Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Effect of extrinsic mortality on the evolution of senescence in guppies

Abstract

Classical theories1,2 for the evolution of senescence predict that organisms that experience low mortality rates attributable to external factors, such as disease or predation, will evolve a later onset of senescence. Here we use patterns of senescence in guppies derived from natural populations that differ in mortality risk to evaluate the generality of these predictions. We have previously found that populations experiencing higher mortality rates evolve earlier maturity and invest more in reproduction, as predicted by evolutionary theory3. We report here that these same populations do not have an earlier onset of senescence with respect to either mortality or reproduction but do with respect to swimming performance, which assesses neuromuscular function. This mosaic pattern of senescence challenges the generality of the association between decreased extrinsic mortality and delayed senescence and invites consideration of more derived theories for the evolution of senescence.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Age at last reproduction.
Figure 2: Fecundity.
Figure 3: Maximum acceleration.

Similar content being viewed by others

References

  1. Medawar, P. B. An Unsolved Problem of Biology (H. K. Lewis and Co., London, 1952)

    Google Scholar 

  2. Williams, G. C. Pleiotropy, natural selection and the evolution of senescence. Evolution 11, 398–411 (1957)

    Article  Google Scholar 

  3. Reznick, D. A., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990)

    Article  ADS  Google Scholar 

  4. Charlesworth, B. Evolution in Age Structured Populations (Cambridge Univ. Press, Cambridge, 1980)

    MATH  Google Scholar 

  5. Abrams, P. Does increased mortality favor the evolution of more rapid senescence? Evolution 47, 877–887 (1993)

    Article  Google Scholar 

  6. Williams, P. D. & Day, T. Antagonistic pleiotropy, mortality source interactions and the evolutionary theory of senescence. Evolution 57, 1478–1488 (2003)

    Article  Google Scholar 

  7. Austad, S. N. & Fischer, K. E. Mammalian aging, metabolism, and ecology—evidence from the Bats and Marsupials. J. Gerontol. 46, B47–B53 (1991)

    Article  CAS  Google Scholar 

  8. Promislow, D. E. L. Senescence in natural-populations of Mammals—a comparative- study. Evolution 45, 1869–1887 (1991)

    Article  Google Scholar 

  9. Austad, S. N. Retarded senescence in an insular population of Virginia opossums (Didelphis virginiana). J. Zool. 299, 695–708 (1993)

    Article  Google Scholar 

  10. Holmes, D. J. & Austad, S. N. The evolution of avian senescence patterns—implications for understanding primary aging processes. Am. Zool. 35, 307–317 (1995)

    Article  Google Scholar 

  11. Keller, L. & Genoud, M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389, 958–960 (1997)

    Article  ADS  CAS  Google Scholar 

  12. Tatar, M., Gray, D. W. & Carey, J. R. Altitudinal variation for senescence in Melanoplus grasshoppers. Oecologia 111, 357–364 (1997)

    Article  ADS  Google Scholar 

  13. Ricklefs, R. E. Evolutionary theories of aging: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. Am. Nat. 152, 24–44 (1998)

    Article  CAS  Google Scholar 

  14. Dudycha, J. & Tessier, A. Natural genetic variation of life span, reproduction, and juvenile growth in Daphnia. Evolution 53, 1744–1756 (1999)

    Article  Google Scholar 

  15. Stearns, S. C., Ackermann, M., Doebeli, M. & Kaiser, M. Experimental evolution of aging, growth, and reproduction in fruitflies. Proc. Natl Acad. Sci. USA 97, 3309–3313 (2000)

    Article  ADS  CAS  Google Scholar 

  16. Hendry, A. P., Morbey, Y. E., Berg, O. K. & Wenburg, J. K. Adaptive variation in senescence: reproductive lifespan in a wild salmon population. Proc. R. Soc. Lond. B 271, 259–266 (2004)

    Article  Google Scholar 

  17. Kirkwood, T. B. L. & Austad, S. N. Why do we age? Nature 408, 233–238 (2000)

    Article  ADS  CAS  Google Scholar 

  18. Partridge, L. & Gems, D. Mechanisms of ageing: public or private? Nature Rev. Genet. 3, 165–175 (2002)

    Article  CAS  Google Scholar 

  19. Reznick, D. N., Butler, M. J. I., Rodd, F. H. & Ross, P. Life history evolution in guppies (Poecilia reticulata). 6. Differential mortality as a mechanism for natural selection. Evolution 50, 1651–1660 (1996)

    PubMed  Google Scholar 

  20. Reznick, D. N., Buckwalter, G., Groff, J. & Elder, D. The evolution of senescence in natural populations of guppies (Poecilia reticulata): a comparative approach. Exp. Gerontol. 36, 791–812 (2001)

    Article  CAS  Google Scholar 

  21. Carvalho, G. R., Shaw, P. W., Magurran, A. E. & Seghers, B. H. Marked genetic divergence revealed by allozymes among populations of the guppy Poecilia reticulata (Poeciliidae), in Trinidad. Biol. J. Linn. Soc. 42, 389–405 (1991)

    Article  Google Scholar 

  22. Reznick, D. N. The impact of predation on life history evolution in Trinidadian guppies: the genetic components of observed life history differences. Evolution 36, 1236–1250 (1982)

    Article  Google Scholar 

  23. Reznick, D. N., Butler, M. J. I. & Rodd, F. H. Life history evolution in guppies 7: The comparative ecology of high and low predation environments. Am. Nat. 157, 126–140 (2001)

    CAS  PubMed  Google Scholar 

  24. S-Plus. S-Plus 6 for Windows Guide to Statistics Vol. 3 (Insightful Corporation, Seattle, Washington, 2001)

    Google Scholar 

  25. Finch, C. E., Pike, M. C. & Whitten, M. Slow mortality rate accelerations during aging in some animals approximate that of humans. Science 249, 902–905 (1990)

    Article  ADS  CAS  Google Scholar 

  26. McMillan, I., Fitz-Earle, M. & Robson, D. S. Quantitative genetics of fertility. I. Lifetime egg production of Drosophila melanogaster. Theor. Genet. 65, 349–353 (1970)

    CAS  Google Scholar 

  27. Domenici, P. & Blake, R. W. The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200, 1165–1178 (1997)

    CAS  PubMed  Google Scholar 

  28. Delbono, O. Neural control of aging skeletal muscle. Aging Cell 2, 21–29 (2003)

    Article  CAS  Google Scholar 

  29. Reznick, D., Ghalambor, C. & Nunney, L. The evolution of senescence in fish. Mech. Ageing Dev. 123, 773–789 (2002)

    Article  Google Scholar 

  30. Luckinbill, L. S. & Clare, M. J. Selection for life span in Drosophila melanogaster. Heredity 55, 9–18 (1985)

    Article  Google Scholar 

  31. Oppenheimer, L., Capizzi, T. P. & Miwa, G. T. Application of the jackknife procedures to inter-experiment comparisons of parameter estimates for the Michaelis–Menten equation. Biochem. J. 197, 721–729 (1981)

    Article  CAS  Google Scholar 

  32. Ghalambor, C., Walker, J. A. & Reznick, D. N. Constraints on adaptive evolution: The functional trade-off between reproduction and burst swimming performance in the guppy (Poecilia reticulata). Am. Nat. 164, 38–50 (2004)

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by NSF Grant and by the Academic Senate of the University of California. We thank P. Abrams, A. Bronikowski, M. Clark and P. Williams for comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David N. Reznick.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Discussion 1

Details of the comparison of the exponential and Gompertz fits to the age at last reproduction and age at death. (DOC 55 kb)

Supplementary Figure 1

Survivorship curves and plots of the natural log of mortality rate (y-axis) versus the log of the age at death (x-axis). (DOC 1082 kb)

Supplementary Discussion 2

A small pilot study on a third population (El Cedro River) of Trinidadian guppies reveals a parallel pattern of senescence. (DOC 52 kb)

Supplementary Discussion 3

Age-specific reproductive value as a function of age was compared between populations. (DOC 39 kb)

Supplementary Figure 2

Senescence as measured by age-specific reproductive value. (DOC 68 kb)

Supplementary Discussion 4

Rate of increase in fecundity with age in guppies from high and low predation environments. (DOC 24 kb)

Supplementary Figure 3

Age-specific fecundity in high and low predation guppies from natural populations. (DOC 121 kb)

Supplementary Methods

Details on the estimation of fecundity functions and reproductive value. (DOC 28 kb)

Supplementary Figure 4

An example of residual analysis using one combination from the Oropuche drainage. (DOC 53 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reznick, D., Bryant, M., Roff, D. et al. Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431, 1095–1099 (2004). https://doi.org/10.1038/nature02936

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02936

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing