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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ftpubmed:oai:pubmedcentral.nih.gov:7660546 2023-05-15T13:57:32+02:00 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 2020-10-27 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7660546/ http://www.ncbi.nlm.nih.gov/pubmed/33108368 https://doi.org/10.1371/journal.pgen.1009173 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7660546/ http://www.ncbi.nlm.nih.gov/pubmed/33108368 http://dx.doi.org/10.1371/journal.pgen.1009173 © 2020 Daane et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. CC-BY PLoS Genet Research Article Text 2020 ftpubmed https://doi.org/10.1371/journal.pgen.1009173 2020-11-22T01:32:35Z 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. Text Antarc* Antarctic Icefish Southern Ocean PubMed Central (PMC) Antarctic Southern Ocean PLOS Genetics 16 10 e1009173 |
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Research Article |
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Research Article 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 |
topic_facet |
Research Article |
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. |
format |
Text |
author |
Daane, Jacob M. Auvinet, Juliette Stoebenau, Alicia Yergeau, Donald Harris, Matthew P. Detrich, H. William |
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 |
publishDate |
2020 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7660546/ http://www.ncbi.nlm.nih.gov/pubmed/33108368 https://doi.org/10.1371/journal.pgen.1009173 |
geographic |
Antarctic Southern Ocean |
geographic_facet |
Antarctic Southern Ocean |
genre |
Antarc* Antarctic Icefish Southern Ocean |
genre_facet |
Antarc* Antarctic Icefish Southern Ocean |
op_source |
PLoS Genet |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7660546/ http://www.ncbi.nlm.nih.gov/pubmed/33108368 http://dx.doi.org/10.1371/journal.pgen.1009173 |
op_rights |
© 2020 Daane et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1371/journal.pgen.1009173 |
container_title |
PLOS Genetics |
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16 |
container_issue |
10 |
container_start_page |
e1009173 |
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1766265201742577664 |