Male sperm storage impairs sperm quality in the zebrafish

Abstract

Variation in sperm traits is widely documented both at inter- and intraspecific level. However, sperm traits vary also between ejaculates of the same male, due for example, to fluctuations in female availability. Variability in the opportunities to mate can indeed have important consequences for sperm traits, as it determines how often sperm are used, and thus the rate at which they are produced and how long they are stored before the mating. While being stored within males’ bodies, sperm are subjected to ageing due to oxidative stress. Sperm storage may significantly impair sperm quality, but evidence linking male sperm storage and variation in sperm traits is still scarce. Here, we tested the effect of the duration of sperm storage on within-male variation in sperm traits in the zebrafish, Danio rerio. We found that without mating opportunities, sperm number increased as storage duration increased, indicating that sperm continue to be produced and accumulate over time within males without being discharged in another way. Long sperm storage (12 days) was associated with an overall impairment in sperm quality, namely sperm motility, sperm longevity, and sperm DNA fragmentation, indicating that sperm aged, and their quality declined during storage. Our results confirm that male sperm storage may generate substantial variation in sperm phenotype, a source of variation which is usually neglected but that should be accounted for in experimental protocols aiming to assay sperm traits or maximise fertilization success.

Sperm metabolic rate predicts female mating frequency acrossDrosophilaspecies

“…Finally, sperm metabolism in the male may itself affect mating rate, as sperm also age in male storage (Gasparini et al. 2017; Cattelan and Gasparini 2021), and males may mate more often in order to avoid transferring such aged sperm (Reinhardt and Siva‐Jothy 2005; Hettyey et al. 2012).…”

“…If individual-specific metabolic signatures are retained across storage environments within a given species, then at least some species-specific metabolic signatures are also likely to be retained between male and female storage. Finally, sperm metabolism in the male may itself affect mating rate, as sperm also age in male storage (Gasparini et al 2017;Cattelan and Gasparini 2021), and males may mate more often in order to avoid transferring such aged sperm (Reinhardt and Siva-Jothy 2005;Hettyey et al 2012).…”

“…2008), with corresponding decreases in various aspects of sperm function, including motility and velocity (Gasparini et al. [2017]; Cattelan and Gasparini [2021]); though see Vega‐Trejo et al. [2019)]), fertilization capacity (White et al.…”

“…1i). From the time of production to the moment of fertilization, sperm cells undergo a process of aging that involves an accumulation of damage to a range of cellular components (Reinhardt 2007;Pizzari et al 2008), with corresponding decreases in various aspects of sperm function, including motility and velocity (Gasparini et al [2017]; Cattelan and Gasparini [2021]); though see Vega-Trejo et al [2019)]), fertilization capacity (White et al 2008), and competitive success (Gasparini et al 2017;Gasparini et al 2018). This decline in sperm function with increasing sperm age represents a potential cost for both males and females, as offspring resulting from old sperm have reduced fitness in a variety of taxa ([White et al 2008;Gasparini et al 2017]; reviewed in 4 and 5).…”

Separating the effects of paternal age and mating history: Evidence for sex‐specific paternal effect in eastern mosquitofish

“…It is possible that the assigned period of mating was insufficient to reveal negative effects associated with repeated mating for some traits. Although, we minimized variation in postmeiotic sperm age, and sperm velocity did not differ with mating treatment (Aich et al 2021b), differences in other ejaculate traits, such as sperm viability and seminal fluid content, might explain the larger brood size of females mated to more experienced males (Borziak et al 2016;Cardozo et al 2020;Ramm 2020;Sepil et al 2020;Cattelan and Gasparini 2021).…”