Genomic clines across the species boundary between a hybrid pine and its progenitor in the eastern Tibetan Plateau

Most species have clearly defined distribution ranges and ecological niches. The genetic and ecological causes of species differentiation and the mechanisms that maintain species boundaries between newly evolved taxa and their progenitors are, however, less clearly defined. This study investigated the genetic structure and clines in Pinus densata, a pine of hybrid origin on the southeastern Tibetan Plateau, to gain an understanding of the contemporary dynamics of species barriers. We analyzed genetic diversity in a range-wide collection of P. densata and representative populations of its progenitors, Pinus tabulifor-mis and Pinus yunnanensis, using exome capture sequencing. We detected four distinct genetic groups within P. densata that reflect its migration history and major gene-flow barriers across the landscape. The demographies of these genetic groups in the Pleistocene were associated with regional glaciation his-tories. Interestingly, population sizes rebounded rapidly during interglacial periods, suggesting persis-tence and resilience of the species during the Quaternary ice age. In the contact zone between P. densata and P. yunnanensis, 3.36% of the analyzed loci (57 849) showed exceptional patterns of intro-gression, suggesting their potential roles in either adaptive introgression or reproductive isolation. These outliers showed strong clines along critical climate gradients and enrichment in a number of biological pro-cesses relevant to high-altitude adaptation. This indicates that ecological selection played an important role in generating genomic heterogeneity and a genetic barrier across a zone of species transition. Our study highlights the forces that operate to maintain species boundaries and promote speciation in the Qinghai-Tibetan Plateau and other mountain systems.

Automated summary

This study investigated the genetic structure and clines in Pinus densata to gain an understanding of the contemporary dynamics of species barriers. It found four distinct genetic groups within P. densata that reflect its migration history and major gene-flow barriers across the landscape. Ecological selection played an important role in generating genomic heterogeneity and a genetic barrier across a zone of species transition.