Phylogenomics shed light on the complex evolutionary history of a gymnosperm genus showing East Asian–Tethyan disjunction

When and how disjunct distributions of biological taxa arose has long attracted interest in biogeography, yet the East Asian–Tethyan disjunction is understudied. Cupressus (Cupressaceae) shows this disjunction, with 10 species in East Asia and three in the Mediterranean region. Here we used target-capture sequencing and obtained 1991 single-copy nuclear genes, plus complete plastomes, to infer the evolutionary history of Cupressus. Our phylogenomic reconstruction resolved four well supported clades in Cupressus, but revealed significant phylogenetic conflicts, with inter-lineage gene flow, incomplete lineage sorting and gene tree estimation error all making important contributions. The Chengiana clade most likely originated by hybridization between the ancestors of the Himalayan–Hengduan Mountains and subtropical Asia clades, whereas orogenic and climatic changes may have facilitated gene flow within the Himalayan–Hengduan Mountains clade. Molecular dating suggested that the most recent common ancestor of Cupressus appeared in East Asia around the middle Eocene period and then became continuously distributed across Eurasia. The East Asian–Tethyan disjunction arose when the Mediterranean and Himalayan–Hengduan Mountains clades diverged, likely to have been driven by Eocene/Oligocene declines in global temperature, then reinforced by the ecogeographic barrier created by the uplift of the Qinghai–Tibet Plateau. Niche shifts in the common ancestor of the Mediterranean clade, and signatures of selection in genes for drought and salt tolerance, probably indicate adaptation of this clade to local conditions. Overall, our study suggested that in-depth phylogenomic analyses are powerful tools in deciphering the complex evolutionary history of the origin of East Asian–Tethyan disjunction of organisms, especially gymnosperms.