Sperm storage by males causes changes in sperm phenotype and influences the reproductive fitness of males and their sons

Abstract

Recent studies suggest that environmentally induced effects on sperm phenotype can influence offspring phenotype beyond the classic Mendelian inheritance mechanism. However, establishing whether such effects are conveyed purely through ejaculates, independently of maternal environmental effects, remains a significant challenge. Here, we assess whether environmentally induced effects on sperm phenotype affects male reproductive success and offspring fitness. We experimentally manipulated the duration of sperm storage by males, and thus sperm age, in the internally fertilizing fish Poecilia reticulata. We first confirm that sperm ageing influences sperm quality and consequently males reproductive success. Specifically, we show that aged sperm exhibit impaired velocity and are competitively inferior to fresh sperm when ejaculates compete to fertilize eggs. We then used homospermic (noncompetitive) artificial insemination to inseminate females with old or fresh sperm and found that male offspring arising from fertilizations by experimentally aged sperm suffered consistently impaired sperm quality when just sexually mature (four months old) and subsequently as adults (13 months old). Although we have yet to determine whether these effects have a genetic or epigenetic basis, our analyses provide evidence that environmentally induced variation in sperm phenotype constitutes an important source of variation in male reproductive fitness that has far reaching implications for offspring fitness. K E Y W O R D S :Epigenetics, male sperm storage, paternal effects, sperm ageing, sperm competition, sperm velocity. Impact SummaryProlonged sperm storage is associated with a reduction in sperm quality in many species, including humans. Such effects have potentially important implications for a male's reproductive fitness because males that store sperm for prolonged periods (e.g., because they become isolated from females, or fail to secure mates) may suffer compromised fertility, or reduced fertilization success when their sperm compete with rival (fresher) sperm during sperm competition. However, in addition to such direct costs associated with male sperm storage, recent studies have suggested a link between environmentally induced changes in sperm quality and offspring traits. Sperm ageing therefore constitutes a potentially widespread source of nongenetic (i.e., not linked to genes) variance in offspring fitness. Here, using the live-bearing guppy (Poecilia reticulata), we provide experimental support for these ideas, showing that sperm storage has far reaching implications for male reproductive fitness. First, we show that males whose sperm were held longer inside their reproductive organs fertilize relatively fewer eggs when in competition with those from males who produced fresher sperm. Second, we provide empirical evidence that the reduction in sperm quality caused by long-term sperm storage has effects that transcend generations by influencing the reproductive fitness of adult offspring; offspring sired by males with age...

The effects of male age, sperm age and mating history on ejaculate senescence

“…Post-meiotic sperm senescence is also apparent as a reduction in sperm motility and velocity (Gasparini, Kelley, & Evans, 2014;Gasparini, Daymond, & Evans, 2018;Pizzari et al, 2008;Vishwanath & Shannon, 1997; but see Firman, Young, Rowe, Duong, & Gasparini, 2015). Crucially, several recent innovative studies have shown that sperm competitiveness declines with sperm age (Gasparini et al, 2018;Gasparini, Dosselli, & Evans, 2017). These studies suggest that sperm age must be controlled for in age-based studies of male sperm traits.…”

Sperm ageing: A complex business

“…Younger males produced faster sperm than older males, while sperm age had the opposite effect: fresh sperm swam more slowly than stored sperm. This last result is particularly interesting because it contrasts with findings in guppies (Gasparini et al, 2014(Gasparini et al, , 2017(Gasparini et al, , 2019)-which, like mosquitofish, are poeciliids. Why aged sperm show increased speed in mosquitofish while showing reduced speed | 1189…”

“…Sperm age may even affect the offspring's own gamete function: male guppies developing from eggs fertilized by old sperm go on to produce sperm that swim more slowly (Gasparini et al, 2017).…”

IntroducingEvolution Letters

“…Our very first paper, by Amanda Gibson et al (2017), is an empirical study examining one of the classical questions in evolutionary biology-the twofold cost of sex. Another paper considers how postcopulatory sexual selection has resulted in transgenerational fitness consequences of sperm storage in an internally fertilizing fish species (Gasparini et al 2017). Our first macroevolutionary paper (Greenberg and Mooers 2017) uses a comparative approach to show that speciation and extinction rates are correlated in amphibians; a pattern that has not been widely described in other taxonomic groups.…”