Genetic variance in reproductive timing contributes to trait evolvability

The additive genetic variance of a quantitative trait usually is interpreted as a measure of its evolvability, i.e., its capacity for adaptive evolution. However, in populations with overlapping generations, evolvability is also affected by the parental age at reproduction because genotypes that reproduce earlier evolve faster than genotypes with later reproduction. I show here that directional selection of a phenotypic trait inevitably links it with relative age at reproduction and thus developmental timing, whether or not age at reproduction affects reproductive success. In turn, the evolved genetic covariance between the selected trait and reproductive age accelerates the evolutionary response of the trait mean, unless counteracted by strong selection for late reproduction. Hence, not only the genetic variance of the trait but also the genetic variance in age at reproduction contributes to a trait's evolvability, even if the trait was initially unrelated to age at reproduction. I further show that stable generation time requires selection of intermediate strength for later reproduction and that episodes of strong selection tend to shorten average generation time. After a proof of principle by individual-based simulations, I present a formalization of this theory in a quantitative genetic framework, leading to a relatively simple extension of the breeder's equation. Finally, I discuss empirical evidence and implications for senescence and life history evolution.