Evolutionary origin and establishment of a dioecious diploid-tetraploid complex

Polyploids recurrently emerge in angiosperms, but most polyploids are likely to go extinct before establishment due to minority cytotype exclusion, which may be specifically a constraint for dioecious plants. Here we test the hypothesis that a stable sex-determination system and spatial/ecological isolation facilitate the establishment of dioecious polyploids. We determined the ploidy levels of 351 individuals from 28 populations of the dioecious species Salix polyclona, and resequenced 190 individuals of S. polyclona and related taxa for genomic diversity analyses. The ploidy survey revealed a frequency 52% of tetraploids in S. polyclona, and genomic k-mer spectra analyses suggested an autopolyploid origin for them. Comparisons of diploid male and female genomes identified a female heterogametic sex-determining factor on chromosome 15, which probably also acts in the dioecious tetraploids. Phylogenetic analyses revealed two diploid clades and a separate clade/grade of tetraploids with a distinct geographic distribution confined to western and central China, where complex mountain systems create higher levels of environmental heterogeneity. Fossil-calibrated phylogenies showed that the polyploids emerged during 7.6-2.3 million years ago, and population demographic histories largely matched the geological and climatic history of the region. Our results suggest that inheritance of the sex-determining system from the diploid progenitor as intrinsic factor and spatial isolation as extrinsic factor may have facilitated the preservation and establishment of polyploid dioecious populations.

Automated summary

We tested the role of stable sex-determination system and spatial/ecological isolation in the establishment of polyploid dioecious plants. Our study focused on the dioecious species Salix polyclona and revealed that 52% of individuals were tetraploids with an autopolyploid origin. Phylogenetic analysis showed that tetraploids had a distinct geographic distribution in western and central China. The inheritance of the sex-determining system from diploid progenitors as an intrinsic factor and spatial isolation as an extrinsic factor may have facilitated the preservation and establishment of polyploid dioecious populations.