Chromosome aberrations in pressure-induced triploid Atlantic salmon

Abstract Background Triploid organisms have three sets of chromosomes. In Atlantic salmon, hydrostatic pressure treatment of newly fertilized eggs has been extensively used to produce triploids which are functionally sterile due to their unpaired chromosomes. These fish often perform poorly on comme...

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Main Authors: K. A. Glover, A. C. Harvey, T. J. Hansen, P. G. Fjelldal, F. N. Besnier, J. B. Bos, F. Ayllon, J. B. Taggart, M. F. Solberg
Format: Article
Language:English
Published: BMC 2020-06-01
Series:BMC Genetics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12863-020-00864-0
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author K. A. Glover
A. C. Harvey
T. J. Hansen
P. G. Fjelldal
F. N. Besnier
J. B. Bos
F. Ayllon
J. B. Taggart
M. F. Solberg
author_facet K. A. Glover
A. C. Harvey
T. J. Hansen
P. G. Fjelldal
F. N. Besnier
J. B. Bos
F. Ayllon
J. B. Taggart
M. F. Solberg
author_sort K. A. Glover
collection DOAJ
description Abstract Background Triploid organisms have three sets of chromosomes. In Atlantic salmon, hydrostatic pressure treatment of newly fertilized eggs has been extensively used to produce triploids which are functionally sterile due to their unpaired chromosomes. These fish often perform poorly on commercial farms, sometimes without explanation. Inheritance patterns in individuals subjected to pressure treatment have not been investigated in Atlantic salmon thus far. However, work on other species suggests that this treatment can result in aberrant inheritance. We therefore studied this in Atlantic salmon by genotyping 16 polymorphic microsatellites in eyed eggs and juveniles which had been subjected to pressure-induction of triploidy. Communally reared juveniles including fish subjected to pressure-induction of triploidy and their diploid siblings were included as a control. Results No diploid offspring were detected in any of the eggs or juveniles which were subjected to hydrostatic pressure; therefore, the induction of triploidy was highly successful. Aberrant inheritance was nevertheless observed in 0.9% of the eggs and 0.9% of the juveniles that had been subjected to pressure treatment. In the communally reared fish, 0.3% of the fish subjected to pressure treatment displayed aberrant inheritance, while their diploid controls displayed 0% aberrant inheritance. Inheritance errors included two eyed eggs lacking maternal DNA across all microsatellites, and, examples in both eggs and juveniles of either the maternal or paternal allele lacking in one of the microsatellites. All individuals displaying chromosome aberrations were otherwise triploid. Conclusions This is the first study to document aberrant inheritance in Atlantic salmon that have been subjected to pressure-induction of triploidy. Our experiments unequivocally demonstrate that even when induction of triploidy is highly successful, this treatment can cause chromosome aberrations in this species. Based upon our novel data, and earlier studies in other organisms, we hypothesize that in batches of Atlantic salmon where low to modest triploid induction rates have been reported, aberrant inheritance is likely to be higher than the rates observed here. Therefore, we tentatively suggest that this could contribute to the unexplained poor performance of triploid salmon that is occasionally reported in commercial aquaculture. These hypotheses require further investigation.
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spelling doaj.art-4ee63a75b135432ea2cfb857f9ee42f72022-12-22T03:02:35ZengBMCBMC Genetics1471-21562020-06-0121111110.1186/s12863-020-00864-0Chromosome aberrations in pressure-induced triploid Atlantic salmonK. A. Glover0A. C. Harvey1T. J. Hansen2P. G. Fjelldal3F. N. Besnier4J. B. Bos5F. Ayllon6J. B. Taggart7M. F. Solberg8Institute of Marine ResearchInstitute of Marine ResearchInstitute of Marine ResearchInstitute of Marine ResearchInstitute of Marine ResearchZEBCAREInstitute of Marine ResearchUniversity of StirlingInstitute of Marine ResearchAbstract Background Triploid organisms have three sets of chromosomes. In Atlantic salmon, hydrostatic pressure treatment of newly fertilized eggs has been extensively used to produce triploids which are functionally sterile due to their unpaired chromosomes. These fish often perform poorly on commercial farms, sometimes without explanation. Inheritance patterns in individuals subjected to pressure treatment have not been investigated in Atlantic salmon thus far. However, work on other species suggests that this treatment can result in aberrant inheritance. We therefore studied this in Atlantic salmon by genotyping 16 polymorphic microsatellites in eyed eggs and juveniles which had been subjected to pressure-induction of triploidy. Communally reared juveniles including fish subjected to pressure-induction of triploidy and their diploid siblings were included as a control. Results No diploid offspring were detected in any of the eggs or juveniles which were subjected to hydrostatic pressure; therefore, the induction of triploidy was highly successful. Aberrant inheritance was nevertheless observed in 0.9% of the eggs and 0.9% of the juveniles that had been subjected to pressure treatment. In the communally reared fish, 0.3% of the fish subjected to pressure treatment displayed aberrant inheritance, while their diploid controls displayed 0% aberrant inheritance. Inheritance errors included two eyed eggs lacking maternal DNA across all microsatellites, and, examples in both eggs and juveniles of either the maternal or paternal allele lacking in one of the microsatellites. All individuals displaying chromosome aberrations were otherwise triploid. Conclusions This is the first study to document aberrant inheritance in Atlantic salmon that have been subjected to pressure-induction of triploidy. Our experiments unequivocally demonstrate that even when induction of triploidy is highly successful, this treatment can cause chromosome aberrations in this species. Based upon our novel data, and earlier studies in other organisms, we hypothesize that in batches of Atlantic salmon where low to modest triploid induction rates have been reported, aberrant inheritance is likely to be higher than the rates observed here. Therefore, we tentatively suggest that this could contribute to the unexplained poor performance of triploid salmon that is occasionally reported in commercial aquaculture. These hypotheses require further investigation.http://link.springer.com/article/10.1186/s12863-020-00864-0TriploidTrisomyAneuploidPUDMosaicAquaculture
spellingShingle K. A. Glover
A. C. Harvey
T. J. Hansen
P. G. Fjelldal
F. N. Besnier
J. B. Bos
F. Ayllon
J. B. Taggart
M. F. Solberg
Chromosome aberrations in pressure-induced triploid Atlantic salmon
BMC Genetics
Triploid
Trisomy
Aneuploid
PUD
Mosaic
Aquaculture
title Chromosome aberrations in pressure-induced triploid Atlantic salmon
title_full Chromosome aberrations in pressure-induced triploid Atlantic salmon
title_fullStr Chromosome aberrations in pressure-induced triploid Atlantic salmon
title_full_unstemmed Chromosome aberrations in pressure-induced triploid Atlantic salmon
title_short Chromosome aberrations in pressure-induced triploid Atlantic salmon
title_sort chromosome aberrations in pressure induced triploid atlantic salmon
topic Triploid
Trisomy
Aneuploid
PUD
Mosaic
Aquaculture
url http://link.springer.com/article/10.1186/s12863-020-00864-0
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