Evidence that fertility trades off with early offspring fitness as males age

Sheri L. Johnson, Sylvia Zellhuber-McMillan, Joanne Gillum, Jessica Dunleavy, Jonathan P. Evans, Shinichi Nakagawa, Neil J. Gemmell

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Models of ageing predict that sperm function and fertility should decline with age as sperm are exposed to free radical damage and mutation accumulation. However, theory also suggests that mating with older males should be beneficial for females because survival to old age is a demonstration of a male’s high genetic and/or phenotypic quality. Consequently, declines in sperm fitness may be offset by indirect fitness benefits exhibited in offspring. While numerous studies have investigated age-based declines in male fertility, none has taken the integrated approach of studying age-based effects on both male fertility and offspring fitness. Here, using a cohort-based longitudinal study of zebrafish (Danio rerio), we report a decline in male mating success and fertility with male age but also compensating indirect benefits. Using in vitro fertilization, we show that offspring from older males exhibit superior early survival compared to those from their youngest counterparts. These findings suggest that the high offspring fitness observed for the subset of males that survive to an old age (approx. 51% in this study) may represent compensating benefits for declining fertility with age, thus challenging widely held views about the fitness costs of mating with older males.

Original languageEnglish
Article number20172174
Number of pages9
JournalProceedings of the Royal Society B: Biological Sciences
Volume285
Issue number1871
DOIs
Publication statusPublished - 31 Jan 2018
Externally publishedYes

Keywords

  • Danio rerio
  • Mating success
  • Sperm quality
  • Zebrafish

Cite this

Johnson, S. L., Zellhuber-McMillan, S., Gillum, J., Dunleavy, J., Evans, J. P., Nakagawa, S., & Gemmell, N. J. (2018). Evidence that fertility trades off with early offspring fitness as males age. Proceedings of the Royal Society B: Biological Sciences, 285(1871), [20172174]. https://doi.org/10.1098/rspb.2017.2174
Johnson, Sheri L. ; Zellhuber-McMillan, Sylvia ; Gillum, Joanne ; Dunleavy, Jessica ; Evans, Jonathan P. ; Nakagawa, Shinichi ; Gemmell, Neil J. / Evidence that fertility trades off with early offspring fitness as males age. In: Proceedings of the Royal Society B: Biological Sciences. 2018 ; Vol. 285, No. 1871.
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Johnson, SL, Zellhuber-McMillan, S, Gillum, J, Dunleavy, J, Evans, JP, Nakagawa, S & Gemmell, NJ 2018, 'Evidence that fertility trades off with early offspring fitness as males age', Proceedings of the Royal Society B: Biological Sciences, vol. 285, no. 1871, 20172174. https://doi.org/10.1098/rspb.2017.2174

Evidence that fertility trades off with early offspring fitness as males age. / Johnson, Sheri L.; Zellhuber-McMillan, Sylvia; Gillum, Joanne; Dunleavy, Jessica; Evans, Jonathan P.; Nakagawa, Shinichi; Gemmell, Neil J.

In: Proceedings of the Royal Society B: Biological Sciences, Vol. 285, No. 1871, 20172174, 31.01.2018.

Research output: Contribution to journalArticleResearchpeer-review

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