Meta-analysis shows no consistent evidence for senescence in ejaculate traits across animals

Abstract

Male reproductive traits such as ejaculate size and quality, are expected to decline with advancing age due to senescence. It is however unclear whether this expectation is upheld across taxa. We perform a meta-analysis on 379 studies, to quantify the effects of advancing male age on ejaculate traits across 157 species of non-human animals. Contrary to predictions, we find no consistent pattern of age-dependent changes in ejaculate traits. This result partly reflects methodological limitations, such as studies sampling a low proportion of adult lifespan, or the inability of meta-analytical approaches to document non-linear ageing trajectories of ejaculate traits; which could potentially lead to an underestimation of senescence. Yet, we find taxon-specific differences in patterns of ejaculate senescence. For instance, older males produce less motile and slower sperm in ray-finned fishes, but larger ejaculates in insects, compared to younger males. Notably, lab rodents show senescence in most ejaculate traits measured. Our study challenges the notion of universal reproductive senescence, highlighting the need for controlled methodologies and a more nuanced understanding of reproductive senescence, cognisant of taxon-specific biology, experimental design, selection pressures, and life-history.

Fig. 1. No consistent evidence for senescence in ejaculate traits, irrespective of taxonomic class.

A Meta-analytical model of the overall effect of advancing male age on ejaculate traits. B Effect of advancing male age on ejaculate traits for each taxonomic class (note that animal classes with less than 25 effect sizes were grouped together in ‘Other’). The size of each data point represents the precision of the effect size (1/SE). The x-axis represents values of effect sizes as Fisher’s z-transformed correlation coefficient (Zr), while the y-axis shows the density distribution of effect sizes. The position of the overall effect is shown by the dark circle, with negative values depicting senescence in ejaculate traits and positive values showing improvement in ejaculate traits with advancing male age. Bold error bars (95% CI) show whether overall effect size is significantly different from zero (i.e. not overlapping zero), while light error bars show the 95% prediction interval (PI) of effect sizes, and black dot shows mean effect size. Sample sizes reported as: k = number of effect sizes (in brackets: number of studies). Source data is provided as a source data file.

Fig. 2. No consistent evidence for senescence in ejaculate traits when all taxa were considered, but some ejaculate traits improve with advancing age (in insects), while other traits decline (in lab rodents).

A Effect of advancing male age on individual ejaculate traits across all 157 species in the dataset. B Effect of advancing male age on individual ejaculate traits in the class- Insecta. C Effect of advancing male age on individual ejaculate traits for the two most over-represented species combined (lab rodents): Mus musculus and Rattus norvegicus. The size of each data point represents the precision of the effect size (1/SE). The x-axis represents values of effect sizes as Fisher’s z-transformed correlation coefficient (Zr), while the y-axis shows the density distribution of effect sizes. The position of the overall effect is shown by the dark circle, with negative values depicting senescence in ejaculate traits and positive values showing improvement in ejaculate traits with advancing male age. Sample sizes reported as: k = number of effect sizes (in brackets: number of studies). Bold error bars (95% CI) show whether overall effect size is significantly different from zero (i.e. not overlapping zero), while light error bars show the 95% PI of effect sizes, and black dot shows mean effect sizes. Note that error bars are not provided for traits with a number of effect sizes less than 3. Source data is provided as a source data file.

Fig. 3. Specific ejaculate traits and taxonomy interacted to affect the evidence for senescence.

Summary of results for how advancing male age affects different ejaculate traits across various taxa in our meta-analysis. “Chickens” refers to domestic chickens and red junglefowl combined. Species icons from PhyloPics, with artist credits and copyright: Kamil S. Jaron (CC0 1.0), Emma Moffett (CC0 1.0), T. Michael Keesey (PDM 1.0), Steven Traver (CC0 1.0), Georgios Lyras (CC0 1.0). Only traits with >3 effect sizes are included in the summary.

Fig. 4. Increasing the proportion of the maximum adult lifespan sampled increased the likelihood of finding senescence.

Effect of proportion of maximum adult lifespan sampled (x-axis) on the effect size i.e. Fisher’s z transformed r (y-axis) across the entire dataset (A), and broken down for domestic (B), laboratory (C), wild (D), and captive animals (E). The size of each data point represents the precision of the effect size (1/SE). The dark line with shaded bars represents the overall effect of lifespan sampled on effect sizes and its 95% CI, respectively, and the black line shows the mean regression line. Negative values depict senescence in ejaculate traits with advancing age, while positive values show improvement in ejaculate traits with advancing male age. Sample sizes reported as: k = number of effect sizes (in brackets: number of studies). Source data is provided as a source data file.