An updated phylogenetic and biogeographic analysis based on genome skimming data reveals convergent evolution of shrubby habit in Clematis in the Pliocene and Pleistocene

Abstract

Convergent evolution, often viewed as the inevitable outcome of natural selection, has received special attention since the time of Darwin. Clematis is well known for its climbing habit, but it has some shrubby species, known as sect. Fruticella s.l. The shrubby Clematis species are distributed in the dry habitats of Central Asia and adjacent areas showing possible convergent evolution. In this study, we assembled the complete plastome and nuclear ribosomal DNA (nrDNA) sequences of 56 Clematis species, representing most sections and covering most of the shrubby species, to reconstruct their evolutionary histories. Using both maximum likelihood and Bayesian methods, the plastome and nrDNA datasets generated similar, but not identical, phylogenetic relationships, which are better resolved than in previous studies. Then, molecular dating, historical range reconstruction, and character optimization analyses were conducted based on this updated phylogenetic framework. All the morphological characters widely used for taxonomy were shown to have evolved multiple times. Molecular dating inferred that Clematis diverged from its sister in the mid Miocene, and all six major clades of Clematis originated during the late Miocene, with a species radiation during the Pliocene to Pleistocene. The results clearly showed that the shrubby habit evolved independently in four lineages of Clematis in Asia. We also revealed that the shrubby lineages have emerged since the very beginning of Pliocene. Asian monsoon variation in the Pliocene and glacial period fluctuation in the Pleistocene may be the driving forces for the origin and diversification of the shrubby Clematis in Central Asia and adjacent dry areas.