does not influence the survival or lifetime reproductive success of either sons or daughters. Instead, sons conceived by fathers with long durations of sexual rest have lower reproductive success than sons conceived by fathers with short durations of sexual rest. C_LIO_LIWe further discover that daughters of low reproductive quality selectively disappear with age, but sons do not, highlighting that demographic processes need to be accounted for when studying paternal age effects. C_LIO_LIOverall, our study suggests that paternal age effects might not be as pervasive as previously assumed. We emphasize that a more nuanced understanding of the mechanisms causing paternal age effects is required, so that studies do not misattribute effects of paternal sperm storage to age. C_LI

evolutionary biology↗

bioRxiv2024

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

Advancing male age can lead to reproductive senescence, which in males is thought to be largely driven by declines in the numbers of sperm transferred by old males. This decline is predicted to be particularly pronounced in polygynous species, where males become sperm limited over a mating sequence. However, males also transfer seminal fluid to females, and little is known about the contribution of seminal fluid to constrain the reproductive output of old, multiply-mating males. Using Drosophila melanogaster, we investigated whether age-related variation in male reproductive output is driven by differential limitation of sperm or seminal fluid, over a series of experimental matings. Consistent with reproductive senescence, old males produced fewer offspring than young males. However, this pattern was not driven by sperm limitation, with old males having more sperm and transferring similar numbers of sperm to a female, compared to young males. Yet surprisingly, females stored fewer sperm when mated to old than young males. Notably, females mated to old multiply-mating males produced more offspring when supplemented with seminal fluid, suggesting that fertility of old males over successive matings was limited by seminal fluid availability. Generally, our study indicates that germline maintenance might be prioritised over somatic maintenance as hypothesized by the disposable soma theory of ageing, and that seminal fluid senescence is a key contributor of reproductive decline with age. While other factors such as differential sperm viability and female post-mating responses could have also influenced our results, our study highlights the under-appreciated role of seminal fluid in mediating male reproductive senescence in polygynous species. Significance statementA key assumption in ageing research is that old males are less fertile than young males, and that this reduced fertility is partly driven by old males producing fewer sperm. However, senescence in male fertility can be caused via other ejaculate-mediated pathways, which we investigate using fruit flies. Contrary to expectations, we reveal that senescence in male fertility is not because of declines in male sperm reserves, but is instead due to age-related changes in seminal fluid and differences in female sperm storage with male age. These declines in the reproductive output of old, multiply-mating males are alleviated by supplementing females with "extra" seminal fluid. Our study demonstrates that male reproductive senescence is reversible, highlighting the underappreciated role of seminal fluid in modulating senescence in polygynous species. These results have potential for improving animal fertility and our understanding of sexual selection.

evolutionary biology↗

bioRxiv2023

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

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. Using Drosophila 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 fathers 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 summaryIts 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 its unclear what their combined influence is, in determining the fathers and offsprings fitness. Using fruit flies, we explored how old paternal age affects a fathers 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 sons 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.

evolutionary biology↗

bioRxiv2023

No general effects of advancing male age on ejaculates: a meta-analysis across the animal kingdom

Senescence, the deterioration of organismal function with advancing age, is a puzzling biological phenomenon. While actuarial senescence (i.e., age-dependent increases in mortality rates) is well described across some taxa, reproductive senescence (i.e. age- dependent declines in reproduction) is less understood, especially in males, with mixed patterns reported across studies. To examine the evidence for male reproductive senescence, we investigated how advancing male age affects ejaculate traits across non-human animals via a meta-analysis yielding 1814 effect sizes from 379 studies. We found no evidence for a general pattern of reproductive senescence. Instead, we found high heterogeneity for how reproduction changes with male age across animals. Some of this heterogeneity (>10%) was associated with biological factors. For example, there were taxonomical differences for some ejaculate traits -- sperm motility declined with male age in lab rodents and fish, whereas ejaculate size improved with male age in bulls, fish, and insects. Some methodological factors were also important in explaining this heterogeneity: studies sampling a larger proportion of a species lifespan were more likely to detect senescence in ejaculate traits, emphasising the need to examine the full life cycle of species to document senescence. Contrary to predictions, we reveal that the evidence for senescence in ejaculate traits is sporadic. Our findings will help generate novel hypotheses and identify more effective methodological approaches for studying male reproductive senescence.

evolutionary biology↗