Conservation Genetics

, 7:303 | Cite as

Estimating effective population size from linkage disequilibrium: severe bias in small samples

  • Phillip R. EnglandEmail author
  • Jean-Marie Cornuet
  • Pierre Berthier
  • David A. Tallmon
  • Gordon Luikart


Effective population size (N e) is a central concept in evolutionary biology and conservation genetics. It predicts rates of loss of neutral genetic variation, fixation of deleterious and favourable alleles, and the increase of inbreeding experienced by a population. A method exists for the estimation of N e from the observed linkage disequilibrium between unlinked loci in a population sample. While an increasing number of studies have applied this method in natural and managed populations, its reliability has not yet been evaluated. We developed a computer program to calculate this estimator of N e using the most widely used linkage disequilibrium algorithm and used simulations to show that this estimator is strongly biased when the sample size is small (<‰100) and below the true N e. This is probably due to the linkage disequilibrium generated by the sampling process itself and the inadequate correction for this phenomenon in the method. Results suggest that N e estimates derived using this method should be regarded with caution in many cases. To improve the method’s reliability and usefulness we propose a way to determine whether a given sample size exceeds the population N e and can therefore be used for the computation of an unbiased estimate.


effective population size linkage disequilibrium sampling bias 



PRE was supported by an Australian Postdoctoral Fellowship, a Région Bourgogne Fellowship and the European Union Econogene project. Andrea Taylor kindly provided northern hairy-nosed wombat microsatellite genotypes. PRE, JMC and GL were supported by the Bureau des Ressources Génétiques. GL also received support from the Division of Biological Sciences at University of Montana.


  1. Ardren WR, Kapuscinski AR (2003) Demographic and genetic estimates of effective population size (N e) reveals genetic compensation in steelhead trout. Mol. Ecol. 12: 35–49CrossRefPubMedGoogle Scholar
  2. Balloux F (1999) EASYPOP, a software for population genetics simulation. ( Institute of Ecology, University of Lausanne, Switzerland
  3. Bartley D, Bagley M, Gall G, Bentley B (1992) Use of linkage disequilibrium data to estimate effective size of hatchery and natural fish populations. Conserv. Biol. 6: 365–375CrossRefGoogle Scholar
  4. Berthier P, Beaumont MA, Cornuet J-M, Luikart G (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: A genealogical approach. Genetics 160: 741–751PubMedGoogle Scholar
  5. Black CW, Krafsur ES (1985) A FORTRAN program for the calculation and analysis of two-locus linkage disequilibrium coefficients. Theoret. Appl. Genet. 70: 491–496CrossRefGoogle Scholar
  6. Cockerham CC, Weir BS (1977) Digenic descent measures for finite populations. Genet. Res. 30: 121–147CrossRefGoogle Scholar
  7. England PR (1998) The conservation genetics of population bottlenecks. Ph.D. thesis, Macquarie University, SydneyGoogle Scholar
  8. Frankham R (1995) Conservation Genetics. Ann. Rev. Genet. 29: 305–327CrossRefPubMedGoogle Scholar
  9. Frankham R (1996) Effective population size/adult population size ratios in wildlife: A review. Genet. Res., Camb. 66: 95–107Google Scholar
  10. Garnier-Gere P, Dillmann C (1992) A computer program for testing pairwise linkage disequilibria in subdivided populations. J. Hered. 83: 239PubMedGoogle Scholar
  11. Harris RB, Allendorf FW (1989) Genetically effective population size of large mammals: An assessment of estimators. Conserv. Biol. 3: 181–191CrossRefGoogle Scholar
  12. Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet. Res., Camb. 38: 209–216Google Scholar
  13. Luikart G, J-M Cornuet, Allendorf FW (1999). Temporal changes in allele frequencies provide estimates of population bottleneck size. Conserv. Biol. 13: 523–530CrossRefGoogle Scholar
  14. Mace GH, Lande R (1991) Assessing extinction threats: Towards an evaluation of IUCN threatened species categories. Conserv. Biol. 5: 148–157CrossRefGoogle Scholar
  15. Raymond M, Rousset F (1995) GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 86: 248–249Google Scholar
  16. Schlotterer C (2004) The evolution of molecular markers. Nat. Rev. Genet. 5: 63–69CrossRefPubMedGoogle Scholar
  17. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol. Evol. 15: 199–203CrossRefPubMedGoogle Scholar
  18. Taylor AC, Sherwin WB, Wayne RK (1994) Genetic variation of microsatellite loci in a bottlenecked species: The northern hairy-nosed wombat Lasiorhinus krefftii. Mol. Ecol. 3: 277–290PubMedCrossRefGoogle Scholar
  19. Waples RS (1991) Genetic methods for estimating effective population size of Cetacean populations. In Genetic Ecology of Whales and Dolphins (ed. Hoelzel AR), pp. 279–300. International Whaling Commission, Special Issue 13, CambridgeGoogle Scholar
  20. Weir B (1979) Inferences about linkage disequilibrium. Biometrics 35: 235–254PubMedCrossRefGoogle Scholar
  21. Wright S (1931) Evolution in Mendelian populations. Genetics 16: 97–159PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Phillip R. England
    • 1
    Email author
  • Jean-Marie Cornuet
    • 2
  • Pierre Berthier
    • 3
  • David A. Tallmon
    • 4
  • Gordon Luikart
    • 5
    • 6
  1. 1.CSIRO Division of Marine & Atmospheric ResearchWembleyAustralia
  2. 2.Centre de Biologie et de Gestion des PopulationsSaint Gely du FescFrance
  3. 3.Populations genetik, Zoologisches InstitutUniversität BernBernSwitzerland
  4. 4.Biology ProgramUniversity of Alaska SoutheastJuneauUSA
  5. 5.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  6. 6.Centro de Investigação em Biodiversidade e␣Recursos Geneticos (CIBIO-UP)Universidade do PortoVairaoPortugal

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