Biochemistry (Moscow)

, Volume 77, Issue 7, pp 716–725 | Cite as

Adaptive aging in the context of evolutionary theory

  • J. J. MitteldorfEmail author


Compelling evidence for an adaptive origin of aging has clashed with traditional evolutionary theory based on exclusively individual selection. The consensus view has been to try to understand aging in the context of a narrow, restrictive evolutionary paradigm, called the Modern Synthesis, or neo-Darwinism. But neo-Darwinism has shown itself to be inadequate in other ways, failing to account for stable ecosystems, for the evolution of sex and the maintenance of diversity and the architecture of the genome, which appears to be optimized for evolvability. Thus aging is not the only reason to consider overhauling the standard theoretical framework. Selection for stable ecosystems is rapid and efficient, and so it is the easiest modification of the neo-Darwinian paradigm to understand and to model. Aging may be understood in this context. More profound and more mysterious are the ways in which the process of evolution itself has been transformed in a boot-strapping process of selection for evolvability. Evolving organisms have learned to channel their variation in ways that are likely to enhance their long-term prospects. This is an expanded notion of fitness. Only in this context can the full spectrum of sophisticated adaptations be understood, including aging, sex, diversity, ecological interdependence, and the structure of the genome.

Key words

evolvability aging sex evolutionary capacitance canalization 


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  1. 1.
    Mitteldorf, J. (2004) Evol. Ecol. Res., 6, 1–17.Google Scholar
  2. 2.
    Mitteldorf, J. (2010) Evolutionary Origins of Aging, in Approaches to the Control of Aging: Building a Pathway to Human Life Extension (Fahy, G. M., West, M. D., Coles, L. S., and Harris, S. B., eds.) Springer, New York.Google Scholar
  3. 3.
    Migliaccio, E., Giorgio, M., Mele, S., Pelicci, G., Reboldi, P., Pandolfi, P. P., Lanfrancone, L., and Pelicci, P. G. (1999) Nature, 402, 309–313.PubMedCrossRefGoogle Scholar
  4. 4.
    Ayyadevara, S., Alla, R., Thaden, J. J., and Shmookler Reis, R. J. (2008) Aging Cell, 7, 13–22.PubMedCrossRefGoogle Scholar
  5. 5.
    Guarente, L., and Kenyon, C. (2000) Nature, 408, 255–262.PubMedCrossRefGoogle Scholar
  6. 6.
    Kenyon, C. (2001) Cell, 105, 165–168.PubMedCrossRefGoogle Scholar
  7. 7.
    Kenyon, C. (2005) Cell, 120, 449–460.PubMedCrossRefGoogle Scholar
  8. 8.
    Clark, W. R. (2004) Advances in Gerontology (Moscow), 14, 7–20.Google Scholar
  9. 9.
    Fabrizio, P., Battistella, L., Vardavas, R., Gattazzo, C., Liou, L. L., Diaspro, A., Dossen, J. W., Gralla, E. B., and Longo, V. D. (2004) J. Cell Boil., 166, 1055–1067.CrossRefGoogle Scholar
  10. 10.
    Cawthon, R. M., Smith, K. R., O’Brien, E., Sivatchenko, A., and Kerber, R. A. (2003) Lancet, 361, 393–395.PubMedCrossRefGoogle Scholar
  11. 11.
    Marzetti, E., and Leeuwenburgh, C. (2006) Exp. Gerontol., 41, 1234–1238.PubMedCrossRefGoogle Scholar
  12. 12.
    Pistilli, E. E., Jackson, J. R., and Alway, S. E. (2006) Apoptosis, 11, 2115–2126.PubMedCrossRefGoogle Scholar
  13. 13.
    Forbes, V. (2000) Funct. Ecol., 14, 12–24.CrossRefGoogle Scholar
  14. 14.
    Masoro, E. J. (2007) Interdiscip. Topics Gerontol., 35, 1–17.Google Scholar
  15. 15.
    Williams, G. (1966) Adaptation and Natural Selection, Princeton University Press, Princeton.Google Scholar
  16. 16.
    Olshansky, S., Hayflick, L., and Carnes, B. (2002) Sci. Am., 286, 92–95.PubMedCrossRefGoogle Scholar
  17. 17.
    Mitteldorf, J. (2006) Evol. Ecol. Res., 8, 561–574.Google Scholar
  18. 18.
    Mitteldorf, J., and Pepper, J. (2009) J. Theor. Biol., 260, 186–195.PubMedCrossRefGoogle Scholar
  19. 19.
    Martin, G. M. (2005) American Aging Assoc. Newsletter, 1–15.Google Scholar
  20. 20.
    Bell, G. (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality, University of California Press, Berkeley.Google Scholar
  21. 21.
    Burt, A. (2000) Evol. Int. J. Org. Evol., 54, 337–351.Google Scholar
  22. 22.
    Ruddle, F. H., Bartels, J. L., Bentley, K. L., Kappen, C., Murtha, M. T., and Pendleton, J. W. (1994) Ann. Rev. Genet., 28, 423–442.PubMedCrossRefGoogle Scholar
  23. 23.
    Kirschner, M., and Gerhart, J. (2006) The Plausibility of Life, Yale University Press, New Haven, CT.Google Scholar
  24. 24.
    Shapiro, J. A. (2011) Evolution: A View from the 21st Century, FT Press.Google Scholar
  25. 25.
    Margulis, L., and Sagan, D. (2002) Acquiring Genomes, Basic Books.Google Scholar
  26. 26.
    Thompson, J. N. (1994) The Coevolutionary Process, University of Chicago Press, Chicago.Google Scholar
  27. 27.
    Endler, J. A. (1985) Natural Selection in the Wild, Princeton University Press, Princeton, NJ.Google Scholar
  28. 28.
    Sober, E. (1980) Philosophy Sci., 47, 350–380.CrossRefGoogle Scholar
  29. 29.
    Layzer, D. (1980) Am. Nat., 115, 809–826.CrossRefGoogle Scholar
  30. 30.
    Wagner, G. P., and Altenberg, L. (1996) Evolution, 50, 967–976.CrossRefGoogle Scholar
  31. 31.
    Martins, A. C. (2011) PLOS One, 6, e24328.PubMedCrossRefGoogle Scholar
  32. 32.
    Libertini, G. (1988) J. Theor. Biol., 132, 145–162.PubMedCrossRefGoogle Scholar
  33. 33.
    Haldane, J. B. S. (1924) Trans Cambridge Phil. Soc., 23, 19–41.Google Scholar
  34. 34.
    Wright, S. (1931) Genetics, 16, 97–159.PubMedGoogle Scholar
  35. 35.
    Fisher, R. A. (1930) The Genetical Theory of Natural Selection, The Clarendon Press, Oxford.Google Scholar
  36. 36.
    Cabej, N. R. (2012) Epigenetic Principles of Evolution, Elsevier, Boston, MA.Google Scholar
  37. 37.
    Darwin, C. (1872) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, John Murray, London.Google Scholar
  38. 38.
    Dawkins, R. (1976) The Selfish Gene, Oxford University Press, Oxford.Google Scholar
  39. 39.
    Pepper, J. W. (2003) Biosystems, 69, 115–126.PubMedCrossRefGoogle Scholar
  40. 40.
    Hughes, A. L. (2000) Adaptive Evolution of Genes and Genomes, Oxford University Press, Oxford, UK.Google Scholar
  41. 41.
    Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W. J., Mattick, J. S., and Haussler, D. (2004) Science, 304, 1321–1325.PubMedCrossRefGoogle Scholar
  42. 42.
    Weismann, A., Poulton, E. B., Schonland, S., and Shipley, A. E. (1891) Essays upon Heredity and Kindred Biological Problems, Clarendon Press, Oxford.Google Scholar
  43. 43.
    Pembrey, M. E. (2002) Eur. J. Hum. Genet., 10, 669–671.PubMedCrossRefGoogle Scholar
  44. 44.
    Wright, G. A., Choudhary, A. F., and Bentley, M. A. (2009) Proc. Biol. Sci., 276, 2597–2604.PubMedCrossRefGoogle Scholar
  45. 45.
    Takahata, N., and Nei, M. (1990) Genetics, 124, 967–978.PubMedGoogle Scholar
  46. 46.
    Dollo, L. (1893) Bull. Soc. Belg. Geol. Pal. Hydr., VII, 164–166.Google Scholar
  47. 47.
    Masel, J. (2005) Genetics, 170, 1359–1371.PubMedCrossRefGoogle Scholar
  48. 48.
    Bergman, A., and Siegal, M. L. (2003) Nature, 424, 549–552.PubMedCrossRefGoogle Scholar
  49. 49.
    Woese, C. R. (2000) Proc. Natl. Acad. Sci. USA, 97, 8392–8396.PubMedCrossRefGoogle Scholar
  50. 50.
    Wynne-Edwards, V. (1962) Animal Dispersion in Relation to Social Behavior, Oliver & Boyd, Edinburgh.Google Scholar
  51. 51.
    Price, G. R. (1970) Nature, 227, 520–521.PubMedCrossRefGoogle Scholar
  52. 52.
    Price, G. R. (1972) Ann. Hum. Genet., 35, 485–490.PubMedCrossRefGoogle Scholar
  53. 53.
    Wilson, D. S. (1975) Proc. Natl. Acad. Sci. USA, 72, 143–146.PubMedCrossRefGoogle Scholar
  54. 54.
    Wilson, D. S. (1980) The Natural Selection of Populations and Communities, Benjamin Cummings, Menlo Park, CA.Google Scholar
  55. 55.
    Maynard Smith, J. (1976) Q. Rev. Biol., 51, 277–283.CrossRefGoogle Scholar
  56. 56.
    Hamilton, W. D. (1964) J. Theor. Biol., 7, 1–16.PubMedCrossRefGoogle Scholar
  57. 57.
    Hamilton, W. D. (1964) J. Theor. Biol., 7, 17–52.PubMedCrossRefGoogle Scholar
  58. 58.
    Sober, E., and Wilson, D. S. (1998) Unto Others: The Evolution and Psychology of Unselfish Behavior, Harvard University Press, Cambridge, MA.Google Scholar
  59. 59.
    Gilpin, M. E. (1975) Group Selection in Predator-Prey Communities, Princeton University Press, Princeton.Google Scholar
  60. 60.
    Pepper, J., and Smuts, B. B. (2000) in Dynamics in Human and Primate Societies: Agent-Based Modeling of Social and Spatial Processes (Kohler, T. A., and Gumerman, G. J., eds.) Oxford University Press, Oxford, pp. 45–76.Google Scholar
  61. 61.
    Klein, D. R. (1968) J. Wildlife Manag., 32, 350–367.CrossRefGoogle Scholar
  62. 62.
    Lockwood, J. A., and Debrey, L. D. (1990) Environ. Entomol., 19, 1194–1205.Google Scholar
  63. 63.
    Travis, J. M. (2004) J. Gerontol., 59, 301–305.Google Scholar
  64. 64.
    Medawar, P. B. (1952) An Unsolved Problem of Biology, Published for the college by H. K. Lewis, London.Google Scholar
  65. 65.
    Trubitsyn, A. (2006) Advances in Gerontology (Moscow), 19, 13–24.Google Scholar
  66. 66.
    Mitteldorf, J., and Pepper, J. (2007) Theory Biosci., 126, 3–8.PubMedCrossRefGoogle Scholar
  67. 67.
    Mitteldorf, J., and Goodnight, C. (2012) Oikos, in press; DOI: 10.1111/j.1600-0706.2012.19995.xGoogle Scholar
  68. 68.
    Bowles, J. T. (1998) Med. Hypoth., 51, 179–221.CrossRefGoogle Scholar
  69. 69.
    Clark, W. R. (1998) Sex and the Origins of Death, Oxford University Press, Oxford.Google Scholar
  70. 70.
    Policansky, D. (1982) Ann. Rev. Ecol. Syst., 13, 471–495.CrossRefGoogle Scholar
  71. 71.
    Michod, R. E. (1999) in Levels of Selection in Evolution (Keller, L., ed.) Princeton University Press, Princeton, NJ.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of VermontBurlingtonUSA

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