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Comparative population genomics in animals uncovers the determinants of genetic diversity

Nature volume 515, pages 261–263 (2014)Cite this article

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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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Figure 1: Genome-wide genetic diversity across the metazoan tree of life.
Figure 2: Life-history traits and genetic diversity relationships.

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  • 12 November 2014

    A minor change was made to the author affiliations.

References

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Keller, L. F. & Waller, D. M. Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 19–23 (2002)

    Google Scholar 

  4. Reusch, T. B. H., Ehlers, A., Hämmerli, A. & Worm, B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl Acad. Sci. USA 102, 2826–2831 (2005)

    Article  ADS  CAS  Google Scholar 

  5. Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623 (2008)

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. Bazin, E., Glémin, S. & Galtier, N. Population size does not influence mitochondrial genetic diversity in animals. Science 312, 570–572 (2006)

    Article  ADS  CAS  Google Scholar 

  9. Nabholz, B., Mauffrey, J.-F., Bazin, E., Galtier, N. & Glemin, S. Determination of mitochondrial genetic diversity in mammals. Genetics 178, 351–361 (2008)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  15. Tsagkogeorga, G., Cahais, V. & Galtier, N. 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)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967)

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  23. Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984)

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Wilfert, L., Gadau, J. & Schmid-Hempel, P. Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98, 189–197 (2007)

    Article  CAS  Google Scholar 

Download references

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

Authors and 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, 36688-0002, Alabama, 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

Authors
  1. J. Romiguier
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  2. P. Gayral
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  3. M. Ballenghien
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  4. A. Bernard
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  6. A. Chenuil
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  10. N. Faivre
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  21. N. Galtier
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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.

Corresponding author

Correspondence to N. Galtier.

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Competing interests

The authors declare no competing financial interests.

Additional information

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.

Extended data figures and tables

Extended Data Figure 1 Phylogenetic tree of metazoan orders and the position of the taxa analysed in this study.

The tree topology is consistent with the NCBI taxonomy. Red arrows identify 25 orders that were sampled. Five gastropod species from two distinct families (Calyptraeidae (Crepidula fornicata, C. plana and Bostrycapulus aculeatus) and Physidae (Physa acuta and P. gyrina)) are not represented because they lacked any assignment to an order in current taxonomy.

Extended Data Figure 2 Correlations between genetic diversity and life history variables.

Blue indicates a positive relationship, red a negative one; colour intensity is proportional to Pearson’s correlation coefficient.

Extended Data Figure 3 Family-level phylogenetic tree (31 families included).

The scale is in million years of divergence.

Extended Data Figure 4 Absence of significant correlation between species genetic diversity with individual sampling size (P = 0.47, r2 = 0.007) and locus sampling size (P = 0.78, r2 = 0.001).

Extended Data Figure 5 Relationship between the πs/propagule-size r2 and the number of sampled loci.

Extended Data Figure 6 Phylum distribution of the first BLAST hit in four representative species.

a, Common vole (Microtus arvalis). b, Glanville fritillary butterfly (Melitaea cinxia). c, Blue mussel (Mytilus edulis). d, Earthworm (Allolobophora chlorotica).

Extended Data Figure 7 Correlation between πn/πs and maximum longevity (P < 10−8, r2 = 0.54).

Only species with at least four individuals are included.

Supplementary information

Supplementary Information

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Supplementary Data

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Supplementary Data

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Supplementary Data

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Supplementary Data

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Romiguier, J., Gayral, P., Ballenghien, M. et al. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515, 261–263 (2014). https://doi.org/10.1038/nature13685

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