Hybridization and incomplete lineage sorting characterize the evolutionary history of two East Asian clades of Stewartia (Theaceae)

Abstract

Reticulate evolution and recalcitrant phylogenetic relationships are common in the East Asian evergreen broad-leaved forests (EA-EBLFs),. Hybridization and incomplete lineage sorting (ILS) can both occur during diversification of these forests, yet the extent of ILS has often been overlooked. Among floristic elements in the EA-EBLFs, plant genera that are disjunctly distributed between eastern Asia and eastern North America (EA-ENA disjuncts) provide an excellent system to explore the magnitude of hybridization and ILS after vicariance and long-distance dispersal. Here, we investigated the evolutionary history of Stewartia L. (Theaceae), one of the EA-ENA disjuncts whose major members inhabit the EA-EBLFs (ca. 20 spp. in EA vs. two spp. in ENA) using target enrichment sequence data obtained from Angiosperms353. Based on nearly complete taxon sampling, we recovered two Stewartia clades (the EA deciduous and evergreen clades) in the EA-EBLFs. Our estimates indicate that these two clades started to diversify in the late Miocene, and the evergreen clade showed a higher diversification rate than the deciduous clade. The SNaQ and NANUQ analyses detected hybridization signals within both clades, primarily involving S. serrata and S. tonkinensis, respectively. In addition, the QuIBL analysis revealed co-occurring introgression and ILS in 98/105 and 318/360 tested triplets (Δ BIC < − 10) in the deciduous and evergreen clades, respectively. The Phytop analysis further supported ILS as the primary source of gene-tree discordance. Our study reveals complex phylogenetic and evolutionary patterns in EA-EBLF endemics and highlights the importance of hybridization and ILS in this region.