Longevity: Reproduction

views updated

LONGEVITY: REPRODUCTION

Reproduction is one of the most important influences on longevity. This influence is both direct, within the life of single individuals, and indirect, through the impact of reproduction on the evolution of longevity, mortality, and related characters. Both effects are considered here.

The direct cost of reproduction

Reproduction generally reduces survival, more reproduction shortening life span, less reproduction increasing life span. This effect is not absolutely universal, but it is one of the better established patterns in the biology of aging.

The most extreme experiments that demonstrate the cost of reproduction for longevity involve castration. In annual plants, such as soybean, stripping the plant of flowers often prolongs life by months. In animals that reproduce just once, castration before reproduction can increase longevity by years. In Pacific salmon, it was possible to extend the life of a castrated fish by more than a decade. In marsupial mice of the genus Antechinus, castrated males live months longer than intact males. There is some evidence that castrating institutionalized human males increases their life span. The records of the British aristocracy also suggest that females who have fewer children also live longer, although much of this data antedates modern medicine. All these examples indicate that reproduction affects longevity within the lives of single organisms, but they do not indicate how reliable the effect is.

Classic experiments using the fruit fly Drosophila subobscura illustrate the consistency with which reproduction reduces survival. Normal, mated, fruit fly females lay many eggs and die fairly soon, most between five to seven weeks of adulthood. Three kinds of females that lay fewer eggs all live longer on average: (1) flies that lack ovaries because of a genetic mutation, (2) flies that are denied access to males, and (3) flies that have been sterilized but are allowed to mate. The generality of the effect on longevity of reproduction is revealed by the fact that three such different manipulations of reproduction all increased longevity.

Indirect effects of reproduction on longevity

Reproduction also affects longevity by a different type of biological mechanism, through its effects on the evolution of aging. These evolutionary effects are twofold: reproduction determines the force of natural selection; and reproduction may be genetically connected to survival by an evolutionary trade-off. These effects will be discussed in order.

Reproduction and the force of natural selection. The evolutionary theory of aging is based on the force of natural selection. The force of natural selection is a function that indicates the impact on fitness of a change to age-specific survival. When this force is strong, natural selection is expected to favor genetic changes that improve survival. When it is weak, natural selection is expected to allow the evolution of poor survival. The key determinant of the strength of the force of natural selection is reproduction. Before reproduction occurs in a population, the force of natural selection acts on survival with full force. For example, a dominant allele that kills its carrier before adulthood will eliminate itself from a population in one generation. This is a case where the force of natural selection is very strong. When a population has completely finished reproduction, the force of natural selection acting on survival is zero. In this case, an allele that kills only after this age is not affected by natural selection, because natural selection has ceased. Between these two ages, the force of natural selection steadily falls. Evidently, the key factor determining the evolution of survival, and thus longevity, is the timing of reproduction.

This abstract theory can be made more concrete by considering experiments in which the timing of reproduction is deliberately manipulated for many generations, making the evolutionary impact of reproduction on survival obvious. These experiments have been performed a number of times in fruit flies. When early reproduction is prevented by discarding eggs laid by younger females, and sired by younger males, over many generations, increased longevity evolves. The experimenter does not need to impose any additional manipulation. Evolution automatically reshapes longevity, because the shift in reproduction to later ages increases the force of natural selection at later ages. In this sense, the pattern of reproduction is the ultimate determinant of aging.

Similar experiments have been performed with mice. Though the results are not as striking, they also show that delayed reproduction leads to the evolution of increased longevity.

Evolution and the cost of reproduction. In some cases, the evolution of aging depends on the cost of reproduction. If a single genetic change alters both early fertility and later survival, but does so in opposite directions, then the evolution of reproduction may affect the evolution of longevity in a different way. The most important case is when a genetic change increases early reproduction at the expense of later survival. This is expected to occur whenever genetic effects emulate the effects of a direct cost of reproduction, described above. The force of natural selection is strong at early ages, but weak at later ages, so any early beneficial effect should be more important than a later bad effect. This, then, should lead to the evolution of decreased longevity as a side-effect of selection for increased early reproduction. Metaphorically, natural selection is choosing early reproduction over later survival.

There is a reasonable amount of evidence that supports this evolutionary cost of reproduction for longevity. Fruit flies that have evolved increased longevity in the laboratory tend to have decreased early fertility, though this effect depends on environment and inbreeding. In nematodes of the genus Caenorhabditis, there has been some inconsistency in the experimental data, but recent experiments seem to show that there is an early physiological cost associated with increased longevity, a cost that may be related to reproduction. It is not expected, however, that there will always be an evolutionary trade-off between reproduction and longevity. In many cases, there may be no such trade-off. But whenever there is such a trade-off, the evolution of longevity will be bound up with the evolution of reproduction.

Michael R. Rose

See also Endocrine System; Evolution of Aging; Longevity: Selection.