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

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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 statement

In 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.

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Acknowledgments

We are thankful to the team of the Papiliorama for allowing us to work with their bat colony under excellent research conditions. We warmly thank Ophélie Gning for her assistance in conducting biochemical analyses and Felizia Koch, Alvaro Sobrino and Laura Panchione for their assistance in the social monitoring. We are also grateful to the world bat library (Geneva) for providing free literature on bat research. Finally, we thank Gerald Wilkinson (editor) and the anonymous reviewers, whose comments and suggestions helped us to improve this manuscript.

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Authors and Affiliations

  1. Institute of Ecology and Evolution, University of Bern, Bern, Switzerland

    Nicolas Jean Fasel, Ahana Aurora Fernandez & Heinz Richner

  2. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

    Nicolas Jean Fasel

  3. Department of Biology, University of Neuchâtel, Neuchâtel, Switzerland

    Charlotte Wesseling, Armelle Vallat, Gaétan Glauser & Fabrice Helfenstein

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  1. Nicolas Jean Fasel
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Correspondence to Nicolas Jean Fasel.

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This study was supported by the University of Bern and the Swiss National Science Foundation (grant no. 31003A_122566 to HR and grant no. PP00P3_139011 to FH). The veterinary office of the Canton Fribourg, after supervision of the Cantonal ethical committee, authorized the experimental set-up and the detention conditions (FR_2013_46). Laboratory analyses were performed blindly with respect to sample identity.

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Communicated by G. S. Wilkinson

Nicolas Jean Fasel and Charlotte Wesseling shared first authorship.

Fabrice Helfenstein and Heinz Richner shared last authorship.

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Fasel, N.J., Wesseling, C., Fernandez, A.A. et al. Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat). Behav Ecol Sociobiol 71, 11 (2017). https://doi.org/10.1007/s00265-016-2251-7

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