Aging has the hallmarks of an evolved adaptation. It is controlled by genes that have been conserved over vast evolutionary distances, and most organisms are able to forestall aging in the most challenging of environments. But fundamental theoretical considerations imply that there can be no direct selection for aging. Senescence reduces individual fitness, and any group benefits are weak and widely dispersed over non-relatives. We offer a resolution to this paradox, suggesting a general mechanism by which senescence might have evolved as an adaptation. The proposed benefit is that senescence protects against infectious epidemics by controlling population density and increasing diversity of the host population. This mechanism is, in fact, already well-accepted in another context: it is the Red Queen Hypothesis for the evolution of sex. We illustrate the hypothesis using a spatially explicit agent-based model in which disease transmission is sensitive to population density as well as homogeneity. We find that individual senescence provides crucial population-level advantages, helping to control both these risk factors. Strong population-level advantages to individual senescence can overcome the within-population disadvantage of senescence. We conclude that frequent local extinctions provide a mechanism by which senescence may be selected as a population-level adaptation in its own right, without assuming pleiotropic benefits to the individual. © 2009 Elsevier Ltd. All rights reserved.
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