Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat)

Abstract

In social systems with alternative reproductive tactics, sneakers face a higher level of sperm competition than harem males and hence are predicted to allocate more resources to ejaculates. Antioxidants can protect sperm against oxidative stress, and thus, their allocation to the ejaculate may depend on mating tactic. In this study on the frugivorous bat Carollia perspicillata, we assessed, for harem and sneaker males, four sperm mobility traits, blood and ejaculate markers of the redox balance and the ejaculate to blood ratios of the redox markers. Under higher sperm competition, sneaker males should allocate proportionally more antioxidant resources to the protection of sperm than harem males. In contrast, harem males should favour pre-copulatory functions, which comprise the protection of blood. We found significantly higher sperm velocity and sperm survival in sneakers. There was no correlation between sperm mobility and sperm enzymatic antioxidant activity or ejaculate levels of lipid peroxidation (oxidative damage). Ejaculate levels of lipid peroxidation and sperm survival showed a significantly positive correlation, which could be attributed to the role of reactive oxygen species for sperm capacitation. Harem and sneaker males showed similar levels of redox balance markers in ejaculate and blood. However, harem males showed a higher ratio of oxidized over reduced glutathione in blood, which may indicate higher cellular stress due to higher metabolism. Overall, our findings suggest that sneakers of C. perspicillata compensate for a higher level of sperm competition by higher sperm mobility. Significance statementIn social systems with alternative reproductive tactics, sneakers face higher level of sperm competition than harem males and hence are predicted to allocate more resources to ejaculates. Antioxidants can protect sperm against oxidative stress, and thus, their allocation to the ejaculate may depend on mating tactic. In this study on the frugivorous bat Carollia perspicillata, we found sperm swimming significantly faster and longer in sneaker males compared to harem males. However, traits other than the investigated antioxidant may favour higher sperm mobility. Measured redox pattern in blood of harem males may indicate higher cellular stress due to higher metabolism. Our results provide support to the current sperm competition models at the intraspecific level, which is still debated for internal fertilizers. This study contributes to better understanding the trade-offs and adaptations resulting from alternative reproductive tactics in mammals.

Individual asymmetry as a predictor of fitness in the batCarollia perspicillata

“…According to Fasel et al (2016), the harem males father approximately 60% of the offspring in a given breeding season, whereas the remaining 40% are fathered by peripheral and bachelor males. Fasel et al (2017) found that sperm velocity and survival were lower in harem males than in sneaker (bachelor + peripheral) males of C. perspicillata. The authors did not associate testicle size with sperm quality measurements, but suggest that ejaculate volume was not statistically different between male mating tactics.…”

“…Fasel et al. () found that sperm velocity and survival were lower in harem males than in sneaker (bachelor + peripheral) males of C. perspicillata . The authors did not associate testicle size with sperm quality measurements, but suggest that ejaculate volume was not statistically different between male mating tactics.…”

“…Males and females of C. perspicillata exhibit high fidelity to natal roosts, but a small proportion might emigrate to different roosts (Fleming, ). The mating system of C. perspicillata presents opportunities for alternative reproductive tactics and sperm competition (Fasel et al., ), and the bachelor males are responsible for approximately 40% of offspring in a given season (Fasel et al., ). In the absence of direct paternity assessments, relative testicle size (independent of body size) is a reliable measure of male investment in spermatogenic activity and reproductive potential (Gomendio, Harcourt, & Roldán, ; Preston, Stevenson, Pemberton, Coltman, & Wilson, ; Schulte‐Hostedde & Millar, ), directly related to the reproductive component of fitness and patterns of sexual selection through sperm competition (Parker, ; Parker & Ball, ).…”

Social dominance, but not parasite load, affects sperm quality and sperm redox status in house sparrows

“…Such status-dependent investment, whereby males at the lower end of the social hierarchy (e.g. satellite or sneaker males) exhibit better sperm performance than dominant males, has been observed in captive and wild vertebrates (Stockley et al, 1994;Froman et al, 2002;Neff et al, 2003;Fitzpatrick et al, 2007;Fasel et al, 2016). Similarly, in house sparrows, which display a linear hierarchy, males at the top and males at the bottom of the hierarchy have been found to produce lower quality ejaculates than males in the middle of the hierarchy (Rojas Mora et al, 2017a).…”

No evidence of inbreeding depression in sperm performance traits in wild song sparrows

“…Under risk of sperm competition, males might trade-off resources between traits that reduce sperm competition (e.g., increased mate guarding) versus traits that increase fertilization success (e.g., increased sperm quality, Kelly & Jennions, 2011;Schradin, Eder, & Müller, 2012). Such statusdependent investment, where non-mate-guarding floater, satellite, or sneaker males exhibit better sperm performance than dominant mateguarding males, has been observed in captive and wild vertebrates (Fasel et al, 2016;Fitzpatrick, Desjardins, Milligan, Montgomerie, & Balshine, 2007;Froman, Pizzari, Feltmann, Castillo-Juarez, & Birkhead, 2002;Neff, Fu, & Gross, 2003;Stockley, Searle, Macdonald, & Jones, 1994). Therefore, effects of individual social status should also be estimated when quantifying sperm performance in systems with statedependent plasticity in tactics.…”