Parallel loss of anthocyanins triggers the incipient sympatric speciation in an alpine ginger

doi:10.1016/j.pld.2025.03.004

Plant Diversity ›› 2025, Vol. 47 ›› Issue (03): 429-439.DOI: 10.1016/j.pld.2025.03.004

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Parallel loss of anthocyanins triggers the incipient sympatric speciation in an alpine ginger

Zhi-Li Zhou (周知里)^a, Tial C. Ling^a,b,c, Jian-Li Zhao (赵建立)^d, Xin-Zhi Wang (王欣之)^a, Lin-Lin Wang (王林林)^a, Li Li (李莉)^d, Wen-Jing Wang (王雯婧)^d, Dong-Rui Jia (贾东瑞)^d, Zhi-Kun Wu (吴之坤)^e, Xu-Dong Sun (孙旭东)^a, Yong-Ping Yang (杨永平)^a, Yuan-Wen Duan (段元文)^a,f,g

a. Yunnan Key Laboratory for Crop Wild Relatives Omics, Germplasm Bank of Wild Species, Institute of Tibetan Plateau Research at Kunming, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, PR China;
b. Department of Environmental and Plant Biology, Ohio University, Athens, OH 45701-2979, USA;
c. University of the Chinese Academy of Sciences, Beijing 100049, PR China;
d. Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming 650504, PR China;
e. Guizhou University of Traditional Chinese Medicine, Guiyang 550025, PR China;
f. Yunnan Lijiang Forest Ecosystem National Observation and Research Station, Kunming Institute of Botany, Chinese Academy of Sciences, Lijiang 674100, PR China;
g. Key Laboratory of Phytochemistry and Natural Medicines, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, PR China

Received:2024-11-20 Revised:2025-02-10 Online:2025-05-21 Published:2025-05-25
Contact: Xu-Dong Sun,E-mail:sunxudong@mail.kib.ac.cn;Yong-Ping Yang,E-mail:yangyp@mail.kib.ac.cn;Yuan-Wen Duan,E-mail:duanyw@mail.kib.ac.cn
Supported by:
The work was financially supported by National Natural Science Foundation of China (32102429, 32371586), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0502), the Yunnan Young Talent Project (YNWR-QNBJ-2019-214), and the CAS-TWAS Presidents Fellowship to Tial Cung Ling.

Parallel loss of anthocyanins triggers the incipient sympatric speciation in an alpine ginger

a. Yunnan Key Laboratory for Crop Wild Relatives Omics, Germplasm Bank of Wild Species, Institute of Tibetan Plateau Research at Kunming, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, PR China;
b. Department of Environmental and Plant Biology, Ohio University, Athens, OH 45701-2979, USA;
c. University of the Chinese Academy of Sciences, Beijing 100049, PR China;
d. Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming 650504, PR China;
e. Guizhou University of Traditional Chinese Medicine, Guiyang 550025, PR China;
f. Yunnan Lijiang Forest Ecosystem National Observation and Research Station, Kunming Institute of Botany, Chinese Academy of Sciences, Lijiang 674100, PR China;
g. Key Laboratory of Phytochemistry and Natural Medicines, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, PR China

通讯作者: Xu-Dong Sun,E-mail:sunxudong@mail.kib.ac.cn;Yong-Ping Yang,E-mail:yangyp@mail.kib.ac.cn;Yuan-Wen Duan,E-mail:duanyw@mail.kib.ac.cn
基金资助:
The work was financially supported by National Natural Science Foundation of China (32102429, 32371586), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0502), the Yunnan Young Talent Project (YNWR-QNBJ-2019-214), and the CAS-TWAS Presidents Fellowship to Tial Cung Ling.

Abstract

Abstract: Change of flower color can readily lead to a shift in pollinators, potentially causing pollinator mediated reproductive isolation or even speciation. Here, we examined the ecological and evolutionary consequences of flower color polymorphism in Roscoea cautleoides, an alpine ginger with sympatric distribution of purple- and yellow-flowered plants. Variations in pollinator visitation and specialization to the flower color contributed greatly to pre-zygotic reproductive isolation, with post-zygotic isolation also observed in reciprocal pollination. Yellow-flowered plants evolved independently from purple-flowered plants in two populations due to the absence of anthocyanins, as supported by metabolic, expression, and genetic analysis. Despite early genetic divergence between the two-flower-colored plants, highly differentiated genes were associated with reproduction and stress, while highly selective genes were enriched in stress. Our results suggest that parallel loss of anthocyanins leads to flower color polymorphism in different populations of R. cautleoides, with pollinator preference contributing to reproductive isolation and subsequent genetic differentiation, indicating the process of incipient speciation triggered by flower color changes with sympatric distribution.

Key words: Pollinator shift, Reproductive isolation, Differentially expressed genes, Genetic differentiation, Roscoea

摘要： Change of flower color can readily lead to a shift in pollinators, potentially causing pollinator mediated reproductive isolation or even speciation. Here, we examined the ecological and evolutionary consequences of flower color polymorphism in Roscoea cautleoides, an alpine ginger with sympatric distribution of purple- and yellow-flowered plants. Variations in pollinator visitation and specialization to the flower color contributed greatly to pre-zygotic reproductive isolation, with post-zygotic isolation also observed in reciprocal pollination. Yellow-flowered plants evolved independently from purple-flowered plants in two populations due to the absence of anthocyanins, as supported by metabolic, expression, and genetic analysis. Despite early genetic divergence between the two-flower-colored plants, highly differentiated genes were associated with reproduction and stress, while highly selective genes were enriched in stress. Our results suggest that parallel loss of anthocyanins leads to flower color polymorphism in different populations of R. cautleoides, with pollinator preference contributing to reproductive isolation and subsequent genetic differentiation, indicating the process of incipient speciation triggered by flower color changes with sympatric distribution.

关键词: Pollinator shift, Reproductive isolation, Differentially expressed genes, Genetic differentiation, Roscoea

Zhi-Li Zhou (周知里), Tial C. Ling, Jian-Li Zhao (赵建立), Xin-Zhi Wang (王欣之), Lin-Lin Wang (王林林), Li Li (李莉), Wen-Jing Wang (王雯婧), Dong-Rui Jia (贾东瑞), Zhi-Kun Wu (吴之坤), Xu-Dong Sun (孙旭东), Yong-Ping Yang (杨永平), Yuan-Wen Duan (段元文). Parallel loss of anthocyanins triggers the incipient sympatric speciation in an alpine ginger[J]. Plant Diversity, 2025, 47(03): 429-439.

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Parallel loss of anthocyanins triggers the incipient sympatric speciation in an alpine ginger

Parallel loss of anthocyanins triggers the incipient sympatric speciation in an alpine ginger

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