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. 2018 Jan 31;285(1871):20172174.
doi: 10.1098/rspb.2017.2174.

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

Sheri L Johnson  1   2   3 , Sylvia Zellhuber-McMillan  2 , Joanne Gillum  2 , Jessica Dunleavy  2 , Jonathan P Evans  4 , Shinichi Nakagawa  5   6 , Neil J Gemmell  2   3
Affiliations

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

Sheri L Johnson et al. Proc Biol Sci. .

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.

Keywords: Danio rerio; mating success; sperm quality; zebrafish.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1.
Figure 1.
Longitudinal study. Effects of age on male survival, mating success, fertility and offspring fitness in zebrafish males. (a) male survival, (b) mating success, (c) sperm production, (d) sperm concentration, (e) sperm swimming speed (VCL), (f) sperm motility, (g) offspring early development, (h) offspring hatching. Mean ± s.e. presented in all plots. Sample sizes: (a) n = 30, (b) n = 54, (c) n = 393, (d) n = 257, (e) n = 321, (f) n = 321, (g) n = 378, (h) n = 375. See electronic supplementary material, table S2 for exact numbers of males sampled at each sampling point.
Figure 2.
Figure 2.
Effects of age on offspring early survival for zebrafish males at 4 months (n = 10 males) and 31 months (n = 9 males). Survival assayed as the proportion of embryos surviving to 15 days post-fertilization. Boxplots represent medians, 25th and 75th percentiles and interquartile ranges, with raw data inset.
Figure 3.
Figure 3.
Cross-sectional study. Effects of age on male survival, mating success, fertility and offspring fitness in young (4-month-old) versus old (greater than 24-month-old) zebrafish males. (a) Sperm swimming speed (VCL), (b) sperm motility, (c) offspring early development and (d) offspring early survival. Sample sizes: (a) n = 182, (b) n = 182, (c) n = 147, (d) n = 39. See electronic supplementary material, table S3 for exact numbers of males sampled at each sampling point. Boxplots represent medians, 25th and 75th percentiles and interquartile ranges, with raw data inset.
See this image and copyright information in PMC

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