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Longevity: Reproduction - Indirect Effects Of Reproduction On Longevity

age aging physiological genetic selection natural evolution force

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

BIBLIOGRAPHY

FINCH, C. E. Longevity, Senescence, and the Genome. Chicago: University of Chicago Press, 1990.

ROSE, M. R. Evolutionary Biology of Aging. New York: Oxford University Press, 1991.

ROSE, M. R., and BRADLEY, T. J. "Evolutionary Physiology of the Cost of Reproduction." OIKOS 83 (1998): 443–451.

WALKER, D. W.; MCCOLL, G.; JENKINS, N. L.; HARRIS, J.; and LITHGOW, G. J. "Evolution of Lifespan in C. elegans." Nature 405 (2000): 296–297.

WESTENDORP, R. G. J., and KIRKWOOD, T. B. L. "Human Longevity at the Cost of Reproductive Success." Nature 396 (1998): 743–746.

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