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.

Keywords: Epigenetics; male sperm storage; paternal effects; sperm ageing; sperm competition; sperm velocity.

Figure 1

Schematic view of the experimental design. The length of sperm storage was manipulated in two groups of adult males to obtain fresh and aged sperm (see Methods for further details). Ejaculates were then collected and used in (i) sperm assays and (ii) artificial inseminations in both competitive (heterospermic) and noncompetitive (homospermic) fertilization trials.

Figure 2

(A) In vitro sperm swimming velocity of males according to their treatment (“fresh” or “aged”). (B–C) Sperm swimming velocity measured from male offspring according to the treatment experienced by their fathers, measured at the onset of sexual maturity (four months of age, panel B), and at 13 months of age (panel C). Bars represent mean ± SE.

Figure 3

Proportion of offspring sired by males from aged‐ or fresh‐sperm group in each of the (n = 30) families. Numbers at top indicate the number of offspring per brood.