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Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot

Polyploids contribute substantially to plant evolution and biodiversity; however, the mechanisms by which they succeed are still unclear. According to the polyploid adaptation hypothesis, successful polyploids spread by repeated adaptive responses to new environments. Here, we tested this hypothesis...

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Autores principales: Han, Ting-Shen, Hu, Zheng-Yan, Du, Zhi-Qiang, Zheng, Quan-Jing, Liu, Jia, Mitchell-Olds, Thomas, Xing, Yao-Wu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Kunming Institute of Botany, Chinese Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9512641/
https://www.ncbi.nlm.nih.gov/pubmed/36187546
http://dx.doi.org/10.1016/j.pld.2022.02.002
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author Han, Ting-Shen
Hu, Zheng-Yan
Du, Zhi-Qiang
Zheng, Quan-Jing
Liu, Jia
Mitchell-Olds, Thomas
Xing, Yao-Wu
author_facet Han, Ting-Shen
Hu, Zheng-Yan
Du, Zhi-Qiang
Zheng, Quan-Jing
Liu, Jia
Mitchell-Olds, Thomas
Xing, Yao-Wu
author_sort Han, Ting-Shen
collection PubMed
description Polyploids contribute substantially to plant evolution and biodiversity; however, the mechanisms by which they succeed are still unclear. According to the polyploid adaptation hypothesis, successful polyploids spread by repeated adaptive responses to new environments. Here, we tested this hypothesis using two tetraploid yellowcresses (Rorippa), the endemic Rorippa elata and the widespread Rorippa palustris, in the temperate biodiversity hotspot of the Hengduan Mountains. Speciation modes were resolved by phylogenetic modeling using 12 low-copy nuclear loci. Phylogeographical patterns were then examined using haplotypes phased from four plastid and ITS markers, coupled with historical niche reconstruction by ecological niche modeling. We inferred the time of hybrid origins for both species as the mid-Pleistocene, with shared glacial refugia within the southern Hengduan Mountains. Phylogeographic and ecological niche reconstruction indicated recurrent northward colonization by both species after speciation, possibly tracking denuded habitats created by glacial retreat during interglacial periods. Common garden experiment involving perennial R. elata conducted over two years revealed significant changes in fitness-related traits across source latitudes or altitudes, including latitudinal increases in survival rate and compactness of plant architecture, suggesting gradual adaptation during range expansion. These findings support the polyploid adaptation hypothesis and suggest that the spread of polyploids was aided by adaptive responses to environmental changes during the Pleistocene. Our results thus provide insight into the evolutionary success of polyploids in high-altitude environments.
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spelling pubmed-95126412022-09-30 Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot Han, Ting-Shen Hu, Zheng-Yan Du, Zhi-Qiang Zheng, Quan-Jing Liu, Jia Mitchell-Olds, Thomas Xing, Yao-Wu Plant Divers Research Paper Polyploids contribute substantially to plant evolution and biodiversity; however, the mechanisms by which they succeed are still unclear. According to the polyploid adaptation hypothesis, successful polyploids spread by repeated adaptive responses to new environments. Here, we tested this hypothesis using two tetraploid yellowcresses (Rorippa), the endemic Rorippa elata and the widespread Rorippa palustris, in the temperate biodiversity hotspot of the Hengduan Mountains. Speciation modes were resolved by phylogenetic modeling using 12 low-copy nuclear loci. Phylogeographical patterns were then examined using haplotypes phased from four plastid and ITS markers, coupled with historical niche reconstruction by ecological niche modeling. We inferred the time of hybrid origins for both species as the mid-Pleistocene, with shared glacial refugia within the southern Hengduan Mountains. Phylogeographic and ecological niche reconstruction indicated recurrent northward colonization by both species after speciation, possibly tracking denuded habitats created by glacial retreat during interglacial periods. Common garden experiment involving perennial R. elata conducted over two years revealed significant changes in fitness-related traits across source latitudes or altitudes, including latitudinal increases in survival rate and compactness of plant architecture, suggesting gradual adaptation during range expansion. These findings support the polyploid adaptation hypothesis and suggest that the spread of polyploids was aided by adaptive responses to environmental changes during the Pleistocene. Our results thus provide insight into the evolutionary success of polyploids in high-altitude environments. Kunming Institute of Botany, Chinese Academy of Sciences 2022-03-16 /pmc/articles/PMC9512641/ /pubmed/36187546 http://dx.doi.org/10.1016/j.pld.2022.02.002 Text en © 2022 Kunming Institute of Botany, Chinese Academy of Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Research Paper
Han, Ting-Shen
Hu, Zheng-Yan
Du, Zhi-Qiang
Zheng, Quan-Jing
Liu, Jia
Mitchell-Olds, Thomas
Xing, Yao-Wu
Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot
title Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot
title_full Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot
title_fullStr Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot
title_full_unstemmed Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot
title_short Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot
title_sort adaptive responses drive the success of polyploid yellowcresses (rorippa, brassicaceae) in the hengduan mountains, a temperate biodiversity hotspot
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9512641/
https://www.ncbi.nlm.nih.gov/pubmed/36187546
http://dx.doi.org/10.1016/j.pld.2022.02.002
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