Integrating morphology, ecology, and genomics: Unraveling the population genetic and evolution within the Rosa graciliflora complex

Abstract

Species delimitation in recently diverged lineages presents significant challenges in plant systematics, particularly in the genus Rosa, where recent radiation, incomplete lineage sorting, and frequent hybridization have created intricate evolutionary patterns. This study presents a comprehensive investigation of a monophyletic complex comprising R. graciliflora, R. tibetica, and R. tsinlingensis, integrating morphological, ecological, and genomic approaches. Morphological analysis of 392 specimens revealed substantial interspecific trait overlap without distinct morphological boundaries, while ecological niche analysis demonstrated significant habitat overlap, both challenging the current taxonomic classification. Phylogenetic analysis, population genetic structure analysis, and principal component analysis (PCA) based on genome-wide SNP data from 190 individuals across 26 populations did not support the monophyly of these three traditionally recognized species, indicating low genetic differentiation and extensively interwoven genetic backgrounds. Population genetic structure primarily reflected geographical distribution patterns, with genetic differentiation mainly driven by geographic distance and environmental factors. Significant gene flow was detected among adjacent populations. Selective sweep analysis identified key genes associated with flower color and flowering time. Correlation analysis suggested that solar radiation is a crucial environmental factor influencing leaflet number and flower color variation. Based on these findings, we propose treating R. tsinlingensis and R. tibetica as synonyms of R. graciliflora. Our findings underscore the limitations of morphological classification in reflecting the genetic and ecological diversity within the R. graciliflora complex, highlighting the importance of multidimensional data in understanding plant evolution and biodiversity conservation in the face of changing environments.