The evolutionary advantages of dying young: Epidemiological implications of longevity in metapopulations

Here we show that pathogen-mediated selection can influence the evolution of host longevity. Greater longevity can impair the fitness of host organisms subject to pathogen attack, by reducing the mortality rate of infected hosts and thus creating a larger and more persistent reservoir of disease, from which infection can spread to the healthy population. Where longer-lived and shorter-lived hosts can infect one another (and thus all share the same risk of infection), selection will favor longer-lived individuals, to the detriment of the host population as a whole. But in metapopulations, selection can favor shorter-lived hosts that are otherwise identical to their longer-lived competitors, because the populations in which they occur will have lower incidence of disease. Under some conditions, shorter-lived hosts can even invade metapopulations of longer-lived hosts, displacing them and driving them to extinction. Our results support three general propositions. First, an organism's life-history traits, and not just its resistance genes, can affect its risk of pathogen attack. Second, pathogen-mediated selection may therefore influence the evolution of host life-history traits that are unrelated to resistance, per se. Third, the magnitude-and even the direction-of selection on host longevity can depend on the structure of the host population.