Reticulate evolution, introgression, and recent diversification in Epimedium sect. Macroceras

Hybridization can hinder or promote diversification, and growing genomic evidence suggests that it can facilitate adaptation and speciation. Despite recent progress, however, the quantitative contribution and temporal scope of hybridization to diversification remain poorly understood. The genus Epimedium is a recently diverged lineage, and sect. Macroceras largely consists of endemic species in Japan that are distributed across diverse environments, including limestone, serpentine, coastal habitats, heavy-snow regions, and regions with mild winters. Although natural hybridization and hybrid species have been reported in this section, molecular evidence demonstrating the contribution of hybridization to lineage diversification is limited. We reconstructed phylogenetic relationships using genome-wide single-nucleotide polymorphism (SNP) data from Epimedium sect. Macroceras and tested for genomic signatures consistent with hybridization. Phylogenetic analyses suggest that E. koreanum from Korea is sister to Japanese Epimedium lineages, consistent with an initial colonization of Japan from the Korean Peninsula. The analyses also revealed complex relationships among Japanese species and frequent signals of historical interspecific introgression. Our results are consistent with a history of recent diversification in sect. Macroceras accompanied by introgressive hybridization, which may have contributed to diversification across heterogeneous environments in Japan. This study provides the first genome-wide insights into the evolutionary history of Epimedium sect. Macroceras and reveals complex reticulate relationships among the lineages.