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Abstract

The adaptation of natural populations to changing environments is often driven by numerous genetic loci predominantly found in non-coding regions with likely gene regulatory roles. Using adaptively diverging marine and freshwater stickleback fish ecotypes as a model, we quantified the degree to which cis- and trans- acting factors underlie expression divergence with allele-specific gene expression assays. Finding a major role for cis-regulatory differences compared to trans-regulatory differences, we next performed comparative epigenomics, chromatin profiling, transcriptomics and genetics to identify thousands of cis- regulatory elements with divergent epigenomic profiles between the ecotypes. Divergent elements are enriched at the promoter and 5’UTR of genes, are proximal to genes showing differential expression, and vary across tissues, with the liver showing considerably higher regulatory divergence than kidney or gills. Allele-specific analyses in F1 hybrids reveals that divergence in chromatin accessibility is itself mostly cis-regulated and these elements show molecular signatures of natural selection. Additionally, forward genetic mapping of chromatin variation identifies QTLs located on the same chromosome as each of the divergent chromatin peaks, and finds little evidence for trans-acting factors controlling differences in chromatin accessibility and regulatory genome function. The high resolution maps of the chromatin and epigenomic landscape in diverging stickleback ecotypes provides functional annotation of regulatory elements within adaptive loci. Combined, our studies show overwhelming evidence for the major role of cis-regulation of the regulatory genome and gene expression in the adaptive divergence of marine and freshwater stickleback in the early stages of speciation.