Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change
In the frigid, oxygen-rich Southern Ocean (SO), Antarctic icefishes (Channichthyidae; Notothenioidei) evolved the ability to survive without producing erythrocytes and hemoglobin, the oxygen-transport system of virtually all vertebrates. Here, we integrate paleoclimate records with an extensive phyl...
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Online Access: | http://dx.doi.org/10.1371/journal.pgen.1009173 https://dx.plos.org/10.1371/journal.pgen.1009173 |
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crplos:10.1371/journal.pgen.1009173 2024-05-19T07:31:17+00:00 Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change Daane, Jacob M. Auvinet, Juliette Stoebenau, Alicia Yergeau, Donald Harris, Matthew P. Detrich, H. William Mullins, Mary C. American Heart Association National Science Foundation National Science Foundation John Simon Guggenheim Memorial Foundation National Science Foundation 2020 http://dx.doi.org/10.1371/journal.pgen.1009173 https://dx.plos.org/10.1371/journal.pgen.1009173 en eng Public Library of Science (PLoS) http://creativecommons.org/licenses/by/4.0/ PLOS Genetics volume 16, issue 10, page e1009173 ISSN 1553-7404 journal-article 2020 crplos https://doi.org/10.1371/journal.pgen.1009173 2024-05-01T06:56:32Z In the frigid, oxygen-rich Southern Ocean (SO), Antarctic icefishes (Channichthyidae; Notothenioidei) evolved the ability to survive without producing erythrocytes and hemoglobin, the oxygen-transport system of virtually all vertebrates. Here, we integrate paleoclimate records with an extensive phylogenomic dataset of notothenioid fishes to understand the evolution of trait loss associated with climate change. In contrast to buoyancy adaptations in this clade, we find relaxed selection on the genetic regions controlling erythropoiesis evolved only after sustained cooling in the SO. This pattern is seen not only within icefishes but also occurred independently in other high-latitude notothenioids. We show that one species of the red-blooded dragonfish clade evolved a spherocytic anemia that phenocopies human patients with this disease via orthologous mutations. The genomic imprint of SO climate change is biased toward erythrocyte-associated conserved noncoding elements (CNEs) rather than to coding regions, which are largely preserved through pleiotropy. The drift in CNEs is specifically enriched near genes that are preferentially expressed late in erythropoiesis. Furthermore, we find that the hematopoietic marrow of icefish species retained proerythroblasts, which indicates that early erythroid development remains intact. Our results provide a framework for understanding the interactions between development and the genome in shaping the response of species to climate change. Article in Journal/Newspaper Antarc* Antarctic Icefish Southern Ocean PLOS PLOS Genetics 16 10 e1009173 |
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English |
description |
In the frigid, oxygen-rich Southern Ocean (SO), Antarctic icefishes (Channichthyidae; Notothenioidei) evolved the ability to survive without producing erythrocytes and hemoglobin, the oxygen-transport system of virtually all vertebrates. Here, we integrate paleoclimate records with an extensive phylogenomic dataset of notothenioid fishes to understand the evolution of trait loss associated with climate change. In contrast to buoyancy adaptations in this clade, we find relaxed selection on the genetic regions controlling erythropoiesis evolved only after sustained cooling in the SO. This pattern is seen not only within icefishes but also occurred independently in other high-latitude notothenioids. We show that one species of the red-blooded dragonfish clade evolved a spherocytic anemia that phenocopies human patients with this disease via orthologous mutations. The genomic imprint of SO climate change is biased toward erythrocyte-associated conserved noncoding elements (CNEs) rather than to coding regions, which are largely preserved through pleiotropy. The drift in CNEs is specifically enriched near genes that are preferentially expressed late in erythropoiesis. Furthermore, we find that the hematopoietic marrow of icefish species retained proerythroblasts, which indicates that early erythroid development remains intact. Our results provide a framework for understanding the interactions between development and the genome in shaping the response of species to climate change. |
author2 |
Mullins, Mary C. American Heart Association National Science Foundation National Science Foundation John Simon Guggenheim Memorial Foundation National Science Foundation |
format |
Article in Journal/Newspaper |
author |
Daane, Jacob M. Auvinet, Juliette Stoebenau, Alicia Yergeau, Donald Harris, Matthew P. Detrich, H. William |
spellingShingle |
Daane, Jacob M. Auvinet, Juliette Stoebenau, Alicia Yergeau, Donald Harris, Matthew P. Detrich, H. William Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change |
author_facet |
Daane, Jacob M. Auvinet, Juliette Stoebenau, Alicia Yergeau, Donald Harris, Matthew P. Detrich, H. William |
author_sort |
Daane, Jacob M. |
title |
Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change |
title_short |
Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change |
title_full |
Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change |
title_fullStr |
Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change |
title_full_unstemmed |
Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change |
title_sort |
developmental constraint shaped genome evolution and erythrocyte loss in antarctic fishes following paleoclimate change |
publisher |
Public Library of Science (PLoS) |
publishDate |
2020 |
url |
http://dx.doi.org/10.1371/journal.pgen.1009173 https://dx.plos.org/10.1371/journal.pgen.1009173 |
genre |
Antarc* Antarctic Icefish Southern Ocean |
genre_facet |
Antarc* Antarctic Icefish Southern Ocean |
op_source |
PLOS Genetics volume 16, issue 10, page e1009173 ISSN 1553-7404 |
op_rights |
http://creativecommons.org/licenses/by/4.0/ |
op_doi |
https://doi.org/10.1371/journal.pgen.1009173 |
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PLOS Genetics |
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16 |
container_issue |
10 |
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e1009173 |
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1799469130986815488 |