Reappraising the role of whole genome duplication and rediploidisation in eukaryotic evolution

Background:

Whole genome duplication (WGD) is a dramatic inherited mutation where all the DNA in each cell (the genome) is doubled. WGD events occurred at critical points in evolution and may have promoted the success of major eukaryotic groups, including flowering plants and vertebrates. Identifying WGD events and revealing how they lead to new gene functions is important to understand how life diversified and became more complex.

 

The significance of WGD lies in the generation of new genes with untapped functional potential. However, after many WGD events the duplicated genes are identical and cannot contribute new functions until DNA sequence divergence takes place. Genetic and physical features of chromosome biology preclude this divergence from occurring until the duplicated chromosomes assume separate identities - a multifaceted process called ‘rediploidisation’, which is integral to unlocking the evolutionary potential of WGD. WGD has been studied for decades, but rediploidisation remains poorly understood in most study systems where WGD events have been characterised. 

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This project is founded on new discoveries that demand a rethink about evolution following WGD. It was recently shown that the duplicated DNA sequences created by three different WGD events in vertebrate evolution diverged at very different times in different parts of the genome because rediploidisation was highly asynchronous (Robertson et al. 2017; Parey et al. 2022; Redmond et al. 2023). Remarkably, large duplicated regions in the genome sequence remained identical (tetraploid) across tens of millions of years.

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In many cases it has been shown that duplicate genes start diverging across the genome soon after a WGD event. Consequently, it is often assumed that maximal evolutionary potential should closely follow WGD - predicting an early ‘explosion’ of biological novelty. However, when duplicate genes diverge asynchronously, biological innovations born from WGD could emerge over longer time-periods, and even independently in species separated by tens of millions of years of evolution. This radically changes understanding of the diversification processes that follow WGD. Additionally, widely used methods to detect when and where WGD events occurred have largely ignored asynchronous rediploidisation, which may have impacted past conclusions in the field.