Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes
Abstract Expression of multiple hemoglobin isoforms with differing physiochemical properties likely helps species adapt to different environmental and physiological conditions. Antarctic notothenioid fishes inhabit the icy Southern Ocean and display fewer hemoglobin isoforms, each with less affinity...
Published in: | Molecular Biology and Evolution |
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Oxford University Press (OUP)
2023
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Online Access: | http://dx.doi.org/10.1093/molbev/msad236 https://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msad236/52550827/msad236.pdf https://academic.oup.com/mbe/article-pdf/40/11/msad236/53676780/msad236.pdf |
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croxfordunivpr:10.1093/molbev/msad236 2024-01-07T09:38:54+01:00 Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes Desvignes, Thomas Bista, Iliana Herrera, Karina Landes, Audrey Postlethwait, John H Yang, Guang 2023 http://dx.doi.org/10.1093/molbev/msad236 https://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msad236/52550827/msad236.pdf https://academic.oup.com/mbe/article-pdf/40/11/msad236/53676780/msad236.pdf en eng Oxford University Press (OUP) https://creativecommons.org/licenses/by-nc/4.0/ Molecular Biology and Evolution volume 40, issue 11 ISSN 0737-4038 1537-1719 Genetics Molecular Biology Ecology, Evolution, Behavior and Systematics journal-article 2023 croxfordunivpr https://doi.org/10.1093/molbev/msad236 2023-12-08T09:41:16Z Abstract Expression of multiple hemoglobin isoforms with differing physiochemical properties likely helps species adapt to different environmental and physiological conditions. Antarctic notothenioid fishes inhabit the icy Southern Ocean and display fewer hemoglobin isoforms, each with less affinity for oxygen than temperate relatives. Reduced hemoglobin multiplicity was proposed to result from relaxed selective pressure in the cold, thermally stable, and highly oxygenated Antarctic waters. These conditions also permitted the survival and diversification of white-blooded icefishes, the only vertebrates living without hemoglobin. To understand hemoglobin evolution during adaptation to freezing water, we analyzed hemoglobin genes from 36 notothenioid genome assemblies. Results showed that adaptation to frigid conditions shaped hemoglobin gene evolution by episodic diversifying selection concomitant with cold adaptation and by pervasive evolution in Antarctic notothenioids compared to temperate relatives, likely a continuing adaptation to Antarctic conditions. Analysis of hemoglobin gene expression in adult hematopoietic organs in various temperate and Antarctic species further revealed a switch in hemoglobin gene expression underlying hemoglobin multiplicity reduction in Antarctic fish, leading to a single hemoglobin isoform in adult plunderfishes and dragonfishes, the sister groups to icefishes. The predicted high hemoglobin multiplicity in Antarctic fish embryos based on transcriptomic data, however, raises questions about the molecular bases and physiological implications of diverse hemoglobin isoforms in embryos compared to adults. This analysis supports the hypothesis that the last common icefish ancestor was vulnerable to detrimental mutations affecting the single ancestral expressed alpha- and beta-globin gene pair, potentially predisposing their subsequent loss. Article in Journal/Newspaper Antarc* Antarctic Icefish Southern Ocean Oxford University Press (via Crossref) Antarctic Southern Ocean Molecular Biology and Evolution |
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Open Polar |
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Oxford University Press (via Crossref) |
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croxfordunivpr |
language |
English |
topic |
Genetics Molecular Biology Ecology, Evolution, Behavior and Systematics |
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Genetics Molecular Biology Ecology, Evolution, Behavior and Systematics Desvignes, Thomas Bista, Iliana Herrera, Karina Landes, Audrey Postlethwait, John H Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes |
topic_facet |
Genetics Molecular Biology Ecology, Evolution, Behavior and Systematics |
description |
Abstract Expression of multiple hemoglobin isoforms with differing physiochemical properties likely helps species adapt to different environmental and physiological conditions. Antarctic notothenioid fishes inhabit the icy Southern Ocean and display fewer hemoglobin isoforms, each with less affinity for oxygen than temperate relatives. Reduced hemoglobin multiplicity was proposed to result from relaxed selective pressure in the cold, thermally stable, and highly oxygenated Antarctic waters. These conditions also permitted the survival and diversification of white-blooded icefishes, the only vertebrates living without hemoglobin. To understand hemoglobin evolution during adaptation to freezing water, we analyzed hemoglobin genes from 36 notothenioid genome assemblies. Results showed that adaptation to frigid conditions shaped hemoglobin gene evolution by episodic diversifying selection concomitant with cold adaptation and by pervasive evolution in Antarctic notothenioids compared to temperate relatives, likely a continuing adaptation to Antarctic conditions. Analysis of hemoglobin gene expression in adult hematopoietic organs in various temperate and Antarctic species further revealed a switch in hemoglobin gene expression underlying hemoglobin multiplicity reduction in Antarctic fish, leading to a single hemoglobin isoform in adult plunderfishes and dragonfishes, the sister groups to icefishes. The predicted high hemoglobin multiplicity in Antarctic fish embryos based on transcriptomic data, however, raises questions about the molecular bases and physiological implications of diverse hemoglobin isoforms in embryos compared to adults. This analysis supports the hypothesis that the last common icefish ancestor was vulnerable to detrimental mutations affecting the single ancestral expressed alpha- and beta-globin gene pair, potentially predisposing their subsequent loss. |
author2 |
Yang, Guang |
format |
Article in Journal/Newspaper |
author |
Desvignes, Thomas Bista, Iliana Herrera, Karina Landes, Audrey Postlethwait, John H |
author_facet |
Desvignes, Thomas Bista, Iliana Herrera, Karina Landes, Audrey Postlethwait, John H |
author_sort |
Desvignes, Thomas |
title |
Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes |
title_short |
Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes |
title_full |
Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes |
title_fullStr |
Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes |
title_full_unstemmed |
Cold-Driven Hemoglobin Evolution in Antarctic Notothenioid Fishes Prior to Hemoglobin Gene Loss in White-Blooded Icefishes |
title_sort |
cold-driven hemoglobin evolution in antarctic notothenioid fishes prior to hemoglobin gene loss in white-blooded icefishes |
publisher |
Oxford University Press (OUP) |
publishDate |
2023 |
url |
http://dx.doi.org/10.1093/molbev/msad236 https://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msad236/52550827/msad236.pdf https://academic.oup.com/mbe/article-pdf/40/11/msad236/53676780/msad236.pdf |
geographic |
Antarctic Southern Ocean |
geographic_facet |
Antarctic Southern Ocean |
genre |
Antarc* Antarctic Icefish Southern Ocean |
genre_facet |
Antarc* Antarctic Icefish Southern Ocean |
op_source |
Molecular Biology and Evolution volume 40, issue 11 ISSN 0737-4038 1537-1719 |
op_rights |
https://creativecommons.org/licenses/by-nc/4.0/ |
op_doi |
https://doi.org/10.1093/molbev/msad236 |
container_title |
Molecular Biology and Evolution |
_version_ |
1787426866116689920 |