Cryptic speciation in the Chinese white pine (Pinus armandii): Implications for the high species diversity of conifers in the Hengduan Mountains, a global biodiversity hotspot

(A) Distribution of sampling localities. (B) Results of the Structure analysis based on the SNPs at K = 2. (C) Principal components analysis (PCA) of 12,548 SNPs obtained from P. armandii and its relatives. (D) Phylogenetic analysis Maximum-likelihood tree constructed from the 13,906 SNPs identified in P. armandii. (E) Heat maps for the net genetic distances (Da) between different groups or species. (F) Predicted distributions of the northern and southern subdivisions using Maxent. [Display omitted] •Cryptic speciation has occurred in Pinus armandii.•The interactions of geography and ecology led to the speciation.•Both geography and ecology contributed to the high conifer diversity in HHM. Conifers are the largest and ecologically and economically most important component group of the gymnosperms. Despite their slow rate of molecular evolution, rapid and recent diversification was unexpectedly prevalent in this ancient group in the Hengduan Mountains, a world’s biodiversity hotspot and gymnosperm diversity center in Southwest China. In this study, we investigated the underlying mechanisms and disentangled the interactions of geography and ecology in speciation and evolution in Pinus armandii, an important forest tree species endemic to China, by integrating analyses of population transcriptomics, population genetics and ecological niche modeling. Many lines of evidence suggest that cryptic speciation has occurred in P. armandii. During the process, geologically induced formation of Mount Gongga and other massive peaks might trigger the initial vicariance isolation of the northern and southern subdivisions, and ecologically based selection then reinforced their differentiation and local adaptation. Our ecological niche analysis and earlier reciprocal transplant experiments in P. armandii provided convincing evidences for the critical role of ecology in the process of speciation. These findings suggest that both geography and ecology contributed significantly to the abundance of very recent and rapid species divergences, which promoted the rising of the extremely high conifer diversity in the Hengduan Mountains.