Abstract
BackgroundThe functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification are often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 million years ago, 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, ‘lineage-specific ohnologue resolution’ (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event.ResultsUsing 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 4550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions >50 million years post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than ‘older’ ohnologues that began diverging in the salmonid ancestor.ConclusionsLORe 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 millions of years, promoting lineage-specific diversification regimes under prevailing ecological pressures.
Highlights
The functional divergence of duplicate genes retained from whole genome duplication (WGD) is thought to promote evolutionary diversification
We demonstrate that one-quarter of retained salmonid ohnologues have evolved under lineage-specific ohnologue resolution’ (LORe), which has had a major impact on salmonid fish evolution at multiple levels of genomic and functional organization
All the gene trees included verified Atlantic salmon ohnologues based on their location within duplicated blocks sharing common rediploidization histories [38]
Summary
The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. In contrast to the duplication of a single or small number of genes, WGD events are unique in allowing the balanced divergence of whole networks of ohnologues This is thought to promote molecular and phenotypic complexity through the biased retention and diversification of interactive signalling pathways, those regulating development [8,9,10]. As WGD events dramatically reshape opportunities for genomic and functional evolution, it is not surprising that an extensive body of literature has sought to identify causal associations between WGD and key episodes of evolutionary history, for example species radiations Such arguments are clearly appealing and have been constructed for WGD events ancestral to vertebrates [11,12,13,14,15], teleost fishes [16,17,18,19] and angiosperms (flowering plants) [10, 20,21,22]. Apparent robust associations between WGD and the rapid evolution of species or phenotypic-level complexity may disappear when extinct lineages are considered, as proposed for WGDs in the stem of vertebrate and teleost evolution [26, 27]
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