THEORIES OF BIOLOGICAL AGING: DISPOSABLE SOMA

Senescence and ageing are processes that affect all organisms and have been described as the diminishing probability of survival accompanied by a reduction of fecundity with increasing age (Partridge, 2001). The disposable soma theory was proposed in an attempt to ascribe an evolutionary framework to understand the existence of, and variations in, the universal process of ageing (Kirkwood, 1977; Kirkwood and Rose, 1991). It proposes that individuals should invest in the maintenance and repair of their soma in relation to their expected life history objectives. However, an individual’s expectation of future survival prospects, and the likelihood of reproduction, are not constant. Distinct species, and sometimes distinct individuals within a species, therefore need to sustain their somas for different lengths of time. The disposable soma theory of aging predicts that species and cohorts in a population expecting, on average, to have high survival and low reproductive rates should invest more heavily in protecting their somas than species and populations that expect a short lifespan and to reproduce rapidly. When animals are released from natural selection, differences in somatic repair and maintenance manifest themselves in interspecific and interpopulation differences in aging rate and lifespan.

Support for the idea that the predation rate on a given population affects that population’s life-history strategy, including the evolution of altered life span, comes from studies of wild guppies. Such evolution in early life-history stategy occurs very quickly in response to mortality rate changes (Reznick, Buckwalter, et al.). Guppy populations that suffer high predation rates are smaller, grow faster, produce young at an earlier age, and allocate more resources to reproduction than those found in low-predation environments (Reznick, Buckwalter, et al.; Reznick, Butler, et al.). In has also been suggested that one reason why birds and bats live longer than ground-dwelling animals of similar size is that, through flight, they have been released from much of the predation pressure experienced by ground animals. (Austad and Fischer; Ricklefs). One study that tested some of the ideas behind the disposable soma theory was carried out on two distinct U.S. populations of Virginia opossums (Austad). One population was found on Sapelo Island, Georgia, and had no mammalian predators; the other population, found on the Georgia mainland, was predated by pumas, foxes, and bobcats. When life-history parameters were measured for both groups, it was found that the island population produced fewer pups per litter than the mainland group and generally survived to a second reproductive season, when they bred again. The island group had, on average, a 25 percent greater average life span and a 50 percent longer maximum life span than the mainland group.

It is important to note that because the disposable soma theory is an evolutionary theory, the linkage between survival, reproduction, and aging is ultimate rather than proximate. Hence, if an individual animal forgoes breeding, it is not expected to achieve immortality, because it has been selected only to protect its soma for the duration that the average individual within that species is expected to survive. However, forgoing reproduction may have a positive impact on aging and longevity (Hamilton and Mestler; Westendorp and Kirkwood). This is not because of the ultimate evolutionary connection between survival expectancy, reproduction, somatic protection, and longevity anticipated by the disposable soma theory, but rather because of an immediate, proximate trade-off between somatic protection and reproduction, possibly mediated via energy allocation strategies. The disposable soma theory suggests that there are two ultimate reasons why individuals might vary in the extent of soma protection.The first is that increases in adult expectation of mortality should lead to decreased protection. If the animal does not expect to live as long, it has less need to protect itself. The second is that increases in the expected rate of reproduction should lead to decreases in somatic protection, as individuals anticipate the trade-off in energy allocation.

The disposable soma theory does not postulate a particular mechanism underpinning somatic defense and therefore is compatible with various mechanistic theories, such as the free radical theory of aging (Harman). In particular, species that have the lowest levels of extrinsic mortality and low reproduction also have the highest rates of resistance to oxidative stress (Ku and Sohal; Barja, Cadenas,. . .Perez-Campo, 1994; Barja, Cadenas,. . .Lopez-Torres, 1994). Further support for this association comes from the opossums mentioned above, where the Sapelo Island population exhibited a reduced rate of age-associated damage in its collagenous tissues compared with the mainland opossums (Austad). DNA repair is lower in rodents than in primates (Cortopassi and Wang), and the somatic cells of mice are far more susceptible to oxidative stress induced by chemical stressors such as paraquat and hydrogen peroxide than are longer-lived mammals (Kapahi et al.). The renal epithelial cells of relatively long-lived birds also are more resistant to both chemical and radioactive insult than those of mice (Ogburn et al.).

Overall, the disposable soma theory provides a useful evolutionary framework for understanding the aging process. There is a considerable body of correlative evidence supporting the theory but strong experimental tests are still lacking.

Colin Selman John R. Speakman

BIBLIOGRAPHY

Austad, S. N., and Fischer, K. E. ‘‘Mammalian Ageing, Metabolism, and Ecology: Evidence from the Bats and Marsupials.’’ Journal of Gerontology 46 (1991): 47–53.

Austad, S. N. ‘‘Retarded Senescence in an Insular Population of Virginia Opossums (Didelphis virginiana ).’’ Journal of Zoology 229 (1993): 695–708.

Austad, S. N. Why We Age. New York: John Wiley and Sons, 1997.

Barja, G.; Cadenas, S.; Rojas, C.; Lopez-Torres, M.; and Perez-Campo, R. ‘‘A Decrease of Free Radical Production Near Critical Targets as a Cause of Maximum Longevity in Animals.’’ Comparative Biochemistry and Physiology 108B (1994): 501–512.

Barja, G.; Cadenas, S.; Rojas, C.; Perez-Campo, R.; and Lopez-Torres, M. ‘‘Low Mitochondrial Free Radical Production Per Unit O₂ Consumption Can Explain the Simultaneous Presence of High Longevity and High Aerobic Metabolic Rate in Birds.’’ Free Radical Research 21 (1994b): 317–328.

Cortopassi, G. A., and Wang, E. ‘‘There is Substantial Agreement among Interspecies Stimates of DNA Repair Activity.’’ Mechanisms of Ageing and Development 91 (1996): 211–218.

Hamilton, J. B., and Mestler, G. B. ‘‘Mortality and Survival: Comparison of Eunuches with Intact Men and Woman in a Mentally Retarded Population.’’ Journal of Gerontology 24 (1969): 395–411.

Harman, D. ‘‘Aging: A Theory Based on Free Radical and Radiation Chemistry.’’ Journal of Gerontology 11 (1956): 298–300.

Kapahi, P.; Boulton, M. E.; and Kirkwood, T. B. L. ‘‘Positive Correlations between Mammalian Lifespans and Cellular Resistance to Stress.’’ Free Radical Biology and Medicine 26 (1999): 495–500.

Kirkwood, T. B. L. ‘‘Evolution of Aging.’’ Nature 270 (1977): 301–304.

Kirkwood, T. B. L. Time of our Lives: The Science of Human Ageing. London: Weidenfeld and Nicolson, 1999.

Kirkwood, T. B. L., and Rose, M. R. ‘‘Evolution of Senescence: Late Survival Sacrificed for Reproduction.’’ Philosophical Transactions of the Royal Society of London B332 (1991): 15–24.

Ku, H. H., and Sohal, R. S. ‘‘Comparison of Mitochondrial Pro-oxidant Generation and Anti-oxidant Defenses between Rat and Pigeon: Possible Basis of Variation in Longevity and Metabolic Potential.’’ Mechanisms of Aging and Development 72 (1993): 67–76.

Ogburn, C. E.; Austad, S. N.; Holmes, D. J.; Kiklevich, J. V.; Gollahon, K.; Rabinovitch, P. S.; and Martin, G. M. ‘‘Cultured Renal Epithelial Cells from Birds and Mice: Enhanced Resistance of Avian Cells to Oxidative Stress and DNA Damage.’’ Journal of Gerontology 53 (1998): B287–B292.

Partridge, L. ‘‘Evolutionary Theories of Ageing Applied to Long-lived Organisms.’’ Experimental Gerontology 36 (2001): 641–650.

Reznick, D.; Buckwalter, G.; Groff, J.; and Elder, D. ‘‘The Evolution of Senescence in Natural Populations of Guppies (Poecilia reticulata ): A Comparative Approach.’’ Experimental Gerontology 36 (2001): 791–812.

Reznick, D.; Butler, M. J.; and Rodd, H. ‘‘Life-History Evolution in Guppies. VII. The Comparative Ecology of High- and Low-Predation Environments.’’ American Naturalist 157 (2001): 126–140.

Ricklefs, R. E. ‘‘Intrinsic Aging-Related Mortality in Birds.’’ Journal of Avian Biology 31 (2000): 103–111.

Westendorp, R. G. J., and Kirkwood, T. B. L. ‘‘Human Longevity at the Cost of Reproductive Success.’’ Nature 396 (1998): 743–746.