Should females prefer old males?

Abstract

Whether females should prefer to mate with old males is controversial. Old males may sire offspring of low quality because of an aging germline, but their proven ability to reach an old age can also be an excellent indicator of superior genetic quality, especially in natural populations. These genetic effects are, however, hard to study in nature, because they are often confounded with direct benefits offered by old males to the female, such as experience and high territory quality. We, therefore, used naturally occurring extra‐pair young to disentangle different aspects of male age on female fitness in a natural population of collared flycatchers because any difference between within‐ and extra‐pair young within a nest should be caused by paternal genetic effects only. Based on 18 years of long‐term data, we found that females paired with older males as social partners experienced an overall reproductive advantage. However, offspring sired by old males were of lower quality as compared to their extra‐pair half‐siblings, whereas the opposite was found in nests attended by young males. These results imply a negative genetic effect of old paternal age, given that extra‐pair males are competitive middle‐age males. Thus, offspring may benefit from being sired by young males but raised by old males, to maximize both genetic and direct effects. Our results show that direct and genetic benefits from pairing with old males may act in opposing directions and that the quality of the germline may deteriorate before other signs of senescence become obvious.

Coevolution of longevity and female germline maintenance

“…Germline maintenance decisions can also depend on the overall condition of the individual and state-dependent allocation decisions between competing life-history demands (Berger et al, 2017; Maklakov & Immler, 2016; Monaghan & Metcalfe, 2019; Sharp & Agrawal, 2012), with implications for sexual selection theory and mate choice processes (Baur & Berger, 2020; Beck & Promislow, 2007; Koppik et al, 2023; Segami et al, 2021). Viewing germline maintenance through a resource acquisition and allocation lens (Jong & Noordwijk, 1992) suggests that optimal mate choice is contingent on not only choosers’ inferences of genetic quality in offspring based on the phenotype of their mating partner, but also of how this phenotype influences changes to the genetic quality of its gametes.…”

“…For example, in many polyandrous species, strong postcopulatory sexual selection (sperm competition) can favour compromised germline maintenance in males (Bartosch -Harlid et al, 2003; Baur & Berger, 2020; Blumenstiel, 2007; Koppik et al, 2023). This suggests that males that are most successful in reproductive competition may sometimes pass on the greatest load of mutations to their offspring, questioning why females should prefer them in the first place (Baur & Berger, 2020; Beck & Promislow, 2007; Segami et al, 2021)? Interestingly, however, optimality theory predicts that females my tailor care depending on the assessed state of male gametes (Servedio et al, 2019), with the result that a male’s mutation rate is not independent of his female mate and her potential compensation for his short-comings, which can complicate interpretations of both age- and sex-biases in mutation rate (Gao et al, 2019a).…”

Cancer Susceptibility as a Cost of Reproduction and Contributor to Life History Evolution

“…For many years, it was expected females of many species chose to mate with old rather than young males, because older males often provide better resources (e.g., territories, parental care) and/or pass good genes on to their offspring (Brooks and Kemp, 2001). However, these theoretical predictions are now thoroughly revisited in the light of recent studies demonstrating the under-estimated occurrence of male reproductive aging, as well as the detrimental consequences of this process on female fitness (Lemaître and Gaillard, 2017;Monaghan and Metcalfe, 2019;Monaghan et al, 2020;Segami et al, 2021). Empirical studies suggest that female preference toward young males could be a pervasive mating tactic in the living world (e.g., Verburgt et al, 2011;Vanpé et al, 2019).…”

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

“…senescence; Johnson and Gemmell, 2012). For example, the "good genes" hypothesis predicts that on average, old males may have better reproductive performance than young males, because older cohorts are purged of lower quality phenotypes due to viability selection (Brooks and Kemp, 2001;Segami et al, 2021). Finally, some studies report no net changes in ejaculate traits with advancing male age (e.g.…”