Origins of polyploids: an example from peonies (Paeonia) and a model for angiosperms

Abstract

The majority of tetraploid peonies are allopolyploids derived from crosses between phylogenetically distinct diploid lineages. Tetraploid Paeonia obovata was previously considered to be an autopolyploid because it is morphologically indistinguishable from the diploid of the same species. The presence of the Adh2 gene in tetraploid P. obovata but the inability to amplify the Adh2 gene from Chinese diploids of P. obovata, however, suggests that the tetraploid was not an autotetraploid derivative of the geographically adjacent diploid populations in China. The Adh gene phylogenies rather suggest that the tetraploid originated from crosses between two geographical races of diploid P. obovata distributed in China and Japan. The intermediate status of tetraploid P. obovata between auto- and allopolyploidy highlights the need for population genetic analyses of polyploid origins along the continuous range of genomic divergence. Here we present a model that describes the probabilities of polyploid formation and establishment as a function of genomic divergence between diploid progenitors. The probability of polyploid formation (P f ) is obtained from the multiplication of the probability of production of unreduced gametes (Pg) and the probability of 'hybridization' (P h ). P f stays relatively stable when the genomic divergence is low, and then decreases progressively rapidly with the increase of genomic divergence between diploid progenitors. The probability of polyploid establishment (P e ), which depends on the rate of appearance of stable beneficial gene combinations and the rate of fertility restoration, is positively correlated with the genomic divergence of diploid parents. Multiplication of P f and P e gives an overall probability of polyploid origins (P o ) that varies continuously along the genomic divergence between diploid progenitors.