Timeless or tainted? The effects of male ageing on seminal fluid

Abstract

Reproductive ageing can occur due to the deterioration of both the soma and germline. In males, it has mostly been studied with respect to age-related changes in sperm. However, the somatic component of the ejaculate, seminal fluid, is also essential for maintaining reproductive function. Whilst we know that seminal fluid proteins (SFPs) are required for male reproductive success across diverse taxa, age-related changes in SFP quantity and composition are little understood. Additionally, only few studies have explored the reproductive ageing of the tissues that produce SFPs, and the resulting reproductive outcomes. Here we provide a systematic review of studies addressing how advancing male age affects the production and properties of seminal fluid, in particular SFPs and oxidative stress, highlighting many open questions and generating new hypotheses for further research. We additionally discuss how declines in function of different components of seminal fluid, such as SFPs and antioxidants, could contribute to age-related loss of reproductive ability. Overall, we find evidence that ageing results in increased oxidative stress in seminal fluid and a decrease in the abundance of various SFPs. These results suggest that seminal fluid contributes towards important age-related changes influencing male reproduction. Thus, it is essential to study this mostly ignored component of the ejaculate to understand male reproductive ageing, and its consequences for sexual selection and paternal age effects on offspring.

No general effects of advancing male age on ejaculates: a meta-analysis across the animal kingdom

“…First, while we found that increasing the proportion of lifespan sampled by a study yielded greater evidence for senescence (also shown by Fricke et al, 2023;Vrtilek et al, 2022), studies tended to sample a low proportion of maximum adult lifespan (median = ~25%, Supplementary Fig. 10).…”

“…sperm number, concentration, and ejaculate size. This increase could be associated with their mating status, as most studies (>75%) on insects in our meta-analysis kept males as virgin (see Fricke et al, 2023;Richardson and Zuk 2022, who show similar results in males and females, respectively). Low mating rates could result in old insects accumulating more sperm and producing larger ejaculates than young males, because many insects have continuous spermatogenesis throughout their lives Hiroyoshi et al, 2021;Malawey et al, 2019;Reinhardt et al, 2011).…”

“…Proportion lifespan sampled* A higher proportion of lifespan sampled will increase the probability of detecting reproductive senescence, as the onset of senescence usually occurs late in life (Gaillard and Lemaitre, 2020;Fricke et al, 2023, Jones et al, 2014Lemaitre et al, 2020;Peron et al, 2010).…”

“…Levels of antioxidants in seminal fluid (Mannucci, 2021) and abundance of seminal fluid proteins can change as males age , independent of changes in sperm. Thesse age-dependent changes in seminal fluid can impact sperm motility, sperm usage, sperm activation, sperm oxidative and DNA damage (Avila et al, 2011;Poiani, 2006), over and above the direct effects of male age on sperm (Fricke et al, 2023).…”

“…Given the diversity of approaches and heterogeneity in studies, a metaanalytical approach is essential to understand the general effects of advancing male age on ejaculate traits. Yet, no study has done this across non-human animals (see Johnson et al, 2015 for humans; Vrtilek et al, 2022 for a systematic review in fish; and Fricke et al, 2023 for effects of male age on seminal fluid).…”