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Long-read genome assemblies reveals a cis-regulatory landscape associated with phenotypic divergence in two sister Siniperca fishes

Background Dissecting the genetic basis of variation in the regulation of gene expression is essential for understanding phenotypic evolution. Structural variants intersecting the cis-regulatory elements are found to cause gene expression variation in several developmental genes, resulting in morphological divergence between species. Due to the difficulty of identifying structural variants accurately across the genome, a comprehensive study of impacts of structural variants in cis-regulatory divergence of closely related species, especially fish species, is still scarce. Recently identified broad H3K4me3 domains are essential for the regulation of genes involved in several biological processes. However, the role of broad H3K4me3 domains in phenotypic divergence remain poorly understood. Siniperca chuatsi and S. scherzeri are two closely related fish species diverge in several phenotypic traits, making them an ideal model to study cis-regulatory evolution in closely related species. Results We generated chromosome-level genomes of S. chuatsi and S. scherzeri. The evolutionary histories of S. chuatsi and S. scherzeri were studied by inferring the dynamic changes in the ancestral population sizes. The genetic basis of adaptation in S. chuatsi and S. scherzeri was dissected by performing gene family expansion and contraction analysis and identifying positively selected genes (PSGs). To investigate the role of SVs in cis-regulatory divergence of closely related fish species, we identified high-quality SVs between S. chuatsi and S. scherzeri, as well as H3K27ac and H3K4me3 domains. Integrated analysis revealed that cis-regulatory divergence caused by SVs played an essential role in the differentiation of metabolism, skin pigmentation, and immunity between S. chuatsi and S. scherzeri. Additionally, divergent broad H3K4me3 domains were found to mostly associate with cancer-related genes in S. chuatsi and S. scherzeri and contribute to their phenotypic divergence. Conclusions Our analysis reveals SVs play an essential role in cis-regulatory variation between the two sister fish species, which in turn contributes to their phenotypic divergence. The divergence of broad H3K4me3 domains contributes to phenotypic divergence between closely related species. Additionally, the association of broad H3K4me3 domains and cancer-related genes has an ancient origin.