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Adaptive aging in the context of evolutionary theory

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Abstract

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.

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References

  1. Mitteldorf, J. (2004) Evol. Ecol. Res., 6, 1–17.

    Google Scholar 

  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. Migliaccio, E., Giorgio, M., Mele, S., Pelicci, G., Reboldi, P., Pandolfi, P. P., Lanfrancone, L., and Pelicci, P. G. (1999) Nature, 402, 309–313.

    Article  PubMed  CAS  Google Scholar 

  4. Ayyadevara, S., Alla, R., Thaden, J. J., and Shmookler Reis, R. J. (2008) Aging Cell, 7, 13–22.

    Article  PubMed  CAS  Google Scholar 

  5. Guarente, L., and Kenyon, C. (2000) Nature, 408, 255–262.

    Article  PubMed  CAS  Google Scholar 

  6. Kenyon, C. (2001) Cell, 105, 165–168.

    Article  PubMed  CAS  Google Scholar 

  7. Kenyon, C. (2005) Cell, 120, 449–460.

    Article  PubMed  CAS  Google Scholar 

  8. Clark, W. R. (2004) Advances in Gerontology (Moscow), 14, 7–20.

    CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  10. Cawthon, R. M., Smith, K. R., O’Brien, E., Sivatchenko, A., and Kerber, R. A. (2003) Lancet, 361, 393–395.

    Article  PubMed  CAS  Google Scholar 

  11. Marzetti, E., and Leeuwenburgh, C. (2006) Exp. Gerontol., 41, 1234–1238.

    Article  PubMed  CAS  Google Scholar 

  12. Pistilli, E. E., Jackson, J. R., and Alway, S. E. (2006) Apoptosis, 11, 2115–2126.

    Article  PubMed  CAS  Google Scholar 

  13. Forbes, V. (2000) Funct. Ecol., 14, 12–24.

    Article  Google Scholar 

  14. Masoro, E. J. (2007) Interdiscip. Topics Gerontol., 35, 1–17.

    CAS  Google Scholar 

  15. Williams, G. (1966) Adaptation and Natural Selection, Princeton University Press, Princeton.

  16. Olshansky, S., Hayflick, L., and Carnes, B. (2002) Sci. Am., 286, 92–95.

    Article  PubMed  Google Scholar 

  17. Mitteldorf, J. (2006) Evol. Ecol. Res., 8, 561–574.

    Google Scholar 

  18. Mitteldorf, J., and Pepper, J. (2009) J. Theor. Biol., 260, 186–195.

    Article  PubMed  Google Scholar 

  19. Martin, G. M. (2005) American Aging Assoc. Newsletter, 1–15.

  20. Bell, G. (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality, University of California Press, Berkeley.

    Google Scholar 

  21. Burt, A. (2000) Evol. Int. J. Org. Evol., 54, 337–351.

    CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  23. Kirschner, M., and Gerhart, J. (2006) The Plausibility of Life, Yale University Press, New Haven, CT.

    Google Scholar 

  24. Shapiro, J. A. (2011) Evolution: A View from the 21st Century, FT Press.

  25. Margulis, L., and Sagan, D. (2002) Acquiring Genomes, Basic Books.

  26. Thompson, J. N. (1994) The Coevolutionary Process, University of Chicago Press, Chicago.

    Google Scholar 

  27. Endler, J. A. (1985) Natural Selection in the Wild, Princeton University Press, Princeton, NJ.

    Google Scholar 

  28. Sober, E. (1980) Philosophy Sci., 47, 350–380.

    Article  Google Scholar 

  29. Layzer, D. (1980) Am. Nat., 115, 809–826.

    Article  Google Scholar 

  30. Wagner, G. P., and Altenberg, L. (1996) Evolution, 50, 967–976.

    Article  Google Scholar 

  31. Martins, A. C. (2011) PLOS One, 6, e24328.

    Article  PubMed  CAS  Google Scholar 

  32. Libertini, G. (1988) J. Theor. Biol., 132, 145–162.

    Article  PubMed  CAS  Google Scholar 

  33. Haldane, J. B. S. (1924) Trans Cambridge Phil. Soc., 23, 19–41.

    Google Scholar 

  34. Wright, S. (1931) Genetics, 16, 97–159.

    PubMed  CAS  Google Scholar 

  35. Fisher, R. A. (1930) The Genetical Theory of Natural Selection, The Clarendon Press, Oxford.

    Google Scholar 

  36. Cabej, N. R. (2012) Epigenetic Principles of Evolution, Elsevier, Boston, MA.

    Google Scholar 

  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. Dawkins, R. (1976) The Selfish Gene, Oxford University Press, Oxford.

    Google Scholar 

  39. Pepper, J. W. (2003) Biosystems, 69, 115–126.

    Article  PubMed  CAS  Google Scholar 

  40. Hughes, A. L. (2000) Adaptive Evolution of Genes and Genomes, Oxford University Press, Oxford, UK.

    Google Scholar 

  41. Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W. J., Mattick, J. S., and Haussler, D. (2004) Science, 304, 1321–1325.

    Article  PubMed  CAS  Google Scholar 

  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. Pembrey, M. E. (2002) Eur. J. Hum. Genet., 10, 669–671.

    Article  PubMed  Google Scholar 

  44. Wright, G. A., Choudhary, A. F., and Bentley, M. A. (2009) Proc. Biol. Sci., 276, 2597–2604.

    Article  PubMed  Google Scholar 

  45. Takahata, N., and Nei, M. (1990) Genetics, 124, 967–978.

    PubMed  CAS  Google Scholar 

  46. Dollo, L. (1893) Bull. Soc. Belg. Geol. Pal. Hydr., VII, 164–166.

    Google Scholar 

  47. Masel, J. (2005) Genetics, 170, 1359–1371.

    Article  PubMed  CAS  Google Scholar 

  48. Bergman, A., and Siegal, M. L. (2003) Nature, 424, 549–552.

    Article  PubMed  CAS  Google Scholar 

  49. Woese, C. R. (2000) Proc. Natl. Acad. Sci. USA, 97, 8392–8396.

    Article  PubMed  CAS  Google Scholar 

  50. Wynne-Edwards, V. (1962) Animal Dispersion in Relation to Social Behavior, Oliver & Boyd, Edinburgh.

    Google Scholar 

  51. Price, G. R. (1970) Nature, 227, 520–521.

    Article  PubMed  CAS  Google Scholar 

  52. Price, G. R. (1972) Ann. Hum. Genet., 35, 485–490.

    Article  PubMed  CAS  Google Scholar 

  53. Wilson, D. S. (1975) Proc. Natl. Acad. Sci. USA, 72, 143–146.

    Article  PubMed  CAS  Google Scholar 

  54. Wilson, D. S. (1980) The Natural Selection of Populations and Communities, Benjamin Cummings, Menlo Park, CA.

    Google Scholar 

  55. Maynard Smith, J. (1976) Q. Rev. Biol., 51, 277–283.

    Article  Google Scholar 

  56. Hamilton, W. D. (1964) J. Theor. Biol., 7, 1–16.

    Article  PubMed  CAS  Google Scholar 

  57. Hamilton, W. D. (1964) J. Theor. Biol., 7, 17–52.

    Article  PubMed  CAS  Google Scholar 

  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. Gilpin, M. E. (1975) Group Selection in Predator-Prey Communities, Princeton University Press, Princeton.

    Google Scholar 

  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. Klein, D. R. (1968) J. Wildlife Manag., 32, 350–367.

    Article  Google Scholar 

  62. Lockwood, J. A., and Debrey, L. D. (1990) Environ. Entomol., 19, 1194–1205.

    Google Scholar 

  63. Travis, J. M. (2004) J. Gerontol., 59, 301–305.

    Google Scholar 

  64. Medawar, P. B. (1952) An Unsolved Problem of Biology, Published for the college by H. K. Lewis, London.

    Google Scholar 

  65. Trubitsyn, A. (2006) Advances in Gerontology (Moscow), 19, 13–24.

    CAS  Google Scholar 

  66. Mitteldorf, J., and Pepper, J. (2007) Theory Biosci., 126, 3–8.

    Article  PubMed  Google Scholar 

  67. Mitteldorf, J., and Goodnight, C. (2012) Oikos, in press; DOI: 10.1111/j.1600-0706.2012.19995.x

  68. Bowles, J. T. (1998) Med. Hypoth., 51, 179–221.

    Article  CAS  Google Scholar 

  69. Clark, W. R. (1998) Sex and the Origins of Death, Oxford University Press, Oxford.

    Google Scholar 

  70. Policansky, D. (1982) Ann. Rev. Ecol. Syst., 13, 471–495.

    Article  Google Scholar 

  71. Michod, R. E. (1999) in Levels of Selection in Evolution (Keller, L., ed.) Princeton University Press, Princeton, NJ.

    Google Scholar 

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  1. Department of Biology, University of Vermont, Burlington, VT, 05405, USA

    J. J. Mitteldorf

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Published in Russian in Biokhimiya, 2012, Vol. 77, No. 7, pp. 858–870.

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Mitteldorf, J.J. Adaptive aging in the context of evolutionary theory. Biochemistry Moscow 77, 716–725 (2012). https://doi.org/10.1134/S0006297912070036

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