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Comparative population genomics in animals uncovers the determinants of genetic diversity

Nature volume 515, pages 261263 (13 November 2014) | Download Citation

This article has been updated


Genetic diversity is the amount of variation observed between DNA sequences from distinct individuals of a given species. This pivotal concept of population genetics has implications for species health, domestication, management and conservation. Levels of genetic diversity seem to vary greatly in natural populations and species, but the determinants of this variation, and particularly the relative influences of species biology and ecology versus population history, are still largely mysterious1,2. Here we show that the diversity of a species is predictable, and is determined in the first place by its ecological strategy. We investigated the genome-wide diversity of 76 non-model animal species by sequencing the transcriptome of two to ten individuals in each species. The distribution of genetic diversity between species revealed no detectable influence of geographic range or invasive status but was accurately predicted by key species traits related to parental investment: long-lived or low-fecundity species with brooding ability were genetically less diverse than short-lived or highly fecund ones. Our analysis demonstrates the influence of long-term life-history strategies on species response to short-term environmental perturbations, a result with immediate implications for conservation policies.

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Change history

  • 12 November 2014

    A minor change was made to the author affiliations.


Primary accessions

Sequence Read Archive


  1. 1.

    The Genetic Basis of Evolutionary Change (Columbia Univ. Press, 1974)

  2. 2.

    et al. Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol. 10, e1001388 (2012)

  3. 3.

    & Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 19–23 (2002)

  4. 4.

    , , & Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl Acad. Sci. USA 102, 2826–2831 (2005)

  5. 5.

    , , , & Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623 (2008)

  6. 6.

    et al. Genetic restoration of the Florida panther. Science 329, 1641–1645 (2010)

  7. 7.

    Conservation genomics. Proc. Natl Acad. Sci. USA 111, 569 (2014)

  8. 8.

    , & Population size does not influence mitochondrial genetic diversity in animals. Science 312, 570–572 (2006)

  9. 9.

    , , , & Determination of mitochondrial genetic diversity in mammals. Genetics 178, 351–361 (2008)

  10. 10.

    et al. Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Res. 22, 602–610 (2012)

  11. 11.

    et al. How does ecological disturbance influence genetic diversity? Trends Ecol. Evol. 28, 670–679 (2013)

  12. 12.

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

  13. 13.

    Genome sequencing and population genomics in non-model organisms. Trends Ecol. Evol. 29, 51–63 (2014)

  14. 14.

    et al. Reference-free transcriptome assembly in non-model animals from next-generation sequencing data. Mol. Ecol. Resources 12, 834–845 (2012)

  15. 15.

    , & The population genomics of a fast evolver: high levels of diversity, functional constraint, and molecular adaptation in the tunicate Ciona intestinalis. Genome Biol. Evol. 4, 740–749 (2012)

  16. 16.

    et al. Reference-free population genomics from next-generation transcriptome data and the vertebrate-invertebrate gap. PLoS Genet. 9, e1003457 (2013)

  17. 17.

    & The Theory of Island Biogeography (Princeton Univ. Press, 1967)

  18. 18.

    Evolution of the mutation rate. Trends Genet. 26, 345–352 (2010)

  19. 19.

    Slightly deleterious mutant substitutions in evolution. Nature 246, 96–98 (1973)

  20. 20.

    et al. Unexpected patterns of fisheries collapse in the world’s oceans. Proc. Natl Acad. Sci. USA 108, 8317–8322 (2011)

  21. 21.

    et al. Next-generation sequencing of transcriptomes: a guide to RNA isolation in non-model animals. Mol. Ecol. Resources 11, 650–661 (2011)

  22. 22.

    et al. Bio++: efficient, extensible libraries and tools for molecular evolution. Mol. Biol. Evol. 30, 1745–1750 (2013)

  23. 23.

    & Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984)

  24. 24.

    et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706–712 (2009)

  25. 25.

    , & Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98, 189–197 (2007)

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We thank the following for providing samples: F. Delsuc, E. Douzery, M. Tilak, G. Dugas, S. Harispe, C. Benoist, D. Bouchon (woodlice), J. Bierne, M. Bierne, B. Houseaux, M. Strand, C. Lemaire, D. Lallias, Service Modèle Biologique Station Marine Roscoff (nemertines), X. Turon, S. Lopez-Legentil (Cystodytes), P. Jarne, P. David, R. Dillon, J. Auld, R. Relyea, C. Lively, J. Jokela, V. Poullain, T. Stewart (snails), S. Lapègue, V. Boulo, F. Batista, D. Lallias, L. Fast Jensen, M. Cantou (oysters), J. Do Nascimento, C. Daguin-Thiébaut, M. Cantou (crabs), L. Bonnaud (cuttlefish), D. Aurelle (gorgonians), F. Viard, Y. Pechenik, A. Cahill, R. Colins (slipper limpets), L. Dupont (earthworms), D. Jollivet (trumpet worms), M. A. Felix, I. Nuez (nematodes), N. Rodes, T. Lenormand, E. Flaven (brine shrimps), Rotterdam Zoo, Zurich Zoo, C. Libert, Montpellier Zoo, S. Martin, la Ferme aux Crocodiles, O. Verneau, C. Ayres, M. Carretero, M. Vanberger, K. Pobolsaj, M. Zuffi, C. Palacios, L. du Preez, B. Halpern, Budapest Zoo (turtles), P. Peret, C. Doutrelant, B. Halpern, B. Rosivall (tits), M. de Dinechin, B. Rey (penguins), Z. Melo-Fereira, P. Alves (hares), N. Brand, M. Chapuisat (bees), R. Blatrix, A. Lenoir, I. Nodet, A. Lugagne, S. Blanquart, L. Serres-Giardi, V. Roustang, N. François, G. Ballantyne, A. Carbonnel, Y. Samuel, G. James, G. Kalytta, F. Guerrini, S. Stenzel, J. Beekman, X. Cerda, S. Ikoen (ants), I. Hanski, S. Ikonen, J. Kullberg, Z. Kolev (fritillary butterflies), F. Viard, X. Turon, Di Jiang, D. Chourrout, B. Vercaemer, E. Newman-Smith, Ascidian Stock Center, Service Modèle Biologique Station Marine Roscoff (ciona), L. Excoffier, G. Heckel (voles), F. Dedeine (termites), C. Atyame, O. Duron, M. Weill (mosquitoes), M. Cantou, H. Violette, F. Batista, J. Hondeville (seahorses), C. Fraïsse, G. Pogson, N. Saarman, J. Normand (mussels), E. Poulin, C. Gonzalez-Weivar, and J. P. Feral (sea urchins). This work was supported by European Research Council advanced grant 232971 (PopPhyl).

Author information


  1. UMR 5554, Institute of Evolutionary Sciences, University Montpellier 2, Centre national de la recherche scientifique, Place E. Bataillon, 34095 Montpellier, France

    • J. Romiguier
    • , P. Gayral
    • , M. Ballenghien
    • , A. Bernard
    • , V. Cahais
    • , R. Dernat
    • , N. Faivre
    • , E. Loire
    • , J. M. Lourenco
    • , B. Nabholz
    • , C. Roux
    • , G. Tsagkogeorga
    • , L. A. Weinert
    • , K. Belkhir
    • , N. Bierne
    • , S. Glémin
    •  & N. Galtier
  2. Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland

    • J. Romiguier
    •  & C. Roux
  3. UMR 7261, Institut de Recherches sur la Biologie de l’Insecte, Centre national de la recherche scientifique, Université François-Rabelais, 37200 Tours, France

    • P. Gayral
  4. Aix-Marseille Université, Institut Méditerranéen de Biodiversité et d’Écologie marine et continentale (IMBE) – CNRS – IRD – UAPV, 13007 Marseille, France

    • A. Chenuil
    •  & A. A.-T. Weber
  5. Department of Biology, University of South Alabama, Mobile, Alabama 36688-0002, USA

    • Y. Chiari
  6. UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, Université Lyon 1, CNRS, 69622 Lyon, France

    • L. Duret
  7. The School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK

    • G. Tsagkogeorga
  8. Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 0ES, UK

    • L. A. Weinert


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N.G. conceived the project. P.G., M.B., N.F., Y.C., L.A.W., G.T., A.C., A.W., J.R., N.G. and N.B. performed sampling and laboratory work. A.B., V.C., E.L., J.R., J.M.L., C.R., P.G., G.T., B.N., R.D., K.B., S.G. and N.G. developed the data analysis pipeline. J.R. collected life-history/geographic variables and produced figures. J.R., A.B., V.C., L.D., E.L. and N.G. analysed the data. S.G., N.B., B.N., J.R. and N.G. provided interpretations and models. J.R., N.B., S.G. and N.G. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to N. Galtier.

Data sets are freely available from the Sequence Read Archive (SRA) database (http://www.ncbi.nlm.nih.gov/sra) under project ID SRP042651 and from the Datasets section of the PopPhyl website (http://kimura.univ-montp2.fr/PopPhyl), in which predicted single nucleotide polymorphisms and genotypes are provided as .vcf files. Scripts and executable files are freely available from the Tools section of the PopPhyl website.

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