Hybridization and divergent climatic preferences drive divergence of two allopatric Gentiana species on the Qinghai–Tibet Plateau

Abstract

Background and Aims Exploring how species diverge is vital for understanding the drivers of speciation. Factors such as geographic separation and ecological selection, hybridization, polyploidization and shifts in mating system are all major mechanisms of plant speciation, but their contributions to divergence are rarely well-understood. Here we test these mechanisms in two plant species, Gentiana lhassica and G. hoae, with the goal of understanding recent allopatric species divergence in the Qinghai-Tibet Plateau (QTP). Methods We performed Bayesian clustering, phylogenetic analysis and estimates of hybridization using 561,302 nuclear genomic SNPs. We performed redundancy analysis, and identified and annotated species-specific SNPs (ssSNPs) to explore the association between climatic preference and genetic divergence. We also estimated the genome sizes using flow cytometry to test for overlooked polyploidy. Key Results Genomic evidence confirms that G. lhassica and G. hoae are closely related but distinct species, while genome size estimates show divergence occurred without polyploidy. G. hoae has significantly higher average Fis value than G. lhassica. Population clustering based on genomic SNPs shows no signature of recent hybridization, however each species is characterized by a distinct history of hybridization with congeners that has shaped genome wide variation. G. lhassica has captured the chloroplast and experienced introgression with a divergent gentian species, while G. hoae has experienced recurrent hybridization with related taxa. Species distribution modelling suggested range overlap in the last Interglacial period, while redundancy analysis showed that precipitation and temperature are the major climatic differences explaining the separation of the species. The species differ by 2,993 ssSNPs, with genome annotation showing missense variants in genes involved in stress resistance. Conclusions This study suggests that the distinctiveness of these species in the QTP is driven by a combination of hybridization, geographical isolation, mating system differences and evolution of divergent climatic preferences.