Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon
Abstract Whole-genome duplications (WGD) have been considered as springboards that potentiate lineage diversification through increasing functional redundancy. Divergence in gene regulatory elements is a central mechanism for evolutionary diversification, yet the patterns and processes governing reg...
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croxfordunivpr:10.1093/gbe/evab059 2024-04-07T07:51:08+00:00 Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon Verta, Jukka-Pekka Barton, Henry J Pritchard, Victoria Primmer, Craig R Yi, Soojin 2021 http://dx.doi.org/10.1093/gbe/evab059 http://academic.oup.com/gbe/advance-article-pdf/doi/10.1093/gbe/evab059/36656067/evab059.pdf http://academic.oup.com/gbe/article-pdf/13/5/evab059/38266254/evab059.pdf en eng Oxford University Press (OUP) http://creativecommons.org/licenses/by/4.0/ Genome Biology and Evolution volume 13, issue 5 ISSN 1759-6653 Genetics Ecology, Evolution, Behavior and Systematics journal-article 2021 croxfordunivpr https://doi.org/10.1093/gbe/evab059 2024-03-08T03:03:26Z Abstract Whole-genome duplications (WGD) have been considered as springboards that potentiate lineage diversification through increasing functional redundancy. Divergence in gene regulatory elements is a central mechanism for evolutionary diversification, yet the patterns and processes governing regulatory divergence following events that lead to massive functional redundancy, such as WGD, remain largely unknown. We studied the patterns of divergence and strength of natural selection on regulatory elements in the Atlantic salmon (Salmo salar) genome, which has undergone WGD 100–80 Ma. Using ChIPmentation, we first show that H3K27ac, a histone modification typical to enhancers and promoters, is associated with genic regions, tissue-specific transcription factor binding motifs, and with gene transcription levels in immature testes. Divergence in transcription between duplicated genes from WGD (ohnologs) correlated with difference in the number of proximal regulatory elements, but not with promoter elements, suggesting that functional divergence between ohnologs after WGD is mainly driven by enhancers. By comparing H3K27ac regions between duplicated genome blocks, we further show that a longer polyploid state post-WGD has constrained regulatory divergence. Patterns of genetic diversity across natural populations inferred from resequencing indicate that recent evolutionary pressures on H3K27ac regions are dominated by largely neutral evolution. In sum, our results suggest that post-WGD functional redundancy in regulatory elements continues to have an impact on the evolution of the salmon genome, promoting largely neutral evolution of regulatory elements despite their association with transcription levels. These results highlight a case where genome-wide regulatory evolution following an ancient WGD is dominated by genetic drift. Article in Journal/Newspaper Atlantic salmon Salmo salar Oxford University Press Genome Biology and Evolution 13 5 |
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Oxford University Press |
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croxfordunivpr |
language |
English |
topic |
Genetics Ecology, Evolution, Behavior and Systematics |
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Genetics Ecology, Evolution, Behavior and Systematics Verta, Jukka-Pekka Barton, Henry J Pritchard, Victoria Primmer, Craig R Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon |
topic_facet |
Genetics Ecology, Evolution, Behavior and Systematics |
description |
Abstract Whole-genome duplications (WGD) have been considered as springboards that potentiate lineage diversification through increasing functional redundancy. Divergence in gene regulatory elements is a central mechanism for evolutionary diversification, yet the patterns and processes governing regulatory divergence following events that lead to massive functional redundancy, such as WGD, remain largely unknown. We studied the patterns of divergence and strength of natural selection on regulatory elements in the Atlantic salmon (Salmo salar) genome, which has undergone WGD 100–80 Ma. Using ChIPmentation, we first show that H3K27ac, a histone modification typical to enhancers and promoters, is associated with genic regions, tissue-specific transcription factor binding motifs, and with gene transcription levels in immature testes. Divergence in transcription between duplicated genes from WGD (ohnologs) correlated with difference in the number of proximal regulatory elements, but not with promoter elements, suggesting that functional divergence between ohnologs after WGD is mainly driven by enhancers. By comparing H3K27ac regions between duplicated genome blocks, we further show that a longer polyploid state post-WGD has constrained regulatory divergence. Patterns of genetic diversity across natural populations inferred from resequencing indicate that recent evolutionary pressures on H3K27ac regions are dominated by largely neutral evolution. In sum, our results suggest that post-WGD functional redundancy in regulatory elements continues to have an impact on the evolution of the salmon genome, promoting largely neutral evolution of regulatory elements despite their association with transcription levels. These results highlight a case where genome-wide regulatory evolution following an ancient WGD is dominated by genetic drift. |
author2 |
Yi, Soojin |
format |
Article in Journal/Newspaper |
author |
Verta, Jukka-Pekka Barton, Henry J Pritchard, Victoria Primmer, Craig R |
author_facet |
Verta, Jukka-Pekka Barton, Henry J Pritchard, Victoria Primmer, Craig R |
author_sort |
Verta, Jukka-Pekka |
title |
Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon |
title_short |
Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon |
title_full |
Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon |
title_fullStr |
Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon |
title_full_unstemmed |
Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon |
title_sort |
genetic drift dominates genome-wide regulatory evolution following an ancient whole-genome duplication in atlantic salmon |
publisher |
Oxford University Press (OUP) |
publishDate |
2021 |
url |
http://dx.doi.org/10.1093/gbe/evab059 http://academic.oup.com/gbe/advance-article-pdf/doi/10.1093/gbe/evab059/36656067/evab059.pdf http://academic.oup.com/gbe/article-pdf/13/5/evab059/38266254/evab059.pdf |
genre |
Atlantic salmon Salmo salar |
genre_facet |
Atlantic salmon Salmo salar |
op_source |
Genome Biology and Evolution volume 13, issue 5 ISSN 1759-6653 |
op_rights |
http://creativecommons.org/licenses/by/4.0/ |
op_doi |
https://doi.org/10.1093/gbe/evab059 |
container_title |
Genome Biology and Evolution |
container_volume |
13 |
container_issue |
5 |
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1795665988400709632 |