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Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere

BACKGROUND: Impatiens sect. Impatiens is distributed across the Northern Hemisphere and has diversified considerably, particularly within the Hengduan Mountains (HDM) in southwest China. Yet, the infra-sectional phylogenetic relationships are not well resolved, largely due to limited taxon sampling...

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Autores principales: Qin, Fei, Xue, Tiantian, Zhang, Xiaoxia, Yang, Xudong, Yu, Jianghong, Gadagkar, Sudhindra R., Yu, Shengxiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10685625/
https://www.ncbi.nlm.nih.gov/pubmed/38030965
http://dx.doi.org/10.1186/s12870-023-04625-w
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author Qin, Fei
Xue, Tiantian
Zhang, Xiaoxia
Yang, Xudong
Yu, Jianghong
Gadagkar, Sudhindra R.
Yu, Shengxiang
author_facet Qin, Fei
Xue, Tiantian
Zhang, Xiaoxia
Yang, Xudong
Yu, Jianghong
Gadagkar, Sudhindra R.
Yu, Shengxiang
author_sort Qin, Fei
collection PubMed
description BACKGROUND: Impatiens sect. Impatiens is distributed across the Northern Hemisphere and has diversified considerably, particularly within the Hengduan Mountains (HDM) in southwest China. Yet, the infra-sectional phylogenetic relationships are not well resolved, largely due to limited taxon sampling and an insufficient number of molecular markers. The evolutionary history of its diversification is also poorly understood. In this study, plastome data and the most complete sampling to date were used to reconstruct a robust phylogenetic framework for this section. The phylogeny was then used to investigate its biogeographical history and diversification patterns, specifically with the aim of understanding the role played by the HDM and past climatic changes in its diversification. RESULTS: A stable phylogeny was reconstructed that strongly supported both the monophyly of the section and its division into seven major clades (Clades I-VII). Molecular dating and ancestral area reconstruction suggest that sect. Impatiens originated in the HDM and Southeast China around 11.76 Ma, after which different lineages dispersed to Northwest China, temperate Eurasia, and North America, mainly during the Pliocene and Pleistocene. An intercontinental dispersal event from East Asia to western North America may have occurred via the Bering Land Bridge or Aleutian Islands. The diversification rate was high during its early history, especially with the HDM, but gradually decreased over time both within and outside the HDM. Multiple linear regression analysis showed that the distribution pattern of species richness was strongly associated with elevation range, elevation, and mean annual temperature. Finally, ancestral niche analysis indicated that sect. Impatiens originated in a relatively cool, middle-elevation area. CONCLUSIONS: We inferred the evolutionary history of sect. Impatiens based on a solid phylogenetic framework. The HDM was the primary source or pump of its diversity in the Northern Hemisphere. Orogeny and climate change may have also shaped its diversification rates, as a steady decrease in the diversification rate coincided with the uplift of the HDM and climate cooling. These findings provide insights into the distribution pattern of sect. Impatiens and other plants in the Northern Hemisphere. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04625-w.
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spelling pubmed-106856252023-11-30 Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere Qin, Fei Xue, Tiantian Zhang, Xiaoxia Yang, Xudong Yu, Jianghong Gadagkar, Sudhindra R. Yu, Shengxiang BMC Plant Biol Research BACKGROUND: Impatiens sect. Impatiens is distributed across the Northern Hemisphere and has diversified considerably, particularly within the Hengduan Mountains (HDM) in southwest China. Yet, the infra-sectional phylogenetic relationships are not well resolved, largely due to limited taxon sampling and an insufficient number of molecular markers. The evolutionary history of its diversification is also poorly understood. In this study, plastome data and the most complete sampling to date were used to reconstruct a robust phylogenetic framework for this section. The phylogeny was then used to investigate its biogeographical history and diversification patterns, specifically with the aim of understanding the role played by the HDM and past climatic changes in its diversification. RESULTS: A stable phylogeny was reconstructed that strongly supported both the monophyly of the section and its division into seven major clades (Clades I-VII). Molecular dating and ancestral area reconstruction suggest that sect. Impatiens originated in the HDM and Southeast China around 11.76 Ma, after which different lineages dispersed to Northwest China, temperate Eurasia, and North America, mainly during the Pliocene and Pleistocene. An intercontinental dispersal event from East Asia to western North America may have occurred via the Bering Land Bridge or Aleutian Islands. The diversification rate was high during its early history, especially with the HDM, but gradually decreased over time both within and outside the HDM. Multiple linear regression analysis showed that the distribution pattern of species richness was strongly associated with elevation range, elevation, and mean annual temperature. Finally, ancestral niche analysis indicated that sect. Impatiens originated in a relatively cool, middle-elevation area. CONCLUSIONS: We inferred the evolutionary history of sect. Impatiens based on a solid phylogenetic framework. The HDM was the primary source or pump of its diversity in the Northern Hemisphere. Orogeny and climate change may have also shaped its diversification rates, as a steady decrease in the diversification rate coincided with the uplift of the HDM and climate cooling. These findings provide insights into the distribution pattern of sect. Impatiens and other plants in the Northern Hemisphere. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04625-w. BioMed Central 2023-11-29 /pmc/articles/PMC10685625/ /pubmed/38030965 http://dx.doi.org/10.1186/s12870-023-04625-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Qin, Fei
Xue, Tiantian
Zhang, Xiaoxia
Yang, Xudong
Yu, Jianghong
Gadagkar, Sudhindra R.
Yu, Shengxiang
Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere
title Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere
title_full Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere
title_fullStr Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere
title_full_unstemmed Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere
title_short Past climate cooling and orogenesis of the Hengduan Mountains have influenced the evolution of Impatiens sect. Impatiens (Balsaminaceae) in the Northern Hemisphere
title_sort past climate cooling and orogenesis of the hengduan mountains have influenced the evolution of impatiens sect. impatiens (balsaminaceae) in the northern hemisphere
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10685625/
https://www.ncbi.nlm.nih.gov/pubmed/38030965
http://dx.doi.org/10.1186/s12870-023-04625-w
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