Abstract

Mountainous regions can promote complex speciation scenarios, including hybridization leading to chloroplast capture, revealed by incongruent phylogenetic trees. Four allopatric Taxus lineages from the Hengduan Mountains, southwestern China, exhibit cytonuclear phylogenetic discordance. We use multi-omic data at the population level to investigate their historical speciation processes. Transcriptome data consistently showed that T. florinii and the Emei type, which are the focus of cytonuclear discordance, originated in the Late Miocene. Population genomic analysis based on ddRAD-seq data revealed limited contemporary inter-specific gene flow. However, neither taxon exhibited the mosaic nuclear genomes that usually characterized hybrids. Taxus florinii appears to have originated when a lineage of T. wallichiana captured the T. chinensis plastid type, whereas plastid introgression in the opposite direction generated the Emei Type. All four species have distinct ecological niches, and introgression might have contributed to, or even initiated, their ecological divergence. We propose that these speciation events represent very rare examples of chloroplast capture events despite the paternal cpDNA inheritance of Gymnosperms. These events might have been triggered by orogenic activities of the Hengduan Mountains and the intensification of the Asian monsoon in the late Miocene, and may represent a scenario more common in these mountains than presently known.