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Open Access Highly Accessed Research article

Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua)

Einar E Nielsen1*, Jakob Hemmer-Hansen1, Nina A Poulsen12, Volker Loeschcke2, Thomas Moen3, Torild Johansen4, Christian Mittelholzer58, Geir-Lasse Taranger4, Rob Ogden6 and Gary R Carvalho7

  • * Corresponding author: Einar E Nielsen een@aqua.dtu.dk

  • † Equal contributors

Author Affiliations

1 National Institute of Aquatic Resources, Technical University of Denmark, Vejlsøvej 39, DK-8600 Silkeborg, Denmark

2 Department of Biological Sciences, Genetics and Ecology, University of Aarhus, Building 1540, Ny Munkegade, DK-8000 Aarhus C, Denmark

3 CIGENE, PO Box 5003, N-1434 Ås, Norway

4 Institute of Marine Research Tromsø, PO Box 6404, N-9294 Tromsø, Norway

5 Institute of Marine Research, PO Box 1870, Nordnes N-5817 Bergen, Norway

6 Tepnel Research Products and Services, Appleton Place, Livingston, EH54 7EZ, UK

7 Molecular Ecology & Fisheries Genetics Laboratory, School of Biological Sciences, Environment Centre Wales, Bangor University, Bangor, Gwynedd LL57 2UW, UK

8 Current address: University of Basel, Klingelbergstrasse 50/70, CH-4056 Basel, Switzerland

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BMC Evolutionary Biology 2009, 9:276  doi:10.1186/1471-2148-9-276

Published: 1 December 2009

Abstract

Background

Marine fishes have been shown to display low levels of genetic structuring and associated high levels of gene flow, suggesting shallow evolutionary trajectories and, possibly, limited or lacking adaptive divergence among local populations. We investigated variation in 98 gene-associated single nucleotide polymorphisms (SNPs) for evidence of selection in local populations of Atlantic cod (Gadus morhua L.) across the species distribution.

Results

Our global genome scan analysis identified eight outlier gene loci with very high statistical support, likely to be subject to directional selection in local demes, or closely linked to loci under selection. Likewise, on a regional south/north transect of central and eastern Atlantic populations, seven loci displayed strongly elevated levels of genetic differentiation. Selection patterns among populations appeared to be relatively widespread and complex, i.e. outlier loci were generally not only associated with one of a few divergent local populations. Even on a limited geographical scale between the proximate North Sea and Baltic Sea populations four loci displayed evidence of adaptive evolution. Temporal genome scan analysis applied to DNA from archived otoliths from a Faeroese population demonstrated stability of the intra-population variation over 24 years. An exploratory landscape genetic analysis was used to elucidate potential effects of the most likely environmental factors responsible for the signatures of local adaptation. We found that genetic variation at several of the outlier loci was better correlated with temperature and/or salinity conditions at spawning grounds at spawning time than with geographic distance per se.

Conclusion

These findings illustrate that adaptive population divergence may indeed be prevalent despite seemingly high levels of gene flow, as found in most marine fishes. Thus, results have important implications for our understanding of the interplay of evolutionary forces in general, and for the conservation of marine biodiversity under rapidly increasing evolutionary pressure from climate and fisheries induced changes in local environments.