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.

Reproductive output of old polygynous males is limited by seminal fluid, not sperm number

“…We found that old males had higher numbers of sperm stored in their seminal vesicles than young males (also shown by Decanini et al, 2013; Kehl et al, 2013, 2015; Reinhardt et al, 2011). Sanghvi et al (2024) in a meta-analysis found a similar pattern across insects, and attribute this to experimental males typically being maintained as virgin, which can lead to longer periods of sperm accumulation in old than young males. Consistent with this, at low mating rates, old males often have larger ejaculates than young males, but at high mating rates this pattern is reversed (Aich et al, 2021; Bressac et al, 2009; Sepil et al, 2020).…”

“…Male reproductive senescence has been demonstrated across taxa, in studies that mate males with an individual female (reviewed in Monaghan and Metcalfe, 2019; Sanghvi et al, 2024). However, these studies are not informative about reproductive senescence in polygynous species (Bressac et al, 2008, 2009), where males are exposed to multiple partners and male reproductive output can be modulated by female order in a male’s mating sequence (Abe, 2019; Lewis, 2004; Macartney et al, 2020; Appendix 1).…”

“…Additionally, the pathways mediating male reproductive senescence can be diverse, and have been difficult to pinpoint. These include age-dependent declines in quality and quantity of sperm (Sanghvi et al, 2024) and seminal fluid (Fricke et al, 2023), changes in male behaviour and mating success (Dean et al, 2010; Hayes et al, 2013) and ejaculate allocation (Win et al, 2013). Furthermore, females might contribute to male reproductive senescence via preference for young males (Radwan, 2003; Vuarin et al, 2019).…”

“…Male reproductive senescence has been demonstrated across taxa, in studies that mate males with an individual female (reviewed in Monaghan and Metcalfe, 2019;Sanghvi et al, 2024).…”

“…Advancing age, often (Lemaitre and Gaillard, 2017; Monaghan et al, 2008), but not always (Jones et al, 2014; Sanghvi et al, 2024), leads to irreversible declines in fecundity and fertility (Vrtilek et al, 2023), a pattern known as reproductive senescence (Monaghan and Metcalfe, 2019). In males, reproductive senescence is primarily attributed to age-dependent deterioration in mating success (Amin et al, 2012; Rezaei et al, 2015), reduced sperm quality (Dean et al, 2010; Gasparini et al, 2019; Johnson et al, 2015; Vuarin et al, 2019), sperm quantity (Cornwallis et al, 2014; Sasson et al, 2012), and sperm performance (Aich et al, 2021; Gasparini et al, 2010).…”