Antioxidant allocation modulates sperm quality across changing social environments

Abstract

In promiscuous species, male reproductive success depends on their ability to mate with fertile females and on the fertilizing ability of their sperm. In such species, theory predicts that, owing to a trade-off between pre- and post-copulatory reproductive traits, males with lesser access to females should increase resource investment into those sperm traits that enhance fertilization success–usually referred to as ejaculate quality. This prediction has been validated in several taxa, yet studies on the physiological mechanisms modulating ejaculate quality are lacking. Sperm cells are highly vulnerable to oxidative stress, which impairs male fertility. Therefore, males that better protect their sperm from oxidative stress are expected to achieve higher ejaculate quality. Based on theoretical expectations, and since social dominance is a major determinant of mating opportunity, we predicted that subordinate males should invest more into the antioxidant protection of their sperm in order to achieve higher ejaculate quality. We maintained 60 male and 60 female wild-caught house sparrows Passer domesticus in outdoor aviaries, where we experimentally manipulated male social status to test our predictions. We measured cellular oxidative stress and enzymatic antioxidant activity in blood and sperm both before and after manipulating social ranks. Before manipulating the social status, we found that ejaculate viability correlated with oxidative stress level in sperm, with dominant males producing more oxidized and less viable ejaculates. Further, males at the lower end of the hierarchy produced ejaculates of similar quality to those of dominant males, suggesting that restricted access to resources might limit male reproductive strategies. After experimentally manipulating the social status, males matched their ejaculate quality to their new rank, while increases in antioxidant investment into ejaculates paralleled increases in ejaculate viability. Oxidative stress has been proposed as a general constraint to the evolution of life histories. Our results highlight oxidative stress and strategic antioxidant allocation as important proximate physiological mechanisms underlying male reproductive strategies.

Is sperm morphology functionally related to sperm swimming ability? A case study in a wild passerine bird with male hierarchies

“…Similar patterns were observed for total sperm length (Additional file 1 : Figure S2). Therefore, our results do not support the hypothesis that sperm morphology is functionally related to sperm swimming ability, and sperm morphology cannot explain the covariation between sperm motility and social status observed previously [ 49 ].…”

“…It is worth noting that although older house sparrow males seem to monopolize extra-pair paternities [ 43 ], Møller [ 48 ] has shown that more dominant males obtain more extra-pair copulations. Moreover, we have shown that male House Sparrows occupying different social ranks produce sperm performing differently [ 49 ]. In the current study, we used data from this previous study [ 49 ] and added morphological measurements of spermatozoa to test whether sperm performance is functionally related to sperm morphology.…”

“…Moreover, we have shown that male House Sparrows occupying different social ranks produce sperm performing differently [ 49 ]. In the current study, we used data from this previous study [ 49 ] and added morphological measurements of spermatozoa to test whether sperm performance is functionally related to sperm morphology. We predicted that, if sperm morphology explains variation in sperm performance, 1) sperm morphology should explain the differences we found in sperm performance across social ranks and should thus differ across social ranks, and 2) the direction of any correlations between sperm morphology and sperm velocity and/or sperm longevity should remain qualitatively the same across all social ranks.…”

Acute aggressive behavior perturbates the oxidative status of a wild bird independently of testosterone and progesterone

“…The effect that acute aggressive behaviors had on OXY concentrations was much stronger in females than in males (i.e., STI females had 39.62% lower OXY concentrations than control females while STI males had only 6.18% lower OXY concentrations than controls). This sex difference in sensitivity could be given by a differential re-allocation of antioxidants to: protect gametes [61], the developing embryo [see above; 19,56,62], and/or those tissues with the greatest oxygen consumption [e.g., muscles; 59]. Sex differences could also be explained by other physiological pathways besides an increase in activity levels (see below for further discussion).…”

Experimental evidence that winning or losing a fight does not affect sperm quality in a field cricket

“…This may explain the drop in sperm number and/or quality of contest winners reported for the Arctic charr (Rudolfsen Figenschou, Folstad, Tveiten, & Figenschou, 2006) and the domestic fowl (Pizzari, Cornwallis, & Froman, 2007), and the increase of sperm numbers in losers described in the broad-horned flour beetle (Okada, Yamane, & Miyatake, 2010). A strenuous fight may also induce physiological consequences, such as increasing cell oxidative stress levels known to be deleterious to sperm (Tremellen, 2008), with more aggressive males, generally winners, investing less in antioxidants and thus producing lower quality ejaculates (Mora et al, 2017).…”