Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera
Parallel evolution of reproductive isolation (PERI) provides strong evidence for natural selection playing a fundamental role in the origin of species. However, PERI has been rarely demonstrated for well established species drawn from different genera. In particular, parallel molecular signatures fo...
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| Format: | Article |
| Language: | English |
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Elsevier
2022-05-01
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| Series: | The Innovation |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666675822000431 |
| _version_ | 1818006263593697280 |
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| author | Zefu Wang Yuanzhong Jiang Xiaoyue Yang Hao Bi Jialiang Li Xingxing Mao Yazhen Ma Dafu Ru Cheng Zhang Guoqian Hao Jing Wang Richard J. Abbott Jianquan Liu |
| author_facet | Zefu Wang Yuanzhong Jiang Xiaoyue Yang Hao Bi Jialiang Li Xingxing Mao Yazhen Ma Dafu Ru Cheng Zhang Guoqian Hao Jing Wang Richard J. Abbott Jianquan Liu |
| author_sort | Zefu Wang |
| collection | DOAJ |
| description | Parallel evolution of reproductive isolation (PERI) provides strong evidence for natural selection playing a fundamental role in the origin of species. However, PERI has been rarely demonstrated for well established species drawn from different genera. In particular, parallel molecular signatures for the same genes in response to similar habitat divergence in such different lineages is lacking. Here, based on whole-genome sequencing data, we first explore the speciation process in two sister species of Carpinus (Betulaceae) in response to divergence for temperature and soil-iron concentration in habitats they occupy in northern and southwestern China, respectively. We then determine whether parallel molecular mutations occur during speciation in this pair of species and also in another sister-species pair of the related genus, Ostryopsis, which occupy similarly divergent habitats in China. We show that gene flow occurred during the origin of both pairs of sister species since approximately 9.8 or approximately 2 million years ago, implying strong natural selection during divergence. Also, in both species pairs we detected concurrent positive selection in a gene (LHY) for flowering time and in two paralogous genes (FRO4 and FRO7) of a gene family known to be important for iron tolerance. These changes were in addition to changes in other major genes related to these two traits. The different alleles of these particular candidate genes possessed by the sister species of Carpinus were functionally tested and indicated likely to alter flowering time and iron tolerance as previously demonstrated in the pair of Ostryopsis sister species. Allelic changes in these genes may have effectively resulted in high levels of prezygotic reproductive isolation to evolve between sister species of each pair. Our results show that PERI can occur in different genera at different timescales and involve similar signatures of molecular evolution at genes or paralogues of the same gene family, causing reproductive isolation as a consequence of adaptation to similarly divergent habitats. |
| first_indexed | 2024-04-14T04:58:57Z |
| format | Article |
| id | doaj.art-78714ca08bfd47cf960564de192a2700 |
| institution | Directory Open Access Journal |
| issn | 2666-6758 |
| language | English |
| last_indexed | 2024-04-14T04:58:57Z |
| publishDate | 2022-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | The Innovation |
| spelling | doaj.art-78714ca08bfd47cf960564de192a27002022-12-22T02:11:04ZengElsevierThe Innovation2666-67582022-05-0133100247Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two generaZefu Wang0Yuanzhong Jiang1Xiaoyue Yang2Hao Bi3Jialiang Li4Xingxing Mao5Yazhen Ma6Dafu Ru7Cheng Zhang8Guoqian Hao9Jing Wang10Richard J. Abbott11Jianquan Liu12State Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, China; Key Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaKey Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaState Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, ChinaKey Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaKey Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaKey Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaKey Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaState Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, ChinaKey Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China; Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, ChinaSichuan Tea College, Yibin University, Yibin 644000, ChinaKey Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, ChinaSchool of Biology, University of St Andrews, St Andrews KY169TH, UKState Key Laboratory of Grassland Agro-Ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, China; Key Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China; Corresponding authorParallel evolution of reproductive isolation (PERI) provides strong evidence for natural selection playing a fundamental role in the origin of species. However, PERI has been rarely demonstrated for well established species drawn from different genera. In particular, parallel molecular signatures for the same genes in response to similar habitat divergence in such different lineages is lacking. Here, based on whole-genome sequencing data, we first explore the speciation process in two sister species of Carpinus (Betulaceae) in response to divergence for temperature and soil-iron concentration in habitats they occupy in northern and southwestern China, respectively. We then determine whether parallel molecular mutations occur during speciation in this pair of species and also in another sister-species pair of the related genus, Ostryopsis, which occupy similarly divergent habitats in China. We show that gene flow occurred during the origin of both pairs of sister species since approximately 9.8 or approximately 2 million years ago, implying strong natural selection during divergence. Also, in both species pairs we detected concurrent positive selection in a gene (LHY) for flowering time and in two paralogous genes (FRO4 and FRO7) of a gene family known to be important for iron tolerance. These changes were in addition to changes in other major genes related to these two traits. The different alleles of these particular candidate genes possessed by the sister species of Carpinus were functionally tested and indicated likely to alter flowering time and iron tolerance as previously demonstrated in the pair of Ostryopsis sister species. Allelic changes in these genes may have effectively resulted in high levels of prezygotic reproductive isolation to evolve between sister species of each pair. Our results show that PERI can occur in different genera at different timescales and involve similar signatures of molecular evolution at genes or paralogues of the same gene family, causing reproductive isolation as a consequence of adaptation to similarly divergent habitats.http://www.sciencedirect.com/science/article/pii/S2666675822000431parallel evolution of reproductive isolationnatural selectionallelic differentiationdivergent habitatsspeciation |
| spellingShingle | Zefu Wang Yuanzhong Jiang Xiaoyue Yang Hao Bi Jialiang Li Xingxing Mao Yazhen Ma Dafu Ru Cheng Zhang Guoqian Hao Jing Wang Richard J. Abbott Jianquan Liu Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera The Innovation parallel evolution of reproductive isolation natural selection allelic differentiation divergent habitats speciation |
| title | Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera |
| title_full | Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera |
| title_fullStr | Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera |
| title_full_unstemmed | Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera |
| title_short | Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera |
| title_sort | molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera |
| topic | parallel evolution of reproductive isolation natural selection allelic differentiation divergent habitats speciation |
| url | http://www.sciencedirect.com/science/article/pii/S2666675822000431 |
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