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Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link

BACKGROUND: Farmed Atlantic salmon are one of the most economically significant global aquaculture products. Early sexual maturation of farmed males represents a significant challenge to this industry and has been linked with the vgll3 genotype. However, tools to aid research of this topic, such as...

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Autores principales: Fjelldal, Per Gunnar, Hansen, Tom J., Wargelius, Anna, Ayllon, Fernando, Glover, Kevin A., Schulz, Rüdiger W., Fraser, Thomas W. K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7664053/
https://www.ncbi.nlm.nih.gov/pubmed/33183224
http://dx.doi.org/10.1186/s12863-020-00927-2
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author Fjelldal, Per Gunnar
Hansen, Tom J.
Wargelius, Anna
Ayllon, Fernando
Glover, Kevin A.
Schulz, Rüdiger W.
Fraser, Thomas W. K.
author_facet Fjelldal, Per Gunnar
Hansen, Tom J.
Wargelius, Anna
Ayllon, Fernando
Glover, Kevin A.
Schulz, Rüdiger W.
Fraser, Thomas W. K.
author_sort Fjelldal, Per Gunnar
collection PubMed
description BACKGROUND: Farmed Atlantic salmon are one of the most economically significant global aquaculture products. Early sexual maturation of farmed males represents a significant challenge to this industry and has been linked with the vgll3 genotype. However, tools to aid research of this topic, such as all-male and clonal fish, are still lacking. The present 6-year study examined if all-male production is possible in Atlantic salmon, a species with heteromorphic sex chromosomes (males being XY, females XX), and if all-male fish can be applied to further explore the vgll3 contribution on the likelihood of early maturation. RESULTS: Estrogen treatment of mixed sex yolk sac larvae gave rise to one sexually mature hermaphrodite with a male genotype (XY) that was used to produce both self-fertilized offspring and androgenetic double haploid (dh) offspring following egg activation with UV treated sperm and pressure shock to block the first mitotic division. There were YY supermales among both offspring types, which were crossed with dh females. Between 1 and 8% of the putative all-male offspring from the eight crosses with self-fertilized supermales were found to have ovaries, and 95% of these phenotypic females were also genetically female. None of the offspring from the one dh supermale cross had ovaries. When assessing the general contribution of the vgll3 locus on the likelihood of early post-smolt sexual maturation (jacking) in the all-male populations we found individuals that were homozygous for the early maturing genotype (97%) were more likely to enter puberty than individuals that were homozygous for the late maturing genotype (26%). However, the likelihood of jacking within individuals with an early/late heterozygous genotype was higher when the early allele came from the dam (94%) compared to the sire (45%). CONCLUSIONS: The present results show that supermale Atlantic salmon are viable and fertile and can be used as a research tool to study important aspects of sexual maturation, such as to further explore the sex dependent parental genetic contribution to age at puberty in Atlantic salmon. In addition, we report the production of viable double haploid supermale fish. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12863-020-00927-2.
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spelling pubmed-76640532020-11-13 Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link Fjelldal, Per Gunnar Hansen, Tom J. Wargelius, Anna Ayllon, Fernando Glover, Kevin A. Schulz, Rüdiger W. Fraser, Thomas W. K. BMC Genet Research Article BACKGROUND: Farmed Atlantic salmon are one of the most economically significant global aquaculture products. Early sexual maturation of farmed males represents a significant challenge to this industry and has been linked with the vgll3 genotype. However, tools to aid research of this topic, such as all-male and clonal fish, are still lacking. The present 6-year study examined if all-male production is possible in Atlantic salmon, a species with heteromorphic sex chromosomes (males being XY, females XX), and if all-male fish can be applied to further explore the vgll3 contribution on the likelihood of early maturation. RESULTS: Estrogen treatment of mixed sex yolk sac larvae gave rise to one sexually mature hermaphrodite with a male genotype (XY) that was used to produce both self-fertilized offspring and androgenetic double haploid (dh) offspring following egg activation with UV treated sperm and pressure shock to block the first mitotic division. There were YY supermales among both offspring types, which were crossed with dh females. Between 1 and 8% of the putative all-male offspring from the eight crosses with self-fertilized supermales were found to have ovaries, and 95% of these phenotypic females were also genetically female. None of the offspring from the one dh supermale cross had ovaries. When assessing the general contribution of the vgll3 locus on the likelihood of early post-smolt sexual maturation (jacking) in the all-male populations we found individuals that were homozygous for the early maturing genotype (97%) were more likely to enter puberty than individuals that were homozygous for the late maturing genotype (26%). However, the likelihood of jacking within individuals with an early/late heterozygous genotype was higher when the early allele came from the dam (94%) compared to the sire (45%). CONCLUSIONS: The present results show that supermale Atlantic salmon are viable and fertile and can be used as a research tool to study important aspects of sexual maturation, such as to further explore the sex dependent parental genetic contribution to age at puberty in Atlantic salmon. In addition, we report the production of viable double haploid supermale fish. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12863-020-00927-2. BioMed Central 2020-11-12 /pmc/articles/PMC7664053/ /pubmed/33183224 http://dx.doi.org/10.1186/s12863-020-00927-2 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Fjelldal, Per Gunnar
Hansen, Tom J.
Wargelius, Anna
Ayllon, Fernando
Glover, Kevin A.
Schulz, Rüdiger W.
Fraser, Thomas W. K.
Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link
title Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link
title_full Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link
title_fullStr Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link
title_full_unstemmed Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link
title_short Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link
title_sort development of supermale and all-male atlantic salmon to research the vgll3 allele - puberty link
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7664053/
https://www.ncbi.nlm.nih.gov/pubmed/33183224
http://dx.doi.org/10.1186/s12863-020-00927-2
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