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

doi:10.1016/j.pld.2022.02.002

Plant Diversity ›› 2022, Vol. 44 ›› Issue (05): 455-467.DOI: 10.1016/j.pld.2022.02.002

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

Ting-Shen Han^a,b,c, Zheng-Yan Hu^a,d, Zhi-Qiang Du^a,d, Quan-Jing Zheng^a,d, Jia Liu^a,b, Thomas Mitchell-Olds^c, Yao-Wu Xing^a,b

a. CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303, China;
b. Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Mengla, Yunnan 666303, China;
c. Department of Biology, Duke University, Box 90338, Durham, NC 27708, USA;
d. University of Chinese Academy of Sciences, Beijing 100049, China

收稿日期:2022-01-18 修回日期:2022-02-22 出版日期:2022-09-25 发布日期:2022-10-14
通讯作者: Ting-Shen Han,E-mail:hantingshen@xtbg.ac.cn;Yao-Wu Xing,E-mail:ywxing@xtbg.org.cn
基金资助:
This work was supported by the National Natural Science Foundation of China (31800177,32170224,and U1802242),and the Strategic Priority Research Program of Chinese Academy of Sciences (XDB31000000).T-S.H.is also supported by the Youth Innovation Promotion Association CAS (2020391),China Scholarship Council (201804910061),and CAS Light of West China Program.We acknowledge Ya-Long Guo at the Institute of Botany CAS for providing Capsella rubella seeds and revising the manuscript.We also thank members of the Paleoecology group,and Biogeography and Ecology group at the Xishuangbanna Tropical Botanical Garden CAS,as well as Zhendong Fang and Lin Liu at the Shangri-La Alpine Botanical Garden who helped with valuable discussions on the transplanting experiment.We thank the anonymous reviewers for helpful comments which greatly improved the manuscript.

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

Ting-Shen Han^a,b,c, Zheng-Yan Hu^a,d, Zhi-Qiang Du^a,d, Quan-Jing Zheng^a,d, Jia Liu^a,b, Thomas Mitchell-Olds^c, Yao-Wu Xing^a,b

a. CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303, China;
b. Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Mengla, Yunnan 666303, China;
c. Department of Biology, Duke University, Box 90338, Durham, NC 27708, USA;
d. University of Chinese Academy of Sciences, Beijing 100049, China

Received:2022-01-18 Revised:2022-02-22 Online:2022-09-25 Published:2022-10-14
Supported by:
This work was supported by the National Natural Science Foundation of China (31800177,32170224,and U1802242),and the Strategic Priority Research Program of Chinese Academy of Sciences (XDB31000000).T-S.H.is also supported by the Youth Innovation Promotion Association CAS (2020391),China Scholarship Council (201804910061),and CAS Light of West China Program.We acknowledge Ya-Long Guo at the Institute of Botany CAS for providing Capsella rubella seeds and revising the manuscript.We also thank members of the Paleoecology group,and Biogeography and Ecology group at the Xishuangbanna Tropical Botanical Garden CAS,as well as Zhendong Fang and Lin Liu at the Shangri-La Alpine Botanical Garden who helped with valuable discussions on the transplanting experiment.We thank the anonymous reviewers for helpful comments which greatly improved the manuscript.

摘要/Abstract

摘要： 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.

关键词: Adaptation, Hengduan mountains, Pleistocene, Polyploidy, Rorippa

Abstract: 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.

Key words: Adaptation, Hengduan mountains, Pleistocene, Polyploidy, Rorippa

Ting-Shen Han, Zheng-Yan Hu, Zhi-Qiang Du, Quan-Jing Zheng, Jia Liu, Thomas Mitchell-Olds, Yao-Wu Xing. Adaptive responses drive the success of polyploid yellowcresses (Rorippa, Brassicaceae) in the Hengduan Mountains, a temperate biodiversity hotspot[J]. Plant Diversity, 2022, 44(05): 455-467.

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

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

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