Genomic Signatures of Selection Are Enriched in Differentially Expressed Genes in Sticklebacks Adapting to...

Whole genome scans have identified numerous adaptive alleles in many species; however, linking these alleles to specific phenotypes remains a major challenge. A promising alternative to direct genotype-phenotype mapping, particularly given the complexities introduced by epistasis, pleiotropy, and environmental variability, is to assess whether differentially expressed genes (DEGs) are enriched in regions of genetic divergence between populations adapted to contrasting environments. Here, we study gene expression patterns in threespine stickleback populations adapting to contrasting environments (marine vs. freshwater) and investigate signatures of selection associated with gene expression evolution during adaptation. We performed transcriptomic experiments of the brain and gill tissues of wild-caught sticklebacks sampled from one marine and two freshwater environments using TagSeq. We found that DEGs in the freshwater environments harbor single nucleotide polymorphisms (SNPs) previously identified to be involved in rapid adaptation and FST outliers. A majority of these SNPs were located in cis-regulatory regions of the genes with predicted low to moderate effects on protein function and structure, although we found a high-impact SNP in the gene col8a1b. Genes such as pvalb4 and acsl4a, involved in calcium regulation in the gill and fatty acid metabolism in the brain, respectively, were enriched with SNPs showing signatures of selection. By linking signatures of selection to tissue-specific gene expression patterns, our study bridges the gap between genomic divergence and the molecular mechanisms underlying physiological adaptation to new environments and identifies specific pathways that can be targeted for future functional studies.