Chromatin Accessibility Reveals Adaptive Regulatory Variation in a Keystone Freshwater Fish

Abstract

Regulatory variation is increasingly recognized as a major driver of adaptive evolution, yet its role in natural populations remains largely unresolved. By integrating ATAC-seq chromatin profiles with population genomic outlier scans and RNA-seq gene expression data, we characterize the functional impact of regulatory elements and identify candidate loci where selection signatures coincide with tissue-specific chromatin and transcriptional shifts. We mapped genome-wide chromatin accessibility in three tissues (eye, liver and spleen) of wild European perch (Perca fluviatilis) inhabiting contrasting humic- (dark-water) and clear-water lakes. We identified over 76,000 accessible chromatin regions spanning 36.1 Mb of the genome, which were enriched for gene functions related to vision, metabolism and immune response. Chromatin landscapes were strongly tissue-specific, while only a subset of regions (0.32%, n = 161) showed differential accessibility between environments, suggesting that the regulatory architecture is dominated by tissue identity rather than environmental context. Integrating population genomic outlier scans with chromatin profiles revealed significant enrichment of adaptive SNPs within common open chromatin regions (1.5-fold) and transcription start sites (1.7-fold), directly implicating cis-regulatory elements as frequent targets of natural selection. This study demonstrates that humic adaptation in perch targets specific regulatory regions readily identified by the ATAC-seq approach, highlighting the value of functional chromatin maps in evolutionary genomics. Together, our results provide one of the first genome-wide regulatory maps for a wild vertebrate and establish a functional framework for connecting natural selection to regulatory mechanisms in the wild.