Male age alone predicts paternity success under sperm competition when effects of age and past mating effort are experimentally separated

Abstract

Older males often perform poorly under post-copulatory sexual selection. It is unclear, however, whether reproductive senescence is because of male age itself or the accumulated costs of the higher lifetime mating effort that is usually associated with male age. To date, very few studies have accounted for mating history and sperm storage when testing the effect of male age on sperm traits, and none test how age and past mating history influence paternity success under sperm competition. Here, we experimentally manipulate male mating history to tease apart its effects from that of age on ejaculate traits and paternity in the mosquitofish, Gambusia holbrooki . We found that old, naive males had more sperm than old, experienced males, while the reverse was true for young males. By contrast, neither male age nor mating history affected sperm velocity. Finally, using artificial insemination to experimentally control the number of sperm per male, we found that old males sired significantly more offspring than young males independently of their mating history. Our results highlight that the general pattern of male reproductive senescence described in many taxa may often be affected by two naturally confounding factors, male mating history and sperm age, rather than male age itself.

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success

“…2020; Aich et al. 2021). From these SNPs, a Hamming Distance Matrix for putative sires and offspring was calculated to determine paternity.…”

“…To assign paternity, we then genotyped single-nucleotide polymorphisms (SNPs) for all the putative sires, females and offspring using a commercial service DArTseq (Kilian et al 2012). This method has been successfully used to obtain paternity data in six previous studies on G. holbrooki (Booksmythe et al 2016;Head et al 2017;Marsh et al 2017;Vega-Trejo et al 2017;Spagopoulou et al 2020;Aich et al 2021). From these SNPs, a Hamming Distance Matrix for putative sires and offspring was calculated to determine paternity.…”

“…2020; fish: Aich et al. 2021). Here, we experimentally manipulated the mating history of young and old male eastern mosquitofish ( Gambusia holbrooki ) so that mating history and age were uncorrelated.…”

A synthesis of senescence predictions for indeterminate growth, and support from multiple tests in wild lake trout

“…Male fitness is a function of mating opportunities, sperm performance and offspring viability [34,45], which can be separated under experimental conditions (e.g. [47,48]). Older males generally produce sperm with reduced fertilization ability [27,29,34] and lead to higher rates of developmental abnormalities among offspring [29].…”

A synthesis of senescence predictions for indeterminate growth, and support from multiple tests in wild lake trout

“…Sperm are particularly vulnerable to oxidative damage [31], and the male mutational bias [42,46], has led to interest in human fertility and paternal effects. Male fitness is a function of mating opportunities, sperm performance and offspring viability [33,44], which can be separated under experimental conditions [e.g., 47,48].…”