Phylogenomics reveals widespread hybridization and polyploidization in Henckelia (Gesneriaceae)

Abstract

Abstract Background and Aims Hybridization has long been recognized as an important process for plant evolution and is often accompanied by polyploidization, another prominent force in generating biodiversity. Despite its pivotal importance in evolution, the actual prevalence and distribution of hybridization across the tree of life remain unclear. Methods We used whole-genome shotgun (WGS) sequencing and cytological data to investigate the evolutionary history of Henckelia, a large genus in the family Gesneriaceae with a high frequency of suspected hybridization and polyploidization events. We generated WGS sequencing data at about 10× coverage for 26 Chinese Henckelia species plus one Sri Lankan species. To untangle the hybridization history, we separately extracted whole plastomes and thousands of single-copy nuclear genes from the sequencing data, and reconstructed phylogenies based on both nuclear and plastid data. We also explored sources of both genealogical and cytonuclear conflicts and identified signals of hybridization and introgression within our phylogenomic dataset using several statistical methods. Additionally, to test the polyploidization history, we evaluated chromosome counts for 45 populations of the 27 Henckelia species studied. Key Results We obtained well-supported phylogenetic relationships using both concatenation- and coalescent-based methods. However, the nuclear phylogenies were highly inconsistent with the plastid phylogeny, and we observed intensive discordance among nuclear gene trees. Further analyses suggested that both incomplete lineage sorting and gene flow contributed to the observed cytonuclear and genealogical discordance. Our analyses of introgression and phylogenetic networks revealed a complex history of hybridization within the genus Henckelia. In addition, based on chromosome counts for 27 Henckelia species, we found independent polyploidization events occurred within Henckelia after different hybridization events. Conclusions Our findings demonstrated that hybridization and polyploidization are common in Henckelia. Furthermore, our results revealed that H. oblongifolia is not a member of the redefined Henckelia and they suggested several other taxonomic treatments in this genus.