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Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon

Meiotic recombination through chromosomal crossovers ensures proper segregation of homologous chromosomes during meiosis, while also breaking down linkage disequilibrium and shuffling alleles at loci located on the same chromosome. Rates of recombination can vary between species, but also between an...

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Autores principales: Brekke, Cathrine, Johnston, Susan E., Knutsen, Tim M., Berg, Peer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10665409/
https://www.ncbi.nlm.nih.gov/pubmed/37993527
http://dx.doi.org/10.1038/s41598-023-47208-3
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author Brekke, Cathrine
Johnston, Susan E.
Knutsen, Tim M.
Berg, Peer
author_facet Brekke, Cathrine
Johnston, Susan E.
Knutsen, Tim M.
Berg, Peer
author_sort Brekke, Cathrine
collection PubMed
description Meiotic recombination through chromosomal crossovers ensures proper segregation of homologous chromosomes during meiosis, while also breaking down linkage disequilibrium and shuffling alleles at loci located on the same chromosome. Rates of recombination can vary between species, but also between and within individuals, sex and chromosomes within species. Indeed, the Atlantic salmon genome is known to have clear sex differences in recombination with female biased heterochiasmy and markedly different landscapes of crossovers between males and females. In male meiosis, crossovers occur strictly in the telomeric regions, whereas in female meiosis crossovers tend to occur closer to the centromeres. However, little is known about the genetic control of these patterns and how this differs at the individual level. Here, we investigate genetic variation in individual measures of recombination in > 5000 large full-sib families of a Norwegian Atlantic salmon breeding population with high-density SNP genotypes. We show that females had 1.6 × higher crossover counts (CC) than males, with autosomal linkage maps spanning a total of 2174 cM in females and 1483 cM in males. However, because of the extreme telomeric bias of male crossovers, female recombination is much more important for generation of new haplotypes with 8 × higher intra-chromosomal genetic shuffling than males. CC was heritable in females (h(2) = 0.11) and males (h(2) = 0.10), and shuffling was also heritable in both sex but with a lower heritability in females (h(2) = 0.06) than in males (h(2) = 0.11). Inter-sex genetic correlations for both traits were close to zero, suggesting that rates and distribution of crossovers are genetically distinct traits in males and females, and that there is a potential for independent genetic change in both sexes in the Atlantic Salmon. Together, these findings give novel insights into the genetic architecture of recombination in salmonids and contribute to a better understanding of how rates and distribution of recombination may evolve in eukaryotes more broadly.
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spelling pubmed-106654092023-11-22 Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon Brekke, Cathrine Johnston, Susan E. Knutsen, Tim M. Berg, Peer Sci Rep Article Meiotic recombination through chromosomal crossovers ensures proper segregation of homologous chromosomes during meiosis, while also breaking down linkage disequilibrium and shuffling alleles at loci located on the same chromosome. Rates of recombination can vary between species, but also between and within individuals, sex and chromosomes within species. Indeed, the Atlantic salmon genome is known to have clear sex differences in recombination with female biased heterochiasmy and markedly different landscapes of crossovers between males and females. In male meiosis, crossovers occur strictly in the telomeric regions, whereas in female meiosis crossovers tend to occur closer to the centromeres. However, little is known about the genetic control of these patterns and how this differs at the individual level. Here, we investigate genetic variation in individual measures of recombination in > 5000 large full-sib families of a Norwegian Atlantic salmon breeding population with high-density SNP genotypes. We show that females had 1.6 × higher crossover counts (CC) than males, with autosomal linkage maps spanning a total of 2174 cM in females and 1483 cM in males. However, because of the extreme telomeric bias of male crossovers, female recombination is much more important for generation of new haplotypes with 8 × higher intra-chromosomal genetic shuffling than males. CC was heritable in females (h(2) = 0.11) and males (h(2) = 0.10), and shuffling was also heritable in both sex but with a lower heritability in females (h(2) = 0.06) than in males (h(2) = 0.11). Inter-sex genetic correlations for both traits were close to zero, suggesting that rates and distribution of crossovers are genetically distinct traits in males and females, and that there is a potential for independent genetic change in both sexes in the Atlantic Salmon. Together, these findings give novel insights into the genetic architecture of recombination in salmonids and contribute to a better understanding of how rates and distribution of recombination may evolve in eukaryotes more broadly. Nature Publishing Group UK 2023-11-22 /pmc/articles/PMC10665409/ /pubmed/37993527 http://dx.doi.org/10.1038/s41598-023-47208-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Brekke, Cathrine
Johnston, Susan E.
Knutsen, Tim M.
Berg, Peer
Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon
title Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon
title_full Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon
title_fullStr Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon
title_full_unstemmed Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon
title_short Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon
title_sort genetic architecture of individual meiotic crossover rate and distribution in atlantic salmon
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10665409/
https://www.ncbi.nlm.nih.gov/pubmed/37993527
http://dx.doi.org/10.1038/s41598-023-47208-3
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