Theory in Biosciences

, Volume 126, Issue 1, pp 3–8 | Cite as

How can evolutionary theory accommodate recent empirical results on organismal senescence?

  • Joshua MitteldorfEmail author
  • John W. Pepper
Original Paper


According to a prominent recent report, guppies collected from sites lacking predators are inferior in every aspect of their life history profile to those evolved in other, nearby sites with predators present. This is an exception to two classical predictions of evolutionary theory: that low extrinsic mortality should be associated with longer life span, and that higher fertility should be associated with shorter life span. Some theorists have tried to accommodate this and other anomalous results within the standard framework, but we argue that the exceptions they carve out do not explain the results at hand. In fact, the findings suggest that population regulation has been selected at the group level, though this is a mechanism that most theorists regard with suspicion. We conclude by relating the present result to other experiments that seem to point in the same direction.


Group selection Aging Guppies Poecilia reticulata Life history theory Reproductive potential 



We thank a very knowledgeable anonymous referee for many helpful comments


  1. Abrams PA (1993) Does increased mortality favor the evolution of more rapid senescence? Evolution 47(3):877–887CrossRefGoogle Scholar
  2. Austad SN (1993) Retarded senescence in an insular population of virginia opossums (Didelphis virginiana). J Zool 229:695–708CrossRefGoogle Scholar
  3. Austad SN, Fischer KE (1991) Mammalian aging, metabolism, and ecology - evidence from the bats and marsupials. J Gerontol 46(2):B47–B53PubMedGoogle Scholar
  4. Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. Croom Helm, LondonGoogle Scholar
  5. Bredesen DE (2004) The non-existent aging program: how does it work? Aging Cell 3(5):255–259PubMedCrossRefGoogle Scholar
  6. Bryant MJ, Reznick D (2004) Comparative studies of senescence in natural populations of guppies. Am Nat 163(1):55–68PubMedCrossRefGoogle Scholar
  7. Charlesworth B (1994) The evolution of life histories. Cambridge University Press, CambridgeGoogle Scholar
  8. Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91Google Scholar
  9. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, OxfordGoogle Scholar
  10. Gray DA, Cade WH (2000) Senescence in field crickets (Orthoptera; Gryllidae): examining the effects of sex and a sex-biased parasitoid. Can J Zool-Rev Canadienne De Zoologie 78(1):140–143CrossRefGoogle Scholar
  11. Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389(6654):958–960CrossRefGoogle Scholar
  12. Kenyon C (2001) A conserved regulatory system for aging. Cell 105(2): 165–168PubMedCrossRefGoogle Scholar
  13. Leroi AM, Chippindale AK, Rose MR (1994) Long-term laboratory evolution of a genetic life-history tradeoff in Drosophila melanogaster. 1. The role of genotype-by-environment interaction. Evolution 48:1244–1257CrossRefGoogle Scholar
  14. Medawar PB (1952) An unsolved problem of biology. H. K. Lewis, LondonGoogle Scholar
  15. Miller RA, Dysko R et al (2000) Mouse (Mus musculus) stocks derived from tropical islands: new models for genetic analysis of life history traits. J Zool 250:94–104Google Scholar
  16. Miller RA, Harper JM et al (2002) Longer life spans and delayed maturation in wild-derived mice. Exp Biol Med 227(7):500–508Google Scholar
  17. Mitteldorf J (2004) Ageing selected for its own sake. Evol Ecol Res 6:937–953Google Scholar
  18. Mitteldorf J (2006) Chaotic population dynamics and the evolution of ageing: proposing a demographic theory of senescence. Evol Ecol Res 8:561–574Google Scholar
  19. Mitteldorf J, Pepper J (2007) Senescence as an adaptation to limit the spread of disease. Theor Pop Biol (in press)Google Scholar
  20. Pepper JW, Smuts BB (2000) The evolution of cooperation in an ecological context: an agent-based model. In: Kohler TA, Gumerman GJ (eds) Dynamics in human and primate societies: agent-based modeling of social and spatial processes. Oxford University Press, Oxford, pp 45–76Google Scholar
  21. Reznick D, Buckwalter G et al (2001) The evolution of senescence in natural populations of guppies (Poecilia reticulata): a comparative approach. Exp Gerontol 36(4–6):791–812PubMedCrossRefGoogle Scholar
  22. Reznick DN, Bryant MJ, Roff D, Ghalambor CK, Ghalambor DE (2004) Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095–1099PubMedCrossRefGoogle Scholar
  23. Ricklefs RE (1998) Evolutionary theories of aging: Confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. Am Nat 152(1):24–44CrossRefPubMedGoogle Scholar
  24. Rose MR (1991) Evolutionary biology of aging. Oxford University Press, OxfordGoogle Scholar
  25. Stearns S (1992) The evolution of life histories. Oxford Press, OxfordGoogle Scholar
  26. Van Valen L (1973) A new evolutionary law. Evol Theory 1:1–30Google Scholar
  27. Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411CrossRefGoogle Scholar
  28. Williams PD, Day T (2003) Antagonistic pleiotropy, mortality source interactions, and the evolutionary theory of senescence. Evolution 57:1478–1488PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.PhiladelphiaUSA

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