Genetica

, Volume 91, Issue 1–3, pp 89–98

Evolution of aging: Testing the theory usingDrosophila

  • L. Partridge
  • N. H. Barton
Article

Abstract

Evolutionary explanations of aging (or senescence) fall into two classes. First, organisms might have evolved the optimal life history, in which survival and fertility late in life are sacrificed for the sake of early reproduction or high pre-adult survival. Second, the life history might be depressed below this optimal compromise by the influx of deleterious mutations; since selection against late-acting mutations is weaker, deleterious mutations will impose a greater load on late life. We discuss ways in which these theories might be investigated and distinguished, with reference to experimental work withDrosophila. While genetic correlations between life history traits determine the immediate response to selection, they are hard to measure, and may not reflect the fundamental constraints on life history. Long term selection experiments are more likely to be informative. The third approach of using experimental manipulations suffers from some of the same problems as measures of genetic correlations; however, these two approaches may be fruitful when used together. The experimental results so far suggest that aging inDrosophila has evolved in part as a consequence of selection for an optimal life history, and in part as a result of accumulation of predominantly late-acting deleterious mutations. Quantification of these effects presents a major challenge for the future.

Key words

aging senescence lifespan survival Drosophila evolution fertility 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barton, N. H., 1990. Pleiotropic models of quantitative variation. Genetics 124: 773–782.PubMedGoogle Scholar
  2. Barton, N. H. & M. Turelli, 1989. Evolutionary quantitative genetics: how little do we know? Ann. Rev. Genet. 23: 337–370.PubMedGoogle Scholar
  3. Bell, G. & V. Koufopanou, 1986. The cost of reproduction. Oxf. Surv. Evol. Biol. 3: 83–131.Google Scholar
  4. Bulmer, M. G., 1980. The Mathematical Theory of Quantitative Genetics. Oxford University Press, Oxford.Google Scholar
  5. Caballero, A., M. Toro & C. Lopez-Fanjul, 1991. The response to artificial selection from new mutations inDrosophila melanogaster, Genetics 128: 89–102.PubMedGoogle Scholar
  6. Calow, P., 1979. The cost of reproduction: a physiological approach. Biol. Rev. 54: 23–40.PubMedGoogle Scholar
  7. Carey, J. R., P. Leido, D. Orozco & J. W. Vaupel, 1992. Slowing of mortality rates at older ages in large medfly cohorts. Science 258: 457–461.PubMedGoogle Scholar
  8. Chapman, T., 1992. A cost of mating with males that do not transfer sperm in femaleDrosophila melanogaster. J. Insect Physiol. 38: 223–227.Google Scholar
  9. Charlesworth, B., 1980. Evolution in Age-Structured Populations. Cambridge University Press, Cambridge.Google Scholar
  10. Charlesworth, B., 1990. Optimization models, quantitative genetics and mutation. Evolution 44: 520–538.Google Scholar
  11. Charnov, E. L., 1989. Phenotypic evolution under Fisher's fundamental theorem of natural selection. Heredity 62: 113–116.PubMedGoogle Scholar
  12. Chippindale, A. K., A. M. Leroi, S. B. Kim & M. R. Rose, 1993. Phenotypic plasticity of life history mimics response to selection inDrosophila melanogaster: trade-offs between survival and reproduction. J. Evol. Biol. 6: 171–193.Google Scholar
  13. Clark, A. G., 1987. Senescence and the genetic-correlation hangup. Amer. Natur. 129: 932–940.Google Scholar
  14. Curtsinger, J. W., H. H. Fukui, D. R. Townsend & J. W. Vaupel, 1992. Demography of genotypes: failure of the limited lifespan paradigm inDrosophila melanogaster. Science 258: 461–463.PubMedGoogle Scholar
  15. Edney, E. B. & R. W. Gill, 1968. Evolution of senescence and specific longevity. Nature 220: 281–282.PubMedGoogle Scholar
  16. Finch, C. E., 1990. Longevity, senescence and the genome. University of Chicago Press, Chicago.Google Scholar
  17. Fowler, K. & L. Partridge, 1989. A cost of mating in female fruitflies. Nature 338: 760–761.Google Scholar
  18. Gomulkiewicz, R. & M. Kirkpatrick, 1992. Quantitative genetics and the evolution of reaction norms. Evolution 46: 390–411.Google Scholar
  19. Hamilton, W. D., 1966. The moulding of senescence by natural selection. J. Theor. Biol. 12: 12–45.PubMedGoogle Scholar
  20. Harshman, L. G., A. A. Hoffmann & T. Prout, 1988. Environmental effects on remating inDrosophila melanogaster. Evolution 42: 312–321.Google Scholar
  21. Hill, W. G., 1982. Rates of change in quantitative traits from fixation of new mutations. Proc. Natl. Acad. Sci. (USA) 79: 142–145.Google Scholar
  22. Houle, D., 1991. Genetic covariance of fitness correlates: what genetic correlations are made of, and why it matters. Evolution 45: 630–648.Google Scholar
  23. Houle, D., D. K. Hoffmaster, S. Assimacopoulos & B. Charlesworth, 1992. The genomic mutation rate for fitness inDrosophila. Nature 359: 58–60.PubMedGoogle Scholar
  24. Hutchinson, E. W., & M. R. Rose, 1991. Quantitative genetics of postponed aging inDrosophila melanogaster. I. Analysis of outbred populations. Genetics 127: 719–727.PubMedGoogle Scholar
  25. Hutchinson, E. W., A. J. Shaw & M. R. Rose, 1991. Quantitative genetics of postponed aging inDrosophila melanogaster. II. Analysis of selected lines. Genetics 127: 729–737.PubMedGoogle Scholar
  26. Kirkwood, T. B. L. & M. R. Rose, 1991. Evolution of senescence: late survival sacrificed for reproduction. Phil. Trans. Roy. Soc. Lond. B. 332: 15–24.Google Scholar
  27. Lamb, M. J., 1964. The effects of radiation on the longevity of femaleDrosophila subobscura. J. Insect Physiol. 10: 487–497.Google Scholar
  28. Lande, R., 1980. The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94: 203–215.Google Scholar
  29. Lande, R., 1982. A quantitative genetic theory of life history evolution. Ecology 63: 609–615.Google Scholar
  30. Lande, R. & S. J. Arnold, 1983. The measurement of selection on correlated characters. Evolution 37: 1210–1226.Google Scholar
  31. Lessells, C. M., 1991. The evolution of life histories, pp. 32–68. Behavioural Ecology: An Evolutionary Approach, edited by J. R. Krebs and N. B. Davies. Blackwell Scientific Publishing.Google Scholar
  32. Luckinbill, L. S., R. Arking, M. J. Clare, W. C. Cirocco & S. A. Buck, 1984. Selection for delayed senescence inDrosophila melanogaster. Evolution 38: 996–1003.Google Scholar
  33. Luckinbill, L. S., J. L. Graves, A. H. Reed & S. Koetsawang, 1988a. Localizing genes that defer senescence inDrosophila melanogaster. Heredity 60: 367–374.PubMedGoogle Scholar
  34. Luckinbill, L. S., J. L. Graves, A. Tomkin & O. Sowirka, 1988b. A qualitative analysis of some life-history correlates of longevity inDrosophila melanogaster. Evol. Ecol. 2: 85–94.Google Scholar
  35. Maynard Smith, J., 1958. The effects of temperature and of egg-laying on the longevity ofDrosophila subobscura. J. Exp. Biol. 35: 832–842.Google Scholar
  36. Mackay, T. F. C., R. F. Lyman & M. S. Jackson, 1992. Effects of P-element insertions on quantitative traits inDrosophila melanogaster. Genetics 130: 315.PubMedGoogle Scholar
  37. McKenzie, J. A. & G. M. Clarke, 1988. Diazinon resistance, fluctuating asymmetry and fitness in the Australian sheep blowfly,Lucilia cuprina. Genetics 120: 213–220.Google Scholar
  38. Medawar, P. B., 1946. Old age and natural death. Modern Quarterly 1: 30–56.Google Scholar
  39. Medawar, P. B., 1952. An unsolved problem of biology. H. K. Lewis, London.Google Scholar
  40. Modi, R. I. & J. Adams, 1991. Coevolution in bacterial-plasmid populations. Evolution 45: 656–667.Google Scholar
  41. Mueller, L. D., 1987. Evolution of accelerated senescence in laboratory populations ofDrosophila. Proc. Natl. Acad. Sci. USA 84: 1974–1977.PubMedGoogle Scholar
  42. Newport, M. E. A. & M. H. Gromko, 1984. The effect of experimental design on female receptivity to remating and its impact on reproductive success inDrosophila melanogaster. Evolution 38: 1261–1272.Google Scholar
  43. Parker, G. A. & J. Maynard Smith. Optimality theory in evolutionary biology. Nature 348: 17–33.Google Scholar
  44. Partridge, L., 1987. Is accelerated senescence a cost of reproduction? Funct. Ecol. 1: 317–320.Google Scholar
  45. Partridge, L., 1988. Lifetime reproductive success inDrosophila. Reproductive success, edited by T. R. Clutton-Brock, University of Chicago Press, Chicago.Google Scholar
  46. Partridge, L., 1992. Measuring reproductive costs. Trends in Ecology and Evolution 7: 99.Google Scholar
  47. Partridge, L. & R. Andrews, 1985. The effect of reproductive activity on the lifespan of maleDrosophila melanogaster is not caused by an acceleration of ageing. J. Insect. Physiol. 31: 393–395.Google Scholar
  48. Partridge, L. & N. H. Barton, 1993. Optimality, mutation and the evolution of ageing. Nature 362: 305–311.PubMedGoogle Scholar
  49. Partridge, L. & K. Fowler, 1991. Non-mating costs of exposure to males in femaleDrosophila melanogaster. J. Insect Physiol. 36: 419–425.Google Scholar
  50. Partridge, L. & K. Fowler, 1992. Direct and correlated responses to selection on age at reproduction inDrosophila melanogaster. Evolution 46: 76–91.Google Scholar
  51. Partridge, L., K. Fowler, S. Trevitt & W. Sharp, 1986. An examination of the effects of males on the survival and egg-production rates of femaleDrosophila melanogaster. J. Insect. Physiol. 32: 925–929.Google Scholar
  52. Partridge, L., A. Green & K. Fowler, 1987. Effects of egg-production and of exposure to males on female survival inDrosophila melanogaster. J. Insect Physiol. 33: 745–749.Google Scholar
  53. Partridge, L. & P. H. Harvey, 1985. Costs of reproduction. Nature 316: 20–21.Google Scholar
  54. Partridge, L. & P. H. Harvey, 1988. The ecological context of life history evolution. Science 241: 1449–1454.Google Scholar
  55. Partridge, L. & R. Sibly, 1991. Constraints in the evolution of life histories. Phil. Trans. R. Soc. Lond.B332: 3–13.Google Scholar
  56. Pease, C. M. & J. J. Bull, 1988, A critique of methods for measuring life-history trade-offs. J. Evol. Biol. 1: 293–303.Google Scholar
  57. Rees, M. & M. J. Long, Germination biology and the ecology of annual plants. Amer. Nat. 139: 484–508.Google Scholar
  58. Reznick, D., 1985. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44: 257–267.Google Scholar
  59. Reznick, D., 1992a. Measuring the costs of reproduction. Trends in Ecology and Evolution 7: 42–45.Google Scholar
  60. Reznick, D., 1992b. Measuring reproductive costs: response to Partridge. Trends in Ecology and Evolution 7: 134.Google Scholar
  61. Roper, C., P. Pignatelli & L. Partridge, 1993. Evolutionary effects of selection on age at reproduction in larval and adultDrosophila melanogaster. Evolution 47: 445–455.Google Scholar
  62. Rose, M. R., 1982. Antagonistic pleiotropy, dominance and genetic variation. Heredity 48: 63–78.Google Scholar
  63. Rose, M. R., 1984. Laboratory evolution of postponed senescence inDrosophila melanogaster. Evolution 38: 1004–1010.Google Scholar
  64. Rose, M. R., 1985. Life history evolution with antagonistic pleiotropy and overlapping generations. Theor. Pop. Biol. 28: 342–358.Google Scholar
  65. Rose, M. R., 1991. Evolutionary Biology of Aging. Oxford University Press, Oxford.Google Scholar
  66. Rose, M. R. & B. Charlesworth, 1980. A test of evolutionary theories of senescence. Nature 287: 141–142.PubMedGoogle Scholar
  67. Rose, M. R. & B. Charlesworth, 1981. Genetics of life history inDrosophila melanogaster. Sib analysis of adult females. Genetics 97: 173–186.Google Scholar
  68. Rose, M. R., P. Service & E. W. Hutchinson, 1987. Three approaches to trade-offs in life history evolution, pp. 91–105 in Genetic Constraints on Adaptive Evolution, edited by V. Loeschcke, Springer-Verlag, Berlin.Google Scholar
  69. Service, P. M., 1987. Physiological mechanisms of increased stress resistance inDrosophila melanogaster selected for postponed senescence. Physiol. Zool. 60: 321–326.Google Scholar
  70. Service, P. M., 1989. The effect of mating status on lifespan, egg laying, and starvation resistance inDrosophila melanogaster in relation to selection on longevity. J. Insect Physiol. 35: 447–452.Google Scholar
  71. Service, P. M., E. W. Hutchinson, M. D. MacKinley & M. R. Rose, 1985. Resistance to environmental stress inDrosophila melanogaster selected for postponed senescence. Physiol. Zool. 58: 380–389.Google Scholar
  72. Service, P. M. and M. R. Rose. Genetic covariation among life-history components: the effect of novel environments. Evolution 39: 943–945.Google Scholar
  73. Shaw, R. G., 1987. Maximum-likelihood approaches applied to quantitative genetics of natural populations. Evolution 41: 82–826.Google Scholar
  74. Stearns, S. C., 1989. Trade-offs in life history evolution. Funct. Ecol. 3: 259–268.Google Scholar
  75. Stearns, S. C., 1992. The Evolution of Life Histories. Oxford University Press, Oxford.Google Scholar
  76. Trevitt, S., 1989. The costs and benefits of repeated mating in the female fruitlyDrosophila melanogaster Meigen. Unpublished PhD Thesis, University of Edinburgh.Google Scholar
  77. Trevitt, S., K. Fowler & L. Partridge, 1988. An effect of egg-deposition on the subsequent fertility and remating frequency of femaleDrosophila melanogaster. J. Insect Physiol. 34: 821–828.Google Scholar
  78. Turelli, M., 1985. Effects of pleiotropy on predictions concerning mutation-selection balance for polygenic traits. Genetics 111: 165–195.PubMedGoogle Scholar
  79. Turelli, M., 1988. Phenotypic evolution, constant covariances, and the maintenance of additive variance. Evolution 42: 1342–1348.Google Scholar
  80. Vaupel, W. V. & A. I. Yashin, 1983. The deviant dynamics of death in heterogeneous populations. RR-83-1, International Institute for Applied Systems Analysis, Laxenburg, Austria.Google Scholar
  81. Wagner, G., 1989. Multivariate mutation-selection balance with constrained pleiotropic effects. Genetics 122: 223–234.PubMedGoogle Scholar
  82. Williams, G. C., 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11: 398–411.Google Scholar
  83. Williams, G. C., 1966. Natural selection, the cost of reproduction, and a refinement of Lack's principle. Amer. Nat. 100: 687–690.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • L. Partridge
    • 1
  • N. H. Barton
    • 1
  1. 1.ICAPB, Division of Biological Sciences, Zoology BuildingUniversity of EdinburghEdinburghUK

Personalised recommendations