Genomics of cold adaptations in the Antarctic notothenioid fish radiation

Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgro...

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Published inNature communications Vol. 14; no. 1; pp. 3412 - 16
Main Authors Bista, Iliana, Wood, Jonathan M. D., Desvignes, Thomas, McCarthy, Shane A., Matschiner, Michael, Ning, Zemin, Tracey, Alan, Torrance, James, Sims, Ying, Chow, William, Smith, Michelle, Oliver, Karen, Haggerty, Leanne, Salzburger, Walter, Postlethwait, John H., Howe, Kerstin, Clark, Melody S., William Detrich, H., Christina Cheng, C.-H., Miska, Eric A., Durbin, Richard
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 09.06.2023
Nature Publishing Group
Nature Portfolio
Subjects
45
45/23
45/91
631/181/2474
631/181/759/2467
631/208/182
631/208/212/748
Adaptation
Animals
Antarctic Regions
Antifreeze glycoproteins
Assemblies
Evolution
Fish
Fishes - genetics
Freezing
Gene clusters
Genes
Genomes
Genomic analysis
Genomics
Glycoproteins
Hemoglobin
Hemoglobins - genetics
Humanities and Social Sciences
multidisciplinary
Nucleotide sequence
Perciformes
Phylogeny
Radiation
Reconstruction
Science
Science (multidisciplinary)
Subgroups
Vertebrates
Antarctic Regions
Southern Ocean
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-023-38567-6

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Abstract Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use the long-read data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes. The notothenioid radiation is a remarkable group of fish adapted to life in the icy waters of the Southern Ocean. This study investigates the evolutionary history of this group and the basis of their adaption to cold environments through genomic analysis of 24 new genome assemblies.
AbstractList Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use the long-read data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes. The notothenioid radiation is a remarkable group of fish adapted to life in the icy waters of the Southern Ocean. This study investigates the evolutionary history of this group and the basis of their adaption to cold environments through genomic analysis of 24 new genome assemblies.
Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use the long-read data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes.Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use the long-read data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes.
Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use the long-read data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes.
Abstract Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use the long-read data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes.
Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve understanding of the evolution of this iconic fish group, here we generate and analyse new genome assemblies for 24 species covering all major subgroups of the radiation, including five long-read assemblies. We present a new estimate for the onset of the radiation at 10.7 million years ago, based on a time-calibrated phylogeny derived from genome-wide sequence data. We identify a two-fold variation in genome size, driven by expansion of multiple transposable element families, and use the long-read data to reconstruct two evolutionarily important, highly repetitive gene family loci. First, we present the most complete reconstruction to date of the antifreeze glycoprotein gene family, whose emergence enabled survival in sub-zero temperatures, showing the expansion of the antifreeze gene locus from the ancestral to the derived state. Second, we trace the loss of haemoglobin genes in icefishes, the only vertebrates lacking functional haemoglobins, through complete reconstruction of the two haemoglobin gene clusters across notothenioid families. Both the haemoglobin and antifreeze genomic loci are characterised by multiple transposon expansions that may have driven the evolutionary history of these genes.The notothenioid radiation is a remarkable group of fish adapted to life in the icy waters of the Southern Ocean. This study investigates the evolutionary history of this group and the basis of their adaption to cold environments through genomic analysis of 24 new genome assemblies.
ArticleNumber 3412
Author Ning, Zemin
Wood, Jonathan M. D.
McCarthy, Shane A.
William Detrich, H.
Torrance, James
Sims, Ying
Clark, Melody S.
Tracey, Alan
Howe, Kerstin
Christina Cheng, C.-H.
Durbin, Richard
Haggerty, Leanne
Oliver, Karen
Postlethwait, John H.
Desvignes, Thomas
Chow, William
Miska, Eric A.
Bista, Iliana
Matschiner, Michael
Salzburger, Walter
Smith, Michelle
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37296119$$D View this record in MEDLINE/PubMed
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Snippet Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve...
Abstract Numerous novel adaptations characterise the radiation of notothenioids, the dominant fish group in the freezing seas of the Southern Ocean. To improve...
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SubjectTerms 45
45/23
45/91
631/181/2474
631/181/759/2467
631/208/182
631/208/212/748
Adaptation
Animals
Antarctic Regions
Antifreeze glycoproteins
Assemblies
Evolution
Fish
Fishes - genetics
Freezing
Gene clusters
Genes
Genomes
Genomic analysis
Genomics
Glycoproteins
Hemoglobin
Hemoglobins - genetics
Humanities and Social Sciences
multidisciplinary
Nucleotide sequence
Perciformes
Phylogeny
Radiation
Reconstruction
Science
Science (multidisciplinary)
Subgroups
Vertebrates
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Title Genomics of cold adaptations in the Antarctic notothenioid fish radiation
URI https://link.springer.com/article/10.1038/s41467-023-38567-6
https://www.ncbi.nlm.nih.gov/pubmed/37296119
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https://pubmed.ncbi.nlm.nih.gov/PMC10256766
https://doaj.org/article/a84ba1265012436ab251e62f2ecd1c47
Volume 14
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