Abstract
Whole-genome duplications (WGD) have been considered as springboards that potentiate lineage diversification through increasing functional redundancy. Divergence in gene regulatory elements is a central mechanism for evolutionary diversification, yet the patterns and processes governing regulatory divergence following events that lead to massive functional redundancy, such as WGD, remain largely unknown. We studied the patterns of divergence and strength of natural selection on regulatory elements in the Atlantic salmon (Salmo salar) genome, which has undergone WGD 100–80 Ma. Using ChIPmentation, we first show that H3K27ac, a histone modification typical to enhancers and promoters, is associated with genic regions, tissue-specific transcription factor binding motifs, and with gene transcription levels in immature testes. Divergence in transcription between duplicated genes from WGD (ohnologs) correlated with difference in the number of proximal regulatory elements, but not with promoter elements, suggesting that functional divergence between ohnologs after WGD is mainly driven by enhancers. By comparing H3K27ac regions between duplicated genome blocks, we further show that a longer polyploid state post-WGD has constrained regulatory divergence. Patterns of genetic diversity across natural populations inferred from resequencing indicate that recent evolutionary pressures on H3K27ac regions are dominated by largely neutral evolution. In sum, our results suggest that post-WGD functional redundancy in regulatory elements continues to have an impact on the evolution of the salmon genome, promoting largely neutral evolution of regulatory elements despite their association with transcription levels. These results highlight a case where genome-wide regulatory evolution following an ancient WGD is dominated by genetic drift.
Highlights
Numerous evolutionary innovations have taken place in conjunction with, or following, large-scale genomic rearrangements such as whole-genome duplications (WGD) (Vandepoele et al 2004; Peer et al 2009; Macqueen and Johnston 2014), which create massive functional redundancy of genes and regulatory elements
By investigating regulatory elements in the Atlantic salmon genome, which has undergone a whole-genome duplication 100–80 Ma, we discovered patterns suggesting that neutral divergence is the prevalent mode of regulatory element evolution post-WGD
To further determine whether the H3K27 acetylation (H3K27ac) peaks were associated with regulatory activity, and represented true gene regulatory elements, we investigated peaks in conjunction with expression levels of genes in immature testis RNA-seq data
Summary
Numerous evolutionary innovations have taken place in conjunction with, or following, large-scale genomic rearrangements such as whole-genome duplications (WGD) (Vandepoele et al 2004; Peer et al 2009; Macqueen and Johnston 2014), which create massive functional redundancy of genes and regulatory elements. Gene expression levels and patterns in metazoan genomes are controlled by enhancer and promoter sequences commonly referred to as regulatory elements (Long et al 2016). Regulation of mammalian gene expression is putatively controlled by hundreds of thousands of regulatory elements (Villar et al 2014; Gasperini et al 2020), their number greatly exceeding the typical number of genes. Through their combined and individual function, regulatory elements have long been hypothesized to significantly contribute to evolutionary change and adaptation (King and Wilson 1975; Stern and Orgogozo 2008)
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