Evolutionary radiation is a widely recognized mode of species diversification, but its underlying mechanisms have not been unambiguously resolved for species-rich cosmopolitan plant genera. In particular, it remains largely unknown how biological and environmental factors have jointly driven its occurrence in specific regions. Here we use Rhododendron, the largest genus of woody plants in the Northern Hemisphere, to investigate how geographic and climatic factors, as well as functional traits, worked together to trigger plant evolutionary radiations and shape the global patterns of species richness based on a solid species phylogeny. Using 3437 orthologous nuclear genes, we reconstructed the first highly supported and dated backbone phylogeny of Rhododendron comprising 200 species that represent all subgenera, sections, and nearly all multi-species subsections, and found that most extant species originated by evolutionary radiations when the genus migrated southwards from circumboreal areas to tropical/subtropical mountains, showing rapid increases of both net diversification rate and evolutionary rate of environmental factors in the Miocene. We also found that the geographically uneven diversification of Rhododendron led to a much higher diversity in Asia than in other continents, which was mainly driven by two environmental variables, i.e., elevation range and annual precipitation, and was further strengthened by the adaptation of leaf functional traits. Our study provides a good example of integrating phylogenomic and ecological analyses in deciphering the mechanisms of plant evolutionary radiations and sheds new light on how the intensification of the Asian monsoon has driven evolutionary radiations in large plant genera of the Himalaya-Hengduan Mountains.

We sampled a total of 202 species of Rhododendron for transcriptome sequencing. Those paired-end reads of 100 bp or 150 bp used in de novo assembly with Trinity v. 2.0.6. After discarding redundant transcripts using CD-HIT v. 4.6.5 with a similarity threshold of 1, the longest transcript of each gene was retained. The coding sequences (CDS) were identified with TransDecoder v. 0.36, and the CDS encoding the longest peptide was retained for the ortholog search. We used 3437 OGs  in phylogenetic reconstruction with the maximum-likelihood (ML) method in IQ-TREE v.2.0-rc1. We used RelTime method and MCMCTree program in divergence time estimation. Ancestral areas were reconstructed using BioGeoBEARS v.1.1.1 implemented in R v.3.6.2. The diversification rates and major shifts were evaluated by BAMM. RPANDA was further used to investigate the impact of global paleo-temperature on the diversification of Rhododendron based on nine temperature-dependent likelihood models.