Huang Y , Feulner PGD , Eizaguirre C, Lenz TL, Bornberg-Bauer E , Milinski M, Reusch TBH, Chain FJJ
Genome-wide genotype-expression relationships reveal that copy number and single nucleotide differentiation contributes to differential gene expression between stickleback ecotypes
Genome Biology and Evolution, 2019

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Repeated and independent emergence of trait divergence that matches habitat differences is a sign of parallel evolution by natural selection. Yet, the molecular underpinnings that are targeted by adaptive evolution often remain elusive. We investigate this question by combining genome-wide analyses of copy number variants (CNVs), single nucleotide polymorphisms (SNPs), and gene expression across four pairs of lake and river populations of the three-spined stickleback (Gasterosteus aculeatus). We tested whether CNVs that span entire genes and SNPs occurring in putative cis-regulatory regions contribute to gene expression differences between sticklebacks from lake and river origins. We found gene CNVs that showed a significant positive association between gene copy number and gene expression, suggesting that CNVs result in dosage effects that can fuel phenotypic variation and serve as substrates for habitat-specific selection. Copy number differentiation between lake and river sticklebacks also contributes to expression differences of two immune-related genes in immune tissues, cathepsin A and GIMAP7. In addition, we found cis-expression quantitative trait loci (cis-eQTL) associated with 1865 genes, including one SNP upstream of a carboxypeptidase gene where both the SNP alleles differentiated and the gene was differentially expressed between lake and river populations. Our study highlights two types of mutations as important sources of genetic variation involved in the evolution of gene expression and in potentially facilitating repeated adaptation to novel environments.