Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon
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 d...
Published in: | Genome Biology and Evolution |
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2021
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ftuhipublicatio:oai:pure.atira.dk:publications/005f5198-de8c-4f93-b963-c50c24518b61 2024-01-28T10:04:31+01:00 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. 2021-03-22 https://pure.uhi.ac.uk/en/publications/005f5198-de8c-4f93-b963-c50c24518b61 https://doi.org/10.1093/gbe/evab059 http://www.scopus.com/inward/record.url?scp=85107088761&partnerID=8YFLogxK http://www.scopus.com/inward/citedby.url?scp=85107088761&partnerID=8YFLogxK eng eng info:eu-repo/semantics/openAccess Verta , J P , Barton , H J , Pritchard , V & Primmer , C R 2021 , ' Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon ' , Genome Biology and Evolution , vol. 13 , no. 5 , evab059 . https://doi.org/10.1093/gbe/evab059 Atlantic salmon ChIPmentation distribution of fitness effects gene regulation histone acetylation whole-genome duplication article 2021 ftuhipublicatio https://doi.org/10.1093/gbe/evab059 2024-01-04T23:21:25Z 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 University of the Highlands and Islands: Research Database of UHI Genome Biology and Evolution 13 5 |
institution |
Open Polar |
collection |
University of the Highlands and Islands: Research Database of UHI |
op_collection_id |
ftuhipublicatio |
language |
English |
topic |
Atlantic salmon ChIPmentation distribution of fitness effects gene regulation histone acetylation whole-genome duplication |
spellingShingle |
Atlantic salmon ChIPmentation distribution of fitness effects gene regulation histone acetylation whole-genome duplication 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 |
Atlantic salmon ChIPmentation distribution of fitness effects gene regulation histone acetylation whole-genome duplication |
description |
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. |
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 |
publishDate |
2021 |
url |
https://pure.uhi.ac.uk/en/publications/005f5198-de8c-4f93-b963-c50c24518b61 https://doi.org/10.1093/gbe/evab059 http://www.scopus.com/inward/record.url?scp=85107088761&partnerID=8YFLogxK http://www.scopus.com/inward/citedby.url?scp=85107088761&partnerID=8YFLogxK |
genre |
Atlantic salmon Salmo salar |
genre_facet |
Atlantic salmon Salmo salar |
op_source |
Verta , J P , Barton , H J , Pritchard , V & Primmer , C R 2021 , ' Genetic Drift Dominates Genome-Wide Regulatory Evolution Following an Ancient Whole-Genome Duplication in Atlantic Salmon ' , Genome Biology and Evolution , vol. 13 , no. 5 , evab059 . https://doi.org/10.1093/gbe/evab059 |
op_rights |
info:eu-repo/semantics/openAccess |
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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1789330231057711104 |