The Role of Parental Age Effects on the Evolution of Aging

Abstract

Many studies have found that older parents have shorter-lived offspring. However, the evolutionary significance of these findings is poorly understood. We carried out large-scale demographic experiments to examine the direct effect of maternal age and paternal age on offspring aging in inbred and outbred strains of the fruit fly Drosophila melanogaster. We found that the age of mothers and, to a lesser extent, the age of fathers can have a large influence on both offspring longevity and the shape of the age-specific mortality trajectory. In two independent experiments we found that older mothers generally produced shorter-lived offspring, although the exact effect of maternal age on offspring longevity differed among strains. These results suggest that maternal age effects on progeny aging may influence the evolution of aging.The youngest mother, on the average, had the longestlived offspring. -Alexander Graham Bell (1918)

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

“…Whether due to maternal effects or defects in their germ line DNA, aging females of many animal species produce poor quality offspring (e.g., Priest et al 2002;Saino et al 2002;Descamps et al 2008), and in humans at least, advanced female age can enhance the deleterious effects of advanced male age on fertility (Kühnert and Nieschlag 2004) and on genetic quality of progeny (Fisch et al 2003). These interaction effects raise the possibility that old female birds, in particular, might maintain their fertility or offspring quality by avoiding pairing with old males with senescent sperm traits and germ cells.…”

Evolution of maternal effect senescence

“…Similar studies of age-specific maternal IGEs are lacking from the literature. However, as discussed above, there is good evidence to suggest maternal effects and IGEs are widespread and important in nature (29)(30)(31) and that maternal age is a powerful predictor of a range of offspring traits (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19). Given that age-specific maternal effects have been detected and estimated in a wild mammal system (59), the estimation of age-specific IGEs in other experimental and observational studies should be feasible.…”

“…Some have proposed that offspring quality should be taken into account in determining how we define aging (14). Others have more explicitly called for the development of new age-structured evolutionary models of aging that explicitly incorporate parental effects (15). The age-structured model presented here accomplishes these goals by explicitly determining the relationship between maternal effect senescence and the actuarial and reproductive senescence that constitutes the classical theory of senescence.…”

“…Amid the many studies of senescing traits, a clear pattern is emerging that relates maternal age to the health, fitness, and lifespan of their progeny across widely diverse taxa including humans (8), birds (9, 10), mammals (11,12), Drosophila species (13)(14)(15) and other arthropods (16)(17)(18), and plants (19). Although observations suggest that maternal effect senescence may not proceed at the same rate as fertility senescence (12,(20)(21)(22)(23)(24), there is no evolutionary theory yet capable of explaining maternal effect senescence or its distinction from fertility senescence.…”

Mutation Patterns Due to Converging Mitochondrial Replication and Transcription Increase Lifespan, and Cause Growth Rate-Longevity Tradeoffs

“…However, the longevity-growth rate tradeoff hypothesis suggests the possibility that the causal interpretation of the association of D ssh r->D ssh t convergence with maximal lifespan is opposite to the direction assumed. This is because offspring fitness decreases with parental age (Kern, 2001;Priest et al, 2002;Moore & Harris, 2003;Moore & Sharma, 2005), putatively due to ontogenetic cumulation of mutations, especially in mothers (McIntyre & Gooding, 1998;Hercus & Hoffmann, 2000), which are inherited by offspring. This issue is particularly relevant to mitochondria.…”