Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod

Abstract Although early embryonic protein production relies exclusively on maternal molecules such as messenger RNAs (mRNAs) incorporated into ovarian follicles, knowledge about any thermally induced, intergenerational effects is scarce in ectotherms. Here, we investigated how elevated temperatures...

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Published in:ICES Journal of Marine Science
Main Authors: Skjærven, Kaja H, Alix, Maud, Kleppe, Lene, Fernandes, Jorge M O, Whatmore, Paul, Nedoluzhko, Artem, Andersson, Eva, Kjesbu, Olav Sigurd
Other Authors: Grant, W Stewart, Research Council of Norway, CLIMRATES, Norwegian Fisheries Research Sales Tax System
Format: Article in Journal/Newspaper
Language:English
Published: Oxford University Press (OUP) 2024
Subjects:
Online Access:http://dx.doi.org/10.1093/icesjms/fsae025
https://academic.oup.com/icesjms/article-pdf/81/4/733/57945921/fsae025.pdf
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spelling croxfordunivpr:10.1093/icesjms/fsae025 2024-09-09T19:29:43+00:00 Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod Skjærven, Kaja H Alix, Maud Kleppe, Lene Fernandes, Jorge M O Whatmore, Paul Nedoluzhko, Artem Andersson, Eva Kjesbu, Olav Sigurd Grant, W Stewart Research Council of Norway CLIMRATES Norwegian Fisheries Research Sales Tax System 2024 http://dx.doi.org/10.1093/icesjms/fsae025 https://academic.oup.com/icesjms/article-pdf/81/4/733/57945921/fsae025.pdf en eng Oxford University Press (OUP) https://creativecommons.org/licenses/by/4.0/ ICES Journal of Marine Science volume 81, issue 4, page 733-747 ISSN 1054-3139 1095-9289 journal-article 2024 croxfordunivpr https://doi.org/10.1093/icesjms/fsae025 2024-06-17T04:18:46Z Abstract Although early embryonic protein production relies exclusively on maternal molecules such as messenger RNAs (mRNAs) incorporated into ovarian follicles, knowledge about any thermally induced, intergenerational effects is scarce in ectotherms. Here, we investigated how elevated temperatures (9°–12°C vs. 6°C) during oogenesis influenced the next generation by targeting maternal mRNAs in Atlantic cod (Gadus morhua) embryos, in view of up- and down-regulated genes in ovarian follicles of pre-spawning adults. Overall, the spawning female liver showed significantly higher levels of free amino acids and N-metabolites at 9°C than at 6°C. Higher-than-optimal temperatures induced adjustments in embryo transcriptome proportional to the temperature increase relative to the control group. The adjustments included alterations in maternal-effect genes, which are developmentally conserved among vertebrates. The transcriptomic differences for a selection of genes in embryos were reflected in ovarian follicles (containing multiple cell types) several months ahead of the spawning season, implying that environmental conditions of the adults are key for adjusting the genetic instructions for offspring development. This programming of fundamental traits from mother to offspring appears part of a sophisticated process to adapt the offspring to a changing ocean, though within life stage-specific, physiological thermal tolerance windows. Article in Journal/Newspaper atlantic cod Gadus morhua Oxford University Press ICES Journal of Marine Science 81 4 733 747
institution Open Polar
collection Oxford University Press
op_collection_id croxfordunivpr
language English
description Abstract Although early embryonic protein production relies exclusively on maternal molecules such as messenger RNAs (mRNAs) incorporated into ovarian follicles, knowledge about any thermally induced, intergenerational effects is scarce in ectotherms. Here, we investigated how elevated temperatures (9°–12°C vs. 6°C) during oogenesis influenced the next generation by targeting maternal mRNAs in Atlantic cod (Gadus morhua) embryos, in view of up- and down-regulated genes in ovarian follicles of pre-spawning adults. Overall, the spawning female liver showed significantly higher levels of free amino acids and N-metabolites at 9°C than at 6°C. Higher-than-optimal temperatures induced adjustments in embryo transcriptome proportional to the temperature increase relative to the control group. The adjustments included alterations in maternal-effect genes, which are developmentally conserved among vertebrates. The transcriptomic differences for a selection of genes in embryos were reflected in ovarian follicles (containing multiple cell types) several months ahead of the spawning season, implying that environmental conditions of the adults are key for adjusting the genetic instructions for offspring development. This programming of fundamental traits from mother to offspring appears part of a sophisticated process to adapt the offspring to a changing ocean, though within life stage-specific, physiological thermal tolerance windows.
author2 Grant, W Stewart
Research Council of Norway
CLIMRATES
Norwegian Fisheries Research Sales Tax System
format Article in Journal/Newspaper
author Skjærven, Kaja H
Alix, Maud
Kleppe, Lene
Fernandes, Jorge M O
Whatmore, Paul
Nedoluzhko, Artem
Andersson, Eva
Kjesbu, Olav Sigurd
spellingShingle Skjærven, Kaja H
Alix, Maud
Kleppe, Lene
Fernandes, Jorge M O
Whatmore, Paul
Nedoluzhko, Artem
Andersson, Eva
Kjesbu, Olav Sigurd
Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod
author_facet Skjærven, Kaja H
Alix, Maud
Kleppe, Lene
Fernandes, Jorge M O
Whatmore, Paul
Nedoluzhko, Artem
Andersson, Eva
Kjesbu, Olav Sigurd
author_sort Skjærven, Kaja H
title Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod
title_short Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod
title_full Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod
title_fullStr Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod
title_full_unstemmed Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod
title_sort ocean warming shapes embryonic developmental prospects of the next generation in atlantic cod
publisher Oxford University Press (OUP)
publishDate 2024
url http://dx.doi.org/10.1093/icesjms/fsae025
https://academic.oup.com/icesjms/article-pdf/81/4/733/57945921/fsae025.pdf
genre atlantic cod
Gadus morhua
genre_facet atlantic cod
Gadus morhua
op_source ICES Journal of Marine Science
volume 81, issue 4, page 733-747
ISSN 1054-3139 1095-9289
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.1093/icesjms/fsae025
container_title ICES Journal of Marine Science
container_volume 81
container_issue 4
container_start_page 733
op_container_end_page 747
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