Comparative population genomics in animals uncovers the determinants of genetic diversity

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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Primary accessions

Sequence Read Archive

Change history

  • 12 November 2014

    A minor change was made to the author affiliations.

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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).

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Authors

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

This file contains additional theoretical developments and modelling. (PDF 810 kb)

Supplementary Data

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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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