Inferring complex evolutionary history of the closely related East Asian wild roses in Rosa sect. Synstylae (Rosaceae) based on genomic evidence from conserved orthologues

Abstract

Background and Aims The section Synstylae in genus Rosa (Rosaceae) comprises 25–36 species and includes several major progenitors of modern rose cultivars. East Asian Synstylae species have recently diverged and are closely related, and their phylogenetic relationships remain unclear. In the present study, we employed a conserved ortholog set (COS) markers and genome-wide nuclear orthologs to elucidate their phylogenetic relationships and unravel their complex evolutionary history. Methods Utilising on eight Rosaceae COS (RosCOS) markers, we analysed a total of 137 accessions representing 15 East Asian Synstylae taxa to establish a robust phylogenetic framework and reconstruct ancestral areas. Furthermore, we constructed the species tree for eight representative species and estimated their divergence times based on 1,683 genome-wide orthologs. The species tree-gene tree coalescence time comparison, Patterson’s D, f4-ratio, and f-branch statistics were analysed to identify incomplete lineage sorting (ILS), genetic introgression, and reticulation events using conserved ortholog data. Key Results RosCOS markers and genome-wide orthologs effectively resolved the robust phylogeny of East Asian Rosa sect. Synstylae. Species divergence times estimated with genome-wide orthologs indicated that East Asian Synstylae species have recently diverged, with an estimated crown age of approximately 2 Mya. The rampant gene tree discordance indicated the possibility of ILS and/or genetic introgression. In the section Synstylae, deeper coalescence in the gene trees compared to the species tree suggested ILS as a source of gene tree discordance. Further, Patterson’s D and f-branch statistics indicated that several lineages in the section were involved in genetic introgression. Conclusions We have unravelled the complex evolutionary history of East Asian Rosa sect. Synstylae, including recent species divergences, ILS, and genetic introgression. Coupled with the geographical and ecological complexity of East Asia, ILS and genetic introgression may have contributed to the rapid diversification of East Asian Synstylae species by permitting adaptation to diverse environments.