Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification

Abstract

The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification is often highly temporally-detached from WGD. Salmonid fish, whose ancestor experienced WGD by autotetraploidization ~95 Ma (i.e. ‘Ss4R’), fit such a ‘time-lag’ model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model called ‘Lineage-specific Ohnologue Resolution’ (LORe) to address the phylogenetic and functional consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One quarter of each salmonid genome, harbouring at least 4,500 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions > 50 Myr post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that promoted salmonid species radiation. We show that LORe ohnologues are enriched for different functions than ‘older’ ohnologues that began diverging in the salmonid ancestor. LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear ‘explosively’, but can arise gradually over tens of Myr, promoting lineage-specific diversification regimes under prevailing ecological pressures.