Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism
Abstract Genetic variation and phenotypic plasticity are both important to adaptive evolution. However, how they act together on particular traits remains poorly understood. Here, we integrated phenotypic, genomic, and transcriptomic data from two allopatric but closely related congeneric oyster spe...
Published in: | Molecular Biology and Evolution |
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Oxford University Press (OUP)
2021
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Online Access: | http://dx.doi.org/10.1093/molbev/msab241 http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msab241/40256678/msab241.pdf http://academic.oup.com/mbe/article-pdf/38/11/5144/40935452/msab241.pdf |
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croxfordunivpr:10.1093/molbev/msab241 2024-09-15T18:03:16+00:00 Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism Li, Ao Li, Li Zhang, Ziyan Li, Shiming Wang, Wei Guo, Ximing Zhang, Guofan Saitou, Naruya National Key R&D Program of China Strategic Priority Research Program of the Chinese Academy of Sciences Distinguished Young Scientists Research Fund of Key Laboratory of Experimental Marine Biology Chinese Academy of Sciences China Postdoctoral Science Foundation Key Deployment Project of Centre for Ocean Mega-Research of Science Chinese Academy of Sciences National Natural Science Foundation of China Technology and Modern Agro-Industry Technology Research System 2021 http://dx.doi.org/10.1093/molbev/msab241 http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msab241/40256678/msab241.pdf http://academic.oup.com/mbe/article-pdf/38/11/5144/40935452/msab241.pdf en eng Oxford University Press (OUP) https://creativecommons.org/licenses/by-nc/4.0/ Molecular Biology and Evolution volume 38, issue 11, page 5144-5155 ISSN 0737-4038 1537-1719 journal-article 2021 croxfordunivpr https://doi.org/10.1093/molbev/msab241 2024-09-03T04:13:15Z Abstract Genetic variation and phenotypic plasticity are both important to adaptive evolution. However, how they act together on particular traits remains poorly understood. Here, we integrated phenotypic, genomic, and transcriptomic data from two allopatric but closely related congeneric oyster species, Crassostrea angulata from southern/warm environments and Crassostrea gigas from northern/cold environments, to investigate the roles of genetic divergence and plasticity in thermal adaptation. Reciprocal transplantation experiments showed that both species had higher fitness in their native habitats than in nonnative environments, indicating strong adaptive divergence. The southern species evolved higher transcriptional plasticity, and the plasticity was adaptive, suggesting that increased plasticity is important for thermal adaptation to warm climates. Genome-wide comparisons between the two species revealed that genes under selection tended to respond to environmental changes and showed higher sequence divergence in noncoding regions. All genes under selection and related to energy metabolism exhibited habitat-specific expression with genes involved in ATP production and lipid catabolism highly expressed in warm/southern habitats, and genes involved in ATP consumption and lipid synthesis were highly expressed in cold/northern habitats. The gene for acyl-CoA desaturase, a key enzyme for lipid synthesis, showed strong selective sweep in the upstream noncoding region and lower transcription in the southern species. These results were further supported by the lower free fatty acid (FFA) but higher ATP content in southern species and habitat, pointing to significance of ATP/FFA trade-off. Our findings provide evidence that noncoding variation and transcriptional plasticity play important roles in shaping energy metabolism for thermal adaptation in oysters. Article in Journal/Newspaper Crassostrea gigas Oxford University Press Molecular Biology and Evolution |
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Open Polar |
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Oxford University Press |
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croxfordunivpr |
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English |
description |
Abstract Genetic variation and phenotypic plasticity are both important to adaptive evolution. However, how they act together on particular traits remains poorly understood. Here, we integrated phenotypic, genomic, and transcriptomic data from two allopatric but closely related congeneric oyster species, Crassostrea angulata from southern/warm environments and Crassostrea gigas from northern/cold environments, to investigate the roles of genetic divergence and plasticity in thermal adaptation. Reciprocal transplantation experiments showed that both species had higher fitness in their native habitats than in nonnative environments, indicating strong adaptive divergence. The southern species evolved higher transcriptional plasticity, and the plasticity was adaptive, suggesting that increased plasticity is important for thermal adaptation to warm climates. Genome-wide comparisons between the two species revealed that genes under selection tended to respond to environmental changes and showed higher sequence divergence in noncoding regions. All genes under selection and related to energy metabolism exhibited habitat-specific expression with genes involved in ATP production and lipid catabolism highly expressed in warm/southern habitats, and genes involved in ATP consumption and lipid synthesis were highly expressed in cold/northern habitats. The gene for acyl-CoA desaturase, a key enzyme for lipid synthesis, showed strong selective sweep in the upstream noncoding region and lower transcription in the southern species. These results were further supported by the lower free fatty acid (FFA) but higher ATP content in southern species and habitat, pointing to significance of ATP/FFA trade-off. Our findings provide evidence that noncoding variation and transcriptional plasticity play important roles in shaping energy metabolism for thermal adaptation in oysters. |
author2 |
Saitou, Naruya National Key R&D Program of China Strategic Priority Research Program of the Chinese Academy of Sciences Distinguished Young Scientists Research Fund of Key Laboratory of Experimental Marine Biology Chinese Academy of Sciences China Postdoctoral Science Foundation Key Deployment Project of Centre for Ocean Mega-Research of Science Chinese Academy of Sciences National Natural Science Foundation of China Technology and Modern Agro-Industry Technology Research System |
format |
Article in Journal/Newspaper |
author |
Li, Ao Li, Li Zhang, Ziyan Li, Shiming Wang, Wei Guo, Ximing Zhang, Guofan |
spellingShingle |
Li, Ao Li, Li Zhang, Ziyan Li, Shiming Wang, Wei Guo, Ximing Zhang, Guofan Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism |
author_facet |
Li, Ao Li, Li Zhang, Ziyan Li, Shiming Wang, Wei Guo, Ximing Zhang, Guofan |
author_sort |
Li, Ao |
title |
Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism |
title_short |
Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism |
title_full |
Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism |
title_fullStr |
Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism |
title_full_unstemmed |
Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism |
title_sort |
noncoding variation and transcriptional plasticity promote thermal adaptation in oysters by altering energy metabolism |
publisher |
Oxford University Press (OUP) |
publishDate |
2021 |
url |
http://dx.doi.org/10.1093/molbev/msab241 http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msab241/40256678/msab241.pdf http://academic.oup.com/mbe/article-pdf/38/11/5144/40935452/msab241.pdf |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
Molecular Biology and Evolution volume 38, issue 11, page 5144-5155 ISSN 0737-4038 1537-1719 |
op_rights |
https://creativecommons.org/licenses/by-nc/4.0/ |
op_doi |
https://doi.org/10.1093/molbev/msab241 |
container_title |
Molecular Biology and Evolution |
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1810440783912763392 |