Quantitative genetics of age at reproduction in wild swans: Support for antagonistic pleiotropy models of senescence

Abstract

Why do individuals stop reproducing after a certain age, and how is this age determined? The antagonistic pleiotropy theory for the evolution of senescence predicts that increased early-life performance should be accompanied by earlier (or faster) senescence. Hence, an individual that has started to breed early should also lose its reproductive capacities early. We investigate here the relationship between age at first reproduction (AFR) and age at last reproduction (ALR) in a free-ranging mute swan (Cygnus olor) population monitored for 36 years. Using multivariate analyses on the longitudinal data, we show that both traits are strongly selected in opposite directions. Analysis of the phenotypic covariance between these characters shows that individuals vary in their inherent quality, such that some individuals have earlier AFR and later ALR than expected. Quantitative genetic pedigree analyses show that both traits possess additive genetic variance but also that AFR and ALR are positively genetically correlated. Hence, although both traits display heritable variation and are under opposing directional selection, their evolution is constrained by a strong evolutionary tradeoff. These results are consistent with the theory that increased early-life performance comes with faster senescence because of genetic tradeoffs.evolutionary tradeoff ͉ genetic correlation ͉ heritability ͉ mute swan ͉ aging T he decline in reproductive performance in organisms of old ages is one component of the evolutionary paradox of aging (1). Aging, or senescence, is the drop in survival and͞or fertility probabilities in old individuals. It is often witnessed in laboratory conditions (e.g., see refs. 2-4) and, more rarely, in nature (5-7). For evolutionary biologists, the evolution of decreased performance and increased mortality with age, which should at first sight be counterselected, is a puzzle. The solution to this puzzle lies in the weaker force of natural selection for older individuals in age-structured populations (8), which allows for the evolution of aging.Two main genetic processes have been proposed as causal mechanisms underlying the evolution of senescence. The first assumes an accumulation of late-acting deleterious mutations as a result of weak selection late in life (referred to as the mutation accumulation theory) (1, 8). Alternatively, aging can be promoted by the active selection of alleles with late deleterious effects but beneficial effects early in life, when selection is strongest (9). This latter theory, known as the antagonistic pleiotropy (AP) theory of aging, can be considered an optimality theory (10) because the evolution of senescence is explained by fitness maximized by good performance early in life, at the expense of performance later. This type of pleiotropic effect is best illustrated in physiological or ecological tradeoffs such as that occurring between reproduction and survival. Indeed this theory has at times been called the ''tradeoff'' model (11). However, an important facet of the AP theory is ...

Age-specific reproduction in a long-lived species: the combined effects of senescence and individual quality

“…In fact, when we come to consider the improvement in performance with age measured on the population as a whole there is an effect due to differential survival of higher-quality individuals, as well as a within-individual age effect for birds of any given quality. This result is also consistent with earlier findings in this colony showing the phenotypic correlation between age at first breeding and ALR is less positive than the null expectation (Charmantier et al 2006c), meaning that higher-quality birds were able to breed both relatively early and relative late in their lives.…”

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Age structure changes and extraordinary lifespan in wild medfly populations

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