Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism
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, Cra...
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ftpubmed:oai:pubmedcentral.nih.gov:8557435 2023-05-15T15:58:54+02:00 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 2021-08-15 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557435/ http://www.ncbi.nlm.nih.gov/pubmed/34390581 https://doi.org/10.1093/molbev/msab241 en eng Oxford University Press http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557435/ http://www.ncbi.nlm.nih.gov/pubmed/34390581 http://dx.doi.org/10.1093/molbev/msab241 © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com CC-BY-NC Mol Biol Evol Discoveries Text 2021 ftpubmed https://doi.org/10.1093/molbev/msab241 2021-11-07T01:47:32Z 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. Text Crassostrea gigas PubMed Central (PMC) Molecular Biology and Evolution 38 11 5144 5155 |
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Discoveries 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 |
topic_facet |
Discoveries |
description |
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. |
format |
Text |
author |
Li, Ao Li, Li Zhang, Ziyan Li, Shiming Wang, Wei Guo, Ximing Zhang, Guofan |
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 |
publishDate |
2021 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557435/ http://www.ncbi.nlm.nih.gov/pubmed/34390581 https://doi.org/10.1093/molbev/msab241 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
Mol Biol Evol |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557435/ http://www.ncbi.nlm.nih.gov/pubmed/34390581 http://dx.doi.org/10.1093/molbev/msab241 |
op_rights |
© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
op_rightsnorm |
CC-BY-NC |
op_doi |
https://doi.org/10.1093/molbev/msab241 |
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Molecular Biology and Evolution |
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38 |
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11 |
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5144 |
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5155 |
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1766394666743234560 |