Developmental contexts of gene-regulatory evolution following whole genome duplication in salmonids.

Abstract

Whole genome duplication (WGD) events during early vertebrate evolution may have promoted phenotypic innovation by expanding the genetic material for functional diversification. However, their ancient origins obscure how gene regulation evolved during rediploidization, the process that generates duplicate genes and regulatory elements following WGD. Salmonids provide a unique window to these mechanisms, because they experienced a more recent autotetraploid WGD and remain at an earlier stage of rediploidization. Here we generated 771 multiomics datasets spanning embryonic and adult tissues in Atlantic salmon and rainbow trout to investigate the evolution of gene expression and regulatory elements. Our analyses show that regulatory evolution following the salmonid WGD was shaped by developmental and tissue-specific constraints known to act across vertebrate species. We identify a peak of within-genome regulatory constraint at the vertebrate phylotypic period, associated with the functional retention of duplicated enhancer pairs harbouring deeply conserved non-coding elements enriched in motifs for master developmental transcription factors. We further identify roles for enhancers and transposable elements in the expression divergence of duplicated genes. This study advances the understanding of regulatory evolution following WGD and offers an open resource supporting vertebrate comparative genomics and research applications in salmonid aquaculture and conservation.