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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 performed comparative epigenomics, chromatin profiling, transcriptomics and genetics to identify thousands of 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 mostly cis-regulated and these elements show molecular signatures of natural selection. Additionally, divergent epigenomic marks cluster into ‘islands’ of genetic differentiation and low recombination, including chromosomal inversions. We show through functional transgenic assays how these cassettes act as hubs to cause concerted changes in gene expression between adaptively diverging populations. The high resolution maps of the chromatin and epigenomic lanscape in diverging stickleback ecotypes provides functional annotation of regulatory elements within adaptive loci. Our study shows how cis-regulated chromatin variation and epigenomic marks at regulatory elements is associated with adaptive divergence and the early stages of speciation, and links their co-inheritance as adaptive regulatory cassettes to the fast and repeated adaptive radiation of sticklebacks.