Good genes and old age: Do old mates provide superior genes?

Abstract

It has been suggested that female preference for older mates in species without parental care has evolved in response to an alleged higher genetic quality of older individuals. This is based on the widespread assumption that viability selection produces older individuals that are genetically superior to younger individuals. In contrast, we propose that the oldest individuals rarely are genetically superior. Quantitative genetic models of life history evolution indicate that young to intermediately aged individuals are likely to possess the highest breeding values of fitness. This conclusion is based on four arguments: 1) Viability selection on older individuals may decrease or at least not substantially increase breeding values of fitness, because there may exist negative genetic correlations between late-age and early-age life history parameters, 2) Fertility selection is likely to raise the fitness of gametes produced by young individuals more than those produced by old individuals, because the covariance between fertility and fitness often decreases with age, 3) The history of selection on their parents makes younger individuals more fit than older individuals, 4) Germ-line mutations, which are generally deleterious, significantly decrease the breeding value of fitness of an individual throughout its lifespan, especially in males. Therefore, females that mate with the oldest males in a population are doing so for reasons other than to obtain offspring of high genetic quality.

Interactive effects of male and female age on extra-pair paternity in a socially monogamous seabird

“…There is some evidence that genes of older males are preferred: old males are more likely to gain extra-pair paternity (EPP) at other nests (Cleasby and Nakagawa 2012; but see Brooks and Kemp 2001), EP sires tend to be older than the males they cuckolded (Akçay and Roughgarden 2007), and older males lose paternity to EP sires less often than younger males (Møller and Ninni 1998). However, the evidence for this preference is mixed (Brooks and Kemp 2001;Cleasby and Nakagawa 2012), and it is possible that inconsistent patterns have arisen through females sometimes preferring middle-aged males and due to fieldworkers almost universally failing to distinguish between middle-aged and old males (Hansen and Price 1995;Jones et al 2000;Radwan 2003). Although senescent individuals have undoubtedly been included in analyses of female choice in wild avian populations, most have probably contrasted young and middle-aged males and, consequently, could not have revealed effects of senescence.…”

“…However, there are also theoretical grounds for expecting older males to provide better genes when differential survival of males generates a correlation between age and quality (Manning 1985;Kokko 1998;Brooks and Kemp 2001) as well as counterarguments based on life history considerations holding that older males are likely to be genetically inferior (Hansen and Price 1995). When choosing mates, females should theoretically take into account not only the decreased fertility and genetic quality that may come with germ line senescence but also the change in genetic quality that may be associated with greater male age (Johnson and Gemmell 2012).…”

The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle

“…Such models argue that females use age as a reliable signal of male quality and that, by mating with older males, they gain indirect benefits through the production of higher-quality offspring. While viability indicator models have gained empirical support (see Brooks & Kemp (2001) for a recent review), direct trade-offs between fitness components and age-specific differences in survival may reduce the fertility of older males and instead promote the evolution of female preference for young and intermediate-age males (Hansen & Price 1995Kokko 1997;Beck & Powell 2000;Beck et al 2002).…”

Male field cricket song reflects age, allowing females to prefer young males

“…The 'good genes' model of sexual selection (Zahavi 1975) predicts that if the genetic characteristics required to survive to an old age in the current environment are heritable, then females should prefer older males as they have demonstrated their viability (Trivers 1972;Halliday 1978Halliday , 1983 and are likely to carry fewer deleterious alleles (Manning 1985). Modelling approaches attempting to explain the evolution of female preference for males (Hansen & Price 1995;Kokko & Lindström 1996;Kokko 1998;Beck & Powell 2000;Beck et al 2002;Beck & Promislow 2007), as well as empirical studies (reviewed in Brooks & Kemp 2001), have demonstrated different outcomes: female preference may evolve for young, intermediate-aged or old males. It is therefore no longer universally accepted that older males always provide good genes.…”