Economics and the evolution of life histories.

B irth and death are subjects of perennial interest. They are shaped by both physiology and behavior, which are themselves shaped (presumably) by natural selection. Thus, it seems natural to suppose that evolutionary ideas would form the core of demography. This, however, is not the case. Students of birth and death are largely divided: social scientists call the subject demography, and evolutionists call it life history evolution. In this issue of PNAS, Ronald Lee (1) proposes a theory that may help heal this divide. Lee’s theory is about aging. Within evolutionary biology, discussion of this subject has been dominated for decades by two theories: mutation accumulation and antagonistic pleiotropy (2). The first of these holds that selection is less effective at removing harmful mutations that act in old age, so such mutations accumulate. The second holds that some mutations are beneficial in youth but harmful later on. Such mutations accumulate because selection is more responsive to early effects than to late ones. Kirkwood’s (3) ‘‘disposable soma’’ theory describes a mechanism that can plausibly generate antagonistic pleiotropy. Lee’s focus is on parental care and other transfers of resources between individuals of different ages. When a woman dies at, say, age 30, the death deprives her children of the care they would have received from her. Thus, a mutation that increases the mortality of 30-year-olds has harmful effects at several ages. This has the flavor of antagonistic pleiotropy, but the theory is broader in that it encompasses cases in which the early and late effects are both harmful or both helpful. The real value of the new theory, however, is in its success in wedding an economic model of exchange between individuals to the evolutionary theory of aging. Lee’s article addresses several important questions. The first of these has to do with the age profile of mortality during childhood. Among humans and many other species, death rates decline dramatically during the initial part of life (4, 5). This pattern is pronounced in some species but apparently absent in others (6). Why should this be? The first attempt at an answer was made 70 years ago by Fisher (7), who observed that an average 15-year-old will contribute more to future generations than will a newborn because the 15-year-old is less likely to die before reproducing. Thus, he argued, selection affects genes more strongly if they are expressed in 15-yearolds than if they are expressed in newborns. From this perspective, high newborn mortality results from the relatively weak selection acting on them. This argument seemed to fit the facts and held sway for 36 years, until Hamilton (8) found its f law in 1966. Fisher had been right to ask what contribution each age class makes to future generations. But what matters is the contribution of the age class as a whole, not the contribution per individual. Correcting