How Life History Shapes Optimal Patterns of Senescence: Implications from Individuals to Societies

One evolutionary view of aging, the disposable soma theory, suggests that an organism's rate of senescence depends on the amount of energy invested in somatic maintenance. Since organisms have limited energy to allocate among growth, maintenance, and reproduction, the optimal amount of energy to invest in maintenance is influenced by the probability of death from extrinsic causes and the effect of somatic investment on survival. In eusocial animals, the disposable soma theory can be used to explain colonies' energy investment in the longevity of workers, who act as the somatic elements of a superorganism. There have been few theoretical considerations of how changes in the costliness of worker maintenance or in the effect of individual life span on group fitness influence a colony's investment in worker longevity. We develop a decision theory model to evaluate how changing the marginal costs and benefits of longevity and extrinsic mortality influence optimal worker life span in a social insect colony. Our model predicts that higher extrinsic mortality favors shorter life span. However, increased life span is favored when marginal benefits are an increasing function of longevity. In honeybees, this explains how greater somatic investment is sometimes favored despite high mortality. Our approach expands the disposable soma theory to make quantitative predictions about the selective pressures shaping senescence in social systems.