Can plastome data resolve recent radiations?Rhodiola(Crassulaceae) as a case study

Abstract

Recent radiations provide excellent models to gain more insights into evolution, speciation and adaptation. To this end, a well-resolved phylogenetic tree is needed. However, resolving phylogenetic relationships within recent radiations has been difficult as traditional phylogenetic markers failed to provide enough information. We here use plastome data to test their capacity in resolving phylogenetic relationships among a recent rapidly diverging group, Rhodiola, on the Qinghai-Tibetan Plateau. We reconstructed a robust phylogenetic backbone of Rhodiola using 23 plastomes representing all subgenera and sections in previous taxonomic treatments. Based on the backbone, we inferred the spatio-temporal pattern of diversification of the genus. We also traced evolution of five important morphological characters of Rhodiola, including sexual system, inflorescence type and flowering stem, based on the maximum likelihood and the threshold models. Two well-supported clades were revealed in Rhodiola, and the two clades were distinguished by sexual system: species in clade I are mostly hermaphrodite (except R. stapfii and R. integrifolia), and those in clade II are all dioecious. Biogeographic analysis showed that Rhodiola probably originated in the Qinghai-Tibetan Plateau and the Hengduan Mountains. The two major clades diverged c. 6.34 Mya, corresponding to a period of rapid uplift of the Hengduan Mountains and intensification of the Asian monsoon. Character evolution analysis confirmed parallel evolution of dioecy and other adaptive traits, such as marcescent flowering stems, in the genus. We demonstrate that plastome data could significantly improve phylogenetic resolution in plant groups resulting from recent radiations. Our results not only shed new light on the evolutionary history of Rhodiola, but also indicate that more plastome data should be used in resolving phylogenetic relationship in plant groups that have undergone recent radiations.