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...

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Main Authors: Pengcheng Fu, Adrien Favre, Rui Wang, Yizhuo Huang, Shanshan Sun
Format: Article
Language:English
Published: BMC 2022-10-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-022-03879-0
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author Pengcheng Fu
Adrien Favre
Rui Wang
Yizhuo Huang
Shanshan Sun
author_facet Pengcheng Fu
Adrien Favre
Rui Wang
Yizhuo Huang
Shanshan Sun
author_sort Pengcheng Fu
collection DOAJ
description 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.
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spelling doaj.art-da1c5b204e7946c9a26c0d2386e6cd772022-12-22T03:56:26ZengBMCBMC Plant Biology1471-22292022-10-0122111510.1186/s12870-022-03879-0Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet PlateauPengcheng Fu0Adrien Favre1Rui Wang2Yizhuo Huang3Shanshan Sun4School of Life Science, Luoyang Normal UniversityRegional nature park of the Trient ValleySchool of Life Science, Luoyang Normal UniversitySchool of Life Science, Luoyang Normal UniversitySchool of Life Science, Luoyang Normal UniversityAbstract 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.https://doi.org/10.1186/s12870-022-03879-0Climatic preferenceDivergenceGenomic SNPsGentianaHybridization
spellingShingle Pengcheng Fu
Adrien Favre
Rui Wang
Yizhuo Huang
Shanshan Sun
Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet Plateau
BMC Plant Biology
Climatic preference
Divergence
Genomic SNPs
Gentiana
Hybridization
title Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet Plateau
title_full Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet Plateau
title_fullStr Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet Plateau
title_full_unstemmed Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet Plateau
title_short Between allopatry and secondary contact: differentiation and hybridization among three sympatric Gentiana species in the Qinghai-Tibet Plateau
title_sort between allopatry and secondary contact differentiation and hybridization among three sympatric gentiana species in the qinghai tibet plateau
topic Climatic preference
Divergence
Genomic SNPs
Gentiana
Hybridization
url https://doi.org/10.1186/s12870-022-03879-0
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