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.

Theory predicts the uneven distribution of genetic diversity within species

Abstract

Global efforts to conserve species have been strongly influenced by the heterogeneous distribution of species diversity across the Earth. This is manifest in conservation efforts focused on diversity hotspots1,2,3. The conservation of genetic diversity within an individual species4,5 is an important factor in its survival in the face of environmental changes and disease6,7. Here we show that diversity within species is also distributed unevenly. Using simple genealogical models, we show that genetic distinctiveness has a scale-free power law distribution. This property implies that a disproportionate fraction of the diversity is concentrated in small sub-populations, even when the population is well-mixed. Small groups are of such importance to overall population diversity that even without extrinsic perturbations, there are large fluctuations in diversity owing to extinctions of these small groups. We also show that diversity can be geographically non-uniform—potentially including sharp boundaries between distantly related organisms—without extrinsic causes such as barriers to gene flow or past migration events. We obtained these results by studying the fundamental scaling properties of genealogical trees. Our theoretical results agree with field data from global samples of Pseudomonas bacteria. Contrary to previous studies8, our results imply that diversity loss owing to severe extinction events is high, and focusing conservation efforts on highly distinctive groups can save much of the diversity.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Section of a genealogical tree for a one-dimensional population (part of a much larger tree).
Figure 2: Distribution of diversity and its fluctuation.
Figure 3: Comparison of theoretical values of uniqueness with data from field populations.
Figure 4: Diversity retained after an extinction episode in a well-mixed population.

References

  1. Prendergast, J. R., Quinn, R. M., Lawton, J. H., Eversham, B. C. & Gibbons, D. W. Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365, 335–337 (1993)

    ADS  Article  Google Scholar 

  2. Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000)

    ADS  CAS  Article  Google Scholar 

  3. Gaston, K. J. Global patterns in biodiversity. Nature 405, 220–227 (2000)

    CAS  Article  Google Scholar 

  4. Ehrlich, P. R. & Wilson, E. O. Biodiversity studies: science and policy. Science 253, 758–761 (1991)

    ADS  CAS  Article  Google Scholar 

  5. Faith, D. P. Genetic diversity and taxonomic priorities for conservation. Biol. Conserv. 68, 69–74 (1994)

    ADS  Article  Google Scholar 

  6. Amos, A. & Balmford, A. When does conservation genetics matter? Heredity 87, 257–265 (2001)

    CAS  Article  Google Scholar 

  7. Frankham, R. et al. Do population size bottlenecks reduce evolutionary potential? Anim. Conserv. 2, 255–260 (1999)

    Article  Google Scholar 

  8. Nee, S. & May, R. M. Extinction and the loss of evolutionary history. Science 278, 692–694 (1997)

    ADS  CAS  Article  Google Scholar 

  9. Hudson, R. R. Gene genealogies and the coalescent process. Oxf. Surv. Evol. Biol. 7, 1–44 (1990)

    Google Scholar 

  10. Barton, N. H. & Wilson, I. Genealogies and geography. Phil. Trans. R. Soc. Lond. B 349, 49–59 (1995)

    ADS  CAS  Article  Google Scholar 

  11. Notohara, M. The structured coalescent process with weak migration. J. Appl. Prob. 38, 1–17 (2001)

    MathSciNet  Article  Google Scholar 

  12. Wilkins, J. F. & Wakeley, J. The coalescent in a continuous, finite, linear population. Genetics 161, 873–888 (2002)

    PubMed  PubMed Central  Google Scholar 

  13. Wright, S. Isolation by distance. Genetics 28, 114–138 (1943)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Fisher, R. A. The distribution of gene ratios for rare mutations. Proc. R. Soc. Edinb. 50, 205–220 (1930)

    MATH  Google Scholar 

  15. Watterson, G. A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256–276 (1975)

    MathSciNet  CAS  Article  Google Scholar 

  16. Wakeley, J. & Takahashi, T. Gene genealogies when the sample size exceeds the effective size of the population. Mol. Biol. Evol. 20, 208–213 (2003)

    CAS  Article  Google Scholar 

  17. Cho, J. C. & Tiedje, J. M. Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl. Environ. Microbiol. 66, 5448–5456 (2000)

    CAS  Article  Google Scholar 

  18. Watterson, G. A. Mutant substitutions at linked nucleotide sites. Adv. Appl. Prob. 14, 206–224 (1982)

    MathSciNet  Article  Google Scholar 

  19. Nei, M. Molecular Evolutionary Genetics (Columbia University Press, New York, 1987)

    Google Scholar 

  20. Irwin, D. E. Phylogeographic breaks without geographic barriers to gene flow. Evolution 56, 2383–2394 (2002)

    Article  Google Scholar 

  21. Hewitt, G. M. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913 (2000)

    ADS  CAS  Article  Google Scholar 

  22. Willis, K. J. & Whittaker, R. J. The refugial debate. Science 287, 1406–1407 (2000)

    CAS  Article  Google Scholar 

  23. Cann, R. Genetic clues to dispersal in human populations: retracing the past from the present. Science 291, 1742–1748 (2001)

    ADS  CAS  Article  Google Scholar 

  24. Finlay, B. J. Global dispersal of free-living microbial eukaryote species. Science 296, 1061–1063 (2002)

    ADS  CAS  Article  Google Scholar 

  25. Whitaker, R. J., Grogan, D. W. & Taylor, J. W. Geographic barriers isolate endemic populations of hyperthermophilic archea. Science 301, 976–978 (2003)

    ADS  CAS  Article  Google Scholar 

  26. Bar-Yam, Y. Multi-scale variety in complex systems. Complexity 9, 37–45 (2004)

    MathSciNet  Article  Google Scholar 

  27. Crozier, R. H. Preserving the information content of species: genetic diversity, phylogeny, and conservation worth. Annu. Rev. Ecol. Syst. 28, 243–268 (1997)

    Article  Google Scholar 

  28. Moritz, C. Defining evolutionarily significant units for conservation. Trends Ecol. Evol. 9, 373–375 (1994)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was funded in part by the National Science Foundation. We are indebted to S. Hubbell, S. Pimm, J. Wakeley, M. Kardar and C. Goodnight for comments. We thank J.-C. Cho and J. Tiedje for comments and for providing the original figure with data from ref. 17.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erik M. Rauch.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Rauch, E., Bar-Yam, Y. Theory predicts the uneven distribution of genetic diversity within species. Nature 431, 449–452 (2004). https://doi.org/10.1038/nature02745

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02745

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