Antagonistic pleiotropy, mortality source interactions, and the evolutionary theory of senescence

Most theoretical work on the evolution of senescence has assumed that all individuals within a population are equally susceptible to extrinsic sources of mortality. An influential qualitative prediction based on this assumption is Williams's hypothesis, which states that more rapid senescence is expected to evolve when the magnitude of such extrinsic mortality sources is increased. Much evidence suggests, however, that for many groups of organisms externally imposed mortality risk is a function of an organism's internal condition and hence susceptibility to such hazards. Here we use a model of antagonistic pleiotropy to investigate the consequences that such interactions (between environmental hazard and internal condition) can have for Williams's hypothesis. As with some previous theory examining noninteractive extrinsic mortality sources, we find that an increase in interactive extrinsic sources of mortality makes it less likely that an individual will survive from birth to any given age, weakening selection against physiological deterioration at all ages and thus favoring more rapid senescence. However, an increase in interactive mortality sources also typically strengthens selection against physiological deterioration at any age, given an individual has survived to that age, because it reduces the fitness of poor-condition individuals more than good-condition individuals. These opposing effects are not felt equally at all ages, with the latter predominating at early ages. The combined effects can therefore result in the novel prediction that an increase in interactive extrinsic mortality sources can select for slower senescent deterioration early in life but more rapid deterioration late in life.