Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation

Evidence from mammals and aves alludes to a possibly conserved seasonal photoperiod induced neuroendocrine cascade which stimulates subsequent sexual maturation however our understanding of this mechanism in teleosts is lacking. Unlike all teleosts studied to date, the Atlantic cod (Gadus morhua) is...

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Published in:Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Main Authors: Doyle, Alice, Cowan, Mairi E, Migaud, Herve, Wright, Peter J, Davie, Andrew
Other Authors: Marine Alliance for Science & Technology Scotland, Institute of Aquaculture, Scottish Government - Enterprise, Environment & Digital - Marine Scotland, orcid:0000-0002-5404-7512, orcid:0000-0002-9524-618X
Format: Article in Journal/Newspaper
Language:English
Published: Elsevier 2021
Subjects:
Online Access:http://hdl.handle.net/1893/33115
https://doi.org/10.1016/j.cbpa.2021.111000
http://dspace.stir.ac.uk/retrieve/709989b4-9854-433c-8930-79996e3a31bc/Graphical%20abstract_1_.tif
http://dspace.stir.ac.uk/retrieve/9d9f00e5-023b-4b58-8ff6-8ce20ea33122/Supplemental%20figures%20Doyle%20et%20al%20CBPA_revised1.pdf
http://dspace.stir.ac.uk/retrieve/5ef2dd5b-4008-4c6d-8584-ef9a95ba0474/Cod%20eya3%20Doyle%20et%20al%20CBPA_unmnarked1.pdf
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record_format openpolar
institution Open Polar
collection University of Stirling: Stirling Digital Research Repository
op_collection_id ftunivstirling
language English
topic Atlantic cod
eya3
dio2
tshβ
Reproduction
Photoperiod
Seasonality
spellingShingle Atlantic cod
eya3
dio2
tshβ
Reproduction
Photoperiod
Seasonality
Doyle, Alice
Cowan, Mairi E
Migaud, Herve
Wright, Peter J
Davie, Andrew
Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation
topic_facet Atlantic cod
eya3
dio2
tshβ
Reproduction
Photoperiod
Seasonality
description Evidence from mammals and aves alludes to a possibly conserved seasonal photoperiod induced neuroendocrine cascade which stimulates subsequent sexual maturation however our understanding of this mechanism in teleosts is lacking. Unlike all teleosts studied to date, the Atlantic cod (Gadus morhua) is a short day breeder with the reduction in day-length from the summer solstice stimulating gametogenesis. Cod specific orthologues of eya3, tshβ and dio2 were identified and their expression was monitored in the brain and pituitary of cod held under either stimulated or inhibited photoperiod conditions. While no differential expression was apparent in brain dio2 & tshβ and pituitary tshβ, there was significant temporal variation in expression of pituitary eya3 under the SNP treatment, with expression level elevating in association with active gametogenesis. Under the LL treatment, sexual maturation was inhibited and there was a corresponding suppression of eya3 expression. In a second study the impact of size/energetic status on the initiation of sexual maturation was investigated. In the feed restricted population maturation was significantly suppressed (5% sexually mature) compared to the ab libitum fed stock (95% sexually mature) with there being a concomitant significant suppression in pituitary eya3 expression. Overall, these results suggest that pituitary eya3 has the potential to act as an integrator of both environmental and energetic regulation of sexual maturation of cod. Being the first account of eya3 induction in a short day breeding teleost, the conserved association with stimulation of reproduction and not seasonal state indicates that the upstream drivers which initiate the pathway differ among vertebrates according to their breeding strategies, but the pathway itself and its role in the reproductive cascade appears to be conserved across the vertebrate clade.
author2 Marine Alliance for Science & Technology Scotland
Institute of Aquaculture
Scottish Government - Enterprise, Environment & Digital - Marine Scotland
orcid:0000-0002-5404-7512
orcid:0000-0002-9524-618X
format Article in Journal/Newspaper
author Doyle, Alice
Cowan, Mairi E
Migaud, Herve
Wright, Peter J
Davie, Andrew
author_facet Doyle, Alice
Cowan, Mairi E
Migaud, Herve
Wright, Peter J
Davie, Andrew
author_sort Doyle, Alice
title Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation
title_short Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation
title_full Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation
title_fullStr Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation
title_full_unstemmed Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation
title_sort neuroendocrine regulation of reproduction in atlantic cod (gadus morhua): evidence of eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation
publisher Elsevier
publishDate 2021
url http://hdl.handle.net/1893/33115
https://doi.org/10.1016/j.cbpa.2021.111000
http://dspace.stir.ac.uk/retrieve/709989b4-9854-433c-8930-79996e3a31bc/Graphical%20abstract_1_.tif
http://dspace.stir.ac.uk/retrieve/9d9f00e5-023b-4b58-8ff6-8ce20ea33122/Supplemental%20figures%20Doyle%20et%20al%20CBPA_revised1.pdf
http://dspace.stir.ac.uk/retrieve/5ef2dd5b-4008-4c6d-8584-ef9a95ba0474/Cod%20eya3%20Doyle%20et%20al%20CBPA_unmnarked1.pdf
genre atlantic cod
Gadus morhua
genre_facet atlantic cod
Gadus morhua
op_relation Doyle A, Cowan ME, Migaud H, Wright PJ & Davie A (2021) Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology, 260, Art. No.: 111000. https://doi.org/10.1016/j.cbpa.2021.111000
111000
http://hdl.handle.net/1893/33115
doi:10.1016/j.cbpa.2021.111000
34089890
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http://dspace.stir.ac.uk/retrieve/5ef2dd5b-4008-4c6d-8584-ef9a95ba0474/Cod%20eya3%20Doyle%20et%20al%20CBPA_unmnarked1.pdf
op_rights This item has been embargoed for a period. During the embargo please use the Request a Copy feature at the foot of the Repository record to request a copy directly from the author. You can only request a copy if you wish to use this work for your own research or private study. Accepted refereed manuscript of: Doyle A, Cowan ME, Migaud H, Wright PJ & Davie A (2021) Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology, 260, Art. No.: 111000. https://doi.org/10.1016/j.cbpa.2021.111000 © 2021, Elsevier. Licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/
http://creativecommons.org/licenses/by-nc-nd/4.0/
2022-06-03
[Cod eya3 Doyle et al CBPA_unmnarked1.pdf] Publisher requires embargo of 12 months after publication.
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op_doi https://doi.org/10.1016/j.cbpa.2021.111000
container_title Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
container_volume 260
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spelling ftunivstirling:oai:dspace.stir.ac.uk:1893/33115 2023-05-15T15:27:07+02:00 Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation Doyle, Alice Cowan, Mairi E Migaud, Herve Wright, Peter J Davie, Andrew Marine Alliance for Science & Technology Scotland Institute of Aquaculture Scottish Government - Enterprise, Environment & Digital - Marine Scotland orcid:0000-0002-5404-7512 orcid:0000-0002-9524-618X 2021-10 image/tiff application/pdf http://hdl.handle.net/1893/33115 https://doi.org/10.1016/j.cbpa.2021.111000 http://dspace.stir.ac.uk/retrieve/709989b4-9854-433c-8930-79996e3a31bc/Graphical%20abstract_1_.tif http://dspace.stir.ac.uk/retrieve/9d9f00e5-023b-4b58-8ff6-8ce20ea33122/Supplemental%20figures%20Doyle%20et%20al%20CBPA_revised1.pdf http://dspace.stir.ac.uk/retrieve/5ef2dd5b-4008-4c6d-8584-ef9a95ba0474/Cod%20eya3%20Doyle%20et%20al%20CBPA_unmnarked1.pdf en eng Elsevier Doyle A, Cowan ME, Migaud H, Wright PJ & Davie A (2021) Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology, 260, Art. No.: 111000. https://doi.org/10.1016/j.cbpa.2021.111000 111000 http://hdl.handle.net/1893/33115 doi:10.1016/j.cbpa.2021.111000 34089890 2-s2.0-85108066979 1734696 http://dspace.stir.ac.uk/retrieve/709989b4-9854-433c-8930-79996e3a31bc/Graphical%20abstract_1_.tif http://dspace.stir.ac.uk/retrieve/9d9f00e5-023b-4b58-8ff6-8ce20ea33122/Supplemental%20figures%20Doyle%20et%20al%20CBPA_revised1.pdf http://dspace.stir.ac.uk/retrieve/5ef2dd5b-4008-4c6d-8584-ef9a95ba0474/Cod%20eya3%20Doyle%20et%20al%20CBPA_unmnarked1.pdf This item has been embargoed for a period. During the embargo please use the Request a Copy feature at the foot of the Repository record to request a copy directly from the author. You can only request a copy if you wish to use this work for your own research or private study. Accepted refereed manuscript of: Doyle A, Cowan ME, Migaud H, Wright PJ & Davie A (2021) Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology, 260, Art. No.: 111000. https://doi.org/10.1016/j.cbpa.2021.111000 © 2021, Elsevier. Licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/ http://creativecommons.org/licenses/by-nc-nd/4.0/ 2022-06-03 [Cod eya3 Doyle et al CBPA_unmnarked1.pdf] Publisher requires embargo of 12 months after publication. CC-BY-NC-ND Atlantic cod eya3 dio2 tshβ Reproduction Photoperiod Seasonality Journal Article NA - Not Applicable (or Unknown) AM - Accepted Manuscript 2021 ftunivstirling https://doi.org/10.1016/j.cbpa.2021.111000 2022-06-13T18:42:43Z Evidence from mammals and aves alludes to a possibly conserved seasonal photoperiod induced neuroendocrine cascade which stimulates subsequent sexual maturation however our understanding of this mechanism in teleosts is lacking. Unlike all teleosts studied to date, the Atlantic cod (Gadus morhua) is a short day breeder with the reduction in day-length from the summer solstice stimulating gametogenesis. Cod specific orthologues of eya3, tshβ and dio2 were identified and their expression was monitored in the brain and pituitary of cod held under either stimulated or inhibited photoperiod conditions. While no differential expression was apparent in brain dio2 & tshβ and pituitary tshβ, there was significant temporal variation in expression of pituitary eya3 under the SNP treatment, with expression level elevating in association with active gametogenesis. Under the LL treatment, sexual maturation was inhibited and there was a corresponding suppression of eya3 expression. In a second study the impact of size/energetic status on the initiation of sexual maturation was investigated. In the feed restricted population maturation was significantly suppressed (5% sexually mature) compared to the ab libitum fed stock (95% sexually mature) with there being a concomitant significant suppression in pituitary eya3 expression. Overall, these results suggest that pituitary eya3 has the potential to act as an integrator of both environmental and energetic regulation of sexual maturation of cod. Being the first account of eya3 induction in a short day breeding teleost, the conserved association with stimulation of reproduction and not seasonal state indicates that the upstream drivers which initiate the pathway differ among vertebrates according to their breeding strategies, but the pathway itself and its role in the reproductive cascade appears to be conserved across the vertebrate clade. Article in Journal/Newspaper atlantic cod Gadus morhua University of Stirling: Stirling Digital Research Repository Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 260 111000