Abstract

BackgroundMarine 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.ResultsOur 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.ConclusionThese 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.

Highlights

  • 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

  • This study suggests that loci subject to directional selection can be found on various geographical scales in Atlantic cod

  • Genetic evidence of local adaptation at the DNA level in marine fishes has been inferred from single genes [20,44,45], or from restricted geographical areas [24]

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Summary

Introduction

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. Even though some groups of marine fishes, such as coral reef fishes, have been found to be highly genetically structured [4], more than 40 years of population genetic research has typically demonstrated low levels of genetic differentiation among local demes compared to other fish species and terrestrial organisms [5]. Genome scan approaches using a high number of genetic markers in natural populations can provide a powerful shortcut for demonstrating local selection pressures by allowing the identification of outlier loci with divergent levels of genetic differentiation [7,8]. Targeted genome scans have recently been used in natural populations of various organisms such as trees (white spruce) [10] and fish (sticklebacks) [11]

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