Letter | Published:

Comparative population genomics in animals uncovers the determinants of genetic diversity

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

Abstract

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

  • Corrected online 12 November 2014

    A minor change was made to the author affiliations.

Accessions

Primary accessions

Sequence Read Archive

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Acknowledgements

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

Affiliations

  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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Contributions

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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    This file contains additional theoretical developments and modelling.

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DOI

https://doi.org/10.1038/nature13685

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