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SNP signatures of selection on standing genetic variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus spp.)

Authors

  • SÉBASTIEN RENAUT,

    1. Département de Biologie, IBIS (Institut de Biologie Intégrative et des Systèmes), Université Laval, Québec, QC, Canada G1V 0A6
    2. Department of Botany, University of British Columbia, 6270 University Blvd, Vancouver, BC, Canada V6T 1Z4
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    • These authors contributed equally to this manuscript.

  • ARNE W. NOLTE,

    1. Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Str., 2, 24306, Plön, Germany
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    • These authors contributed equally to this manuscript.

  • SEAN M. ROGERS,

    1. Department of Biological Sciences, University of Calgary, 2500 University Drive N.W. Calgary, AB, Canada T2N 1N4
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  • NICOLAS DEROME,

    1. Département de Biologie, IBIS (Institut de Biologie Intégrative et des Systèmes), Université Laval, Québec, QC, Canada G1V 0A6
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  • LOUIS BERNATCHEZ

    1. Département de Biologie, IBIS (Institut de Biologie Intégrative et des Systèmes), Université Laval, Québec, QC, Canada G1V 0A6
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Sébastien Renaut, Fax: 1 604 822 6089; E-mail: sebastien.renaut.1@ulaval.ca

Abstract

As populations adapt to novel environments, divergent selection will promote heterogeneous genomic differentiation via reductions in gene flow for loci underlying adaptive traits. Using a data set of over 100 SNP markers, genome scans were performed to investigate the effect of natural selection maintaining differentiation in five lakes harbouring sympatric pairs of normal and dwarf lake whitefish (Coregonus clupeaformis). A variable proportion of SNPs (between 0% and 12%) was identified as outliers, which corroborated the predicted intensity of competitive interactions unique to each lake. Moreover, strong reduction in heterozygosity was typically observed for outlier loci in dwarf but not in normal whitefish, indicating that directional selection has been acting on standing genetic variation more intensively in dwarf whitefish. SNP associations in backcross hybrid progeny identified 16 genes exhibiting genotype–phenotype associations for four adaptive traits (growth, swimming activity, gill rakers and condition factor). However, neither simple relationship between elevated levels of genetic differentiation with adaptive phenotype nor conspicuous genetic signatures for parallelism at outlier loci were detected, which underscores the importance of independent evolution among lakes. The integration of phenotypic, transcriptomic and functional genomic information identified two candidate genes (sodium potassium ATPase and triosephosphate isomerase) involved in the recent ecological divergence of lake whitefish. Finally, the identification of several markers under divergent selection suggests that many genes, in an environment-specific manner, are recruited by selection and ultimately contributed to the repeated ecological speciation of a dwarf phenotype.

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