Accurately Inferring Ancient Auto and Allopolyploidization Events using Forward-time Simulations

Abstract

Multiple rounds of whole-genome duplication (WGD) followed by diploidization have occurred throughout the evolutionary history of angiosperms. To understand how these cycles occur, much work has been done to model the genomic consequences and evolutionary significance of WGD. The machinations of diploidization are strongly influenced by the mode of speciation (allo or autopolyploidy). However, there is no discrete boundary between allo and autopolyploidy, which is best described as a continuum. Here we present a forward-time polyploid genome evolution simulator called SpecKS. SpecKS models polyploid speciation as originating from a 2D continuum, whose dimensions account for both the level of genetic differentiation between the ancestral parental genomes, as well the time lag between ancestral speciation and their subsequent reunion in the derived polyploid. Using extensive simulations, we demonstrate that changes in initial conditions along either dimension of the 2D continuum deterministically affect the shape of the Ks histogram. Our findings indicate that the error in the common method of estimating WGD time from the Ks histogram peak scales with the degree of allopolyploidy, and we present an alternative, accurate estimation method that is independent of the degree of allopolyploidy. Lastly, we use SpecKS to derive tests that infer both the lag time between parental divergence and WGD time, and the diversity of the ancestral species, from an input Ks histogram. We apply the latter test to transcriptomic data from over 200 species across the plant kingdom, the results of which are concordant with the prevailing theory that the majority of angiosperm lineages are derived from diverse parental genomes and may be of allopolyploid origin.