Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet Plateau

Abstract

Background Mountains of the world host a significant portion of all terrestrial biodiversity, and the region of the Qinghai-Tibet Plateau (QTP) stands as one of the most remarkable mountain regions on Earth. Because many explosive radiations occurred there, the QTP is a natural laboratory which is ideal to investigate patterns and processes linked to speciation and diversification. Indeed, understanding how closely related and sympatric species diverged is vital to explore drivers fostering speciation, a topic only rarely investigated in the QTP. By combining genomic and environmental data, we explored the speciation process among three closely related and sympatric species, Gentiana hexaphylla, G. lawrencei and G. veitchiorum in the QTP region. Results Combining genome sizes and cytological data, our results showed that G. hexaphylla and G. veitchiorum are diploid, whereas G. lawrencei is tetraploid. Genetic clustering and phylogenetic reconstruction based on genomic SNPs indicated a clear divergence among the three species. Bayesian clustering, migrant, and D-statistic analyses all showed an obvious signature of hybridization among the three species, in particular between G. lawrencei and both G. hexaphylla and G. veitchiorum in almost all populations. Environmental variables related to precipitation and particularly temperature showed significant differences among the three gentians, and in fact a redundancy analysis confirmed that temperature and precipitation were the major climatic factors explaining the genetic differentiation among the three species. Conclusion Our study suggested that ancient hybridization, polyploidization, geological isolation and the evolution of different climatic preferences were all likely to be involved in the divergence of the three Gentiana species, as may be the case for many other taxa in the QTP region.

Cryptic diversity and rampant hybridization in annual gentians on the Qinghai-Tibet Plateau revealed by population genomic analysis

“…Although the Bayankala Mountains are not characterized by high ruggedness as the HM, their average elevation of approximately 5000 m makes them sufficient to serve as barriers throughout glacial cycles for species like Gentiana aristata with short-distance dispersal pollinators. Recently, a set of studies on plants from the QTP region, including Pinus armandii ( Liu et al., 2019 ), Rheum palmatum ( Feng et al., 2020 ), and Gentiana hexaphylla ( Fu et al., 2022b ), identified a distinct genetic pattern in this topographically complicated environment. These geographical characteristics also had an important impact on species assembly across the HM and the greater QTP region ( Li et al., 2021 ).…”

“…The QTP region serves as both the center of biodiversity for approximately 360 Gentiana species ( Ho and Liu, 2001 ) and the primary source for colonization of other regions ( Favre et al., 2016 ). As observed in the majority of plant lineages, abiotic factors, including geological processes, geographical isolation, and climatic changes, are correlated with diversification and speciation in several lineages of Gentiana ( Zhang et al., 2009 ; Favre et al., 2016 ; Fu et al., 2018 , 2020 , 2022b ; Sun et al., 2022 ). In addition, according to growing evidence from phylogenetic and population genetic studies, hybridization is frequently observed in Gentiana , both in the QTP region ( Chen et al., 2021 ; Fu et al., 2021a , 2022a ) and Europe ( Favre et al., 2021 ).…”