Abstract
Two evolutionary genetic models—mutation accumulation and antagonistic pleiotropy—have been proposed to explain the origin and maintenance of senescence. In this paper, we focus our attention on the mutation accu mulation model. We re-examine previous evidence for mutation accumulation in light of new information from large-scale demographic experiments. After discussing evidence for the predictions that have been put forth from models of mutation accumulation, we discuss two critical issues at length. First, we discuss the possibility that classical fruit fly stock maintenance regimes may give rise to spurious results in selection studies of aging. Second, we consider evidence for the assumptions underlying evolutionary models of aging. These models assume that mutations act additively on age-specific survival rate, that there exist mutations whose effects are confined to late age-classes, and that all mutations have equal effects. Recent empirical evidence suggests that each of these three assumptions is unlikely to be true. On the basis of these results, we do not conclude that mutation accumulation is no longer a valid explanation for the evolution of aging. Rather, we suggest that we now need to begin developing more biologically realistic genetic models for the evolution of aging.
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References
Abrams, P., 1991. The fitness costs of senescence: the evolutionary importance of events in early adult life. Evolutionary Ecology 5: 343–360.
Ashburner, M., 1989. Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Bell, G. & V. Koufopanou, 1985. The cost of reproduction. Oxford Surveys in Evolutionary Biology 3: 83–131.
Carey, J.R., P. Liedo, D. Orozco & J.W. Vaupel, 1992. Slowing of mortality rates at older ages in large medfly cohorts. Science 258: 457–461.
Charlesworth, B., 1990. Optimization models, quantitative genetics, and mutation. Evolution 44: 520–538.
Charlesworth, B., 1994. Evolution in Age-Structured Populations. Cambridge University Press, Cambridge.
Charlesworth, B. & K.A. Hughes, 1996. Age-specific inbreeding depression and components of genetic variance in relation to the evolution of senescence. Proc. Natl. Acad. Sci. USA. 93: 6140–6145.
Chippindale, A.K., D.T. Hoang, P.M. Service & M.R. Rose, 1994. The evolution of development in Drosophila melanogaster selected for postponed senescence. Evolution 48: 1880–1899.
Chippindale, A.K., A.M. Leroi, S.B. Kim & M.R. Rose, 1993. Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction. J. Evol. Biol. 6: 171–193.
Clark, A.G., 1987. Senescence and the genetic correlation hang-up. Amer. Natur. 129: 932–940.
Clark, A.G. & R.N. Guadalupe, 1995. Probing the evolution of senescence in Drosophila melanogaster with P-element tagging. Genetica 96: 225–234.
Clark, A.G. & L. Wang, 1994. Comparative evolutionary analysis of metabolism in nine Drosophila species. Evolution 48: 1230–1243.
Comfort, A., 1979. The Biology of Senescence, 3rd ed. Churchill Livingstone, Edinburgh.
Comstock, R.E. & H.F. Robinson, 1952. Estimation of average dom inance of genes, pp. 494–516 in Heterosis, edited by J. W. Gowen. Iowa State College Press, Ames, Iowa.
Curtsinger, J.W., 1995. Density, mortality, and the narrow view. Genetica 96: 187–189.
Curtsinger, J.W., H.H. Fukui, A.A. Khazaeli, A. Kirscher, S.D. Pletcher, D.E.L. Promislow & M. Tatar, 1995. Genetic variation and aging. Annual Review of Genetics 29: 553–575.
Curtsinger, J.W., H.H. Fukui, D.R. Townsend & J.W. Vaupel, 1992. Demography of genotypes: Failure of the limited life-span para digm in Drosophila melanogaster. Science 258: 461–463.
Dobzhansky, T., R.C. Lewontin & O. Pavlovsky, 1964. The capacity for increase in chromosomally polymorphic and monomorphic populations of Drosophila pseudoobscura. Heredity 19: 597–614.
Ebert, D., L. Yampolsky & A.J. Van Noordwijk, 1993. Genetics of life-history in Daphnia magna. 2. Phenotypic plasticity. Heredity 70: 344–352.
Engström, G., L.-E. Liljedahl, M. Rasmuson & T. Björklund, 1989. Expression of genetic and environmental variation during ageing. I. Estimation of variance components for number of adult offspring in Drosophila melanogaster. Theoretical and Applied Genetics 77: 119–122.
Falconer, D.S. & T.F.C. Mackay, 1996. Introduction to Quantitative Genetics. Longman Group Limited, Essex.
Finch, C.E., M.C. Pike & M. Witten, 1990. Slow mortality rate accelerations during aging in some animals approximate that of humans. Science 249: 902–906.
Fukui, H.H., L. Ackert & J.W. Curtsinger, 1996. Deceleration of age-specific mortality rates in chromosomal homozygotes and heterozygotes ofDrosophila melanogaster. Experimental Geron tology 31: 517–531.
Graves, J.L., 1995. Population density effects on longevity revisited: A note in response to ‘Density and age-specific mortality’ by J.W. Curtsinger. Genetica 96: 183–186.
Hamilton, W.D., 1966. The moulding of senescence by natural selection. J. Theor. Biol. 12: 12–45.
Houle, D., K.A. Hughes, D.K. Hoffmaster, J. Ihara, S. Assimacopoulos, D. Canada & B. Charlesworth, 1994. The effects of sponta neous mutation on quantitative traits. I. Variances and covariances of life history traits. Genetics 138: 773–785.
Hughes, K.A., 1995. The evolutionary genetics of male life-history characters in Drosophila melanogaster. Evolution 49: 521–537.
Hughes, K.A. & B. Charlesworth, 1994. A genetic analysis of senes cence in Drosophila. Nature 367: 64–66.
Keightley, P.D., 1996. Nature of deleterious mutation load in Drosophila. Genetics 144: 1993–1999.
Kondrashov, A.S., 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336: 435–440.
Kosuda, K., 1985. The aging effect on male mating activity in Drosophila melanogaster. Behav. Genet. 15: 297–303.
Luckinbill, L.S., R. Arking, M.J. Clare, W.J. Cirocco & S.A. Buck, 1984. Selection for delayed senescence in Drosophila melanogaster. Evolution 38: 996–1003.
Lynch, M., J. Conery & R. Burger, 1995. Mutation accumulation and the extinction of small populations. Amer. Natur. 146: 489–518.
Mackay, T.F.C., J.D. Fry, R.F. Lyman & S.V. Nuzhdin, 1994. Polygenic mutation in Drosophila melanogaster — Estimates from response to selection in inbred lines. Genetics 136: 937–951.
Medawar, P.B., 1952. An Unsolved Problem in Biology. H. K. Lewis, London.
Mueller, L.D., 1987. Evolution of accelerated senescence in labora tory populations of Drosophila. Proc. Natl. Acad. Sci. USA. 84: 1974–1977.
Mueller, L.D. & F.J. Ayala, 1981. Trade-off between r-selection andK K-selection in Drosophila populations. Proc. Natl. Acad. Sci. USA. 78: 1303–1305.
Mukai, T., H.E. Schaffer, T.K. Watanabe & J.F. Crow, 1974. The genetic variance for viability and its components in a population of Drosophila melanogaster. Genetics 72: 763–769.
Nuzhdin, S.V., E.G. Pasyukova, C.L. Dilda, Z.-B. Zeng & T.F.C. Mackay, 1997. Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 94: 9734–9739.
Orr, W.C. & R.S. Sohal, 1994. Extension of life-span by overex-pression of Superoxide dismutase and catalase in Drosophila melanogaster. Science 263: 1128–1130.
Partridge, L. & R. Andrews, 1985. The effect of reproductive activity on the longevity of male Drosophila melanogaster is not caused by an acceleration of ageing. J. Insect Physiol. 31: 393–395.
Partridge, L. & N.H. Barton, 1993. Optimality, mutation and the evolution of aging. Nature 362: 305–311.
Partridge, L. & N.H. Barton, 1996. On measuring the rate of ageing. Proc. R. Soc. Lond. B. 263: 1365–1371.
Partridge, L. & K. Fowler, 1992. Direct and correlated responses to selection on age at reproduction in Drosophila melanogaster. Evolution 46: 76–91.
Pletcher, S.D., D. Houle & J.W. Curtsinger, 1998. Age-specific prop erties of spontaneous mutations affecting mortality in Drosophila melanogaster. Genetics 148: 287–303.
Pomiankowski, A., Y. Iwasa & S. Nee, 1991. The evolution of costly mate preferences. I. Fisher and biased mutation. Evolution 45: 1422–1430.
Promislow, D.E.L., 1991. Senescence in natural populations of mam mals: A comparative study. Evolution 45: 1869–1887.
Promislow, D.E.L., M. Tatar, A. Khazaeli & J.W. Curtsinger, 1996. Age-specific patterns of genetic variance in Drosophila melanogaster. I. Mortality. Genetics 143: 839–848.
Promislow, D.E.L., M. Tatar, S. Pletcher & J.R. Carey, Submitted. Below-threshold mortality: Implications for studies in evolution, ecology and demography. Journal of Evolutionary Biology.
Rogina, B. & S.L. Helfand, 1995. Regulation of gene-expression is linked to life-span in adult Drosophila. Genetics 141: 1043–1048.
Rogina, B. & S.L. Helfand, 1996. Timing of expression of a gene in the adult Drosophila is regulated by mechanisms independent of temperature and metabolic rate. Genetics 143: 1643–1651.
Rose, M.R., 1984. Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38: 1004–1010.
Rose, M.R., 1985. Life history evolution with antagonistic pleiotropy and overlapping generations. Theor. Pop. Biol. 28: 342–358.
Rose, M.R., 1991. Evolutionary Biology of Aging. Oxford Univer sity Press, Oxford.
Rose, M.R. & B. Charlesworth, 1980. A test of evolutionary theories of senescence. Nature 287: 141–142.
Rose, M.R. & B. Charlesworth, 1981a. Genetics of life-history evolution in Drosophila melanogaster.II.Exploratory selection experiments. Genetics 97: 187–196.
Rose, M.R. & B. Charlesworth, 1981b. Genetics of life-history evolution in Drosophila melanogaster.I.Sib analysis of adult females. Genetics 97: 173–186.
Searle, S.R., G. Casella & C.E. McCulloch, 1992. Variance Components. Wiley, New York.
Service, P.M., E.W. Hutchinson & M.R. Rose, 1988. Multiple genetic mechanisms for the evolution of senescence in Drosophila melanogaster. Evolution 42: 708–716.
Service, P.M. & M.R. Rose, 1985. Genetic covariation among lifehistory components: the effects of novel environments. Evolution 39: 943–945.
Simmons, M.J. & J.F. Crow, 1977. Mutations affecting fitness in Drosophila populations. Ann. Rev. Genet. 11: 49–78.
Tanaka, Y., 1993. A genetic mechanism for the evolution of senes cence in Callosobruchus chinensis (the azuki bean weevil). Heredity 70: 318–321.
Tatar, M. & J.R. Carey, 1995. Nutrition mediates reproductive trade offs with age-specific mortality in the beetle Callosobruchus maculatus. Ecology 76: 2066–2073.
Tatar, M., J.R. Carey & J.W. Vaupel, 1993. Long term cost of repro duction without accelerated senescence in Callosobruchus maculatus: analysis of age-specific mortality. Evolution 47: 1302–1312.
Tatar, M., A. Khazaeli & J.W. Curtsinger, 1997. Chaperoning extend ed life. Nature 390: 30.
Tatar, M., D.E.L. Promislow, A. Khazaeli & J. Curtsinger, 1996. Age-specific patterns of genetic variance in Drosophila melanogaster: II. Fecundity and its genetic correlation with agespecific mortality. Genetics 143: 849–858.
Vaupel, J.W., T.E. Johnson & G.J. Lithgow, 1994. Rates of mortality in populations of Caenorhabditis elegans. Science 266: 826.
Wattiaux, J.M., 1968a. Cumulative parental effects in Drosophila subobscura. Evolution 22: 406–421.
Wattiaux, J.M., 1968b. Parental age effects in Drosophila pseudoob-scura. Exp. Geront. 3: 55–61.
Weindruch, R. & R.L. Walford, 1982. Dietary restriction in mice beginning at 1 year of age: Effect on life-span and spontaneous cancer incidence. Science 215: 1415–1418.
Williams, G.C., 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11: 398–411.
Yu, B.P., E.J. Masoro & C.A. McMahan, 1985. Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. J. Gerontology 40: 656–670.
Zwaan, B., R. Bijlsma & R. F. Hoekstra, 1995. Artificial selection for development time in Drosophila melanogaster in relation to the evolution of aging: Direct and correlated responses. Evolution 49: 635–648.
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Promislow, D.E.L., Tatar, M. (1998). Mutation and senescence: where genetics and demography meet. In: Woodruff, R.C., Thompson, J.N. (eds) Mutation and Evolution. Contemporary Issues in Genetics and Evolution, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5210-5_24
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