Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon
Abstract 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 b...
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| Format: | Article |
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Nature Portfolio
2023-11-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-47208-3 |
| _version_ | 1827634306969763840 |
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| author | Cathrine Brekke Susan E. Johnston Tim M. Knutsen Peer Berg |
| author_facet | Cathrine Brekke Susan E. Johnston Tim M. Knutsen Peer Berg |
| author_sort | Cathrine Brekke |
| collection | DOAJ |
| description | Abstract 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 (h2 = 0.11) and males (h2 = 0.10), and shuffling was also heritable in both sex but with a lower heritability in females (h2 = 0.06) than in males (h2 = 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. |
| first_indexed | 2024-03-09T15:12:32Z |
| format | Article |
| id | doaj.art-2e80e12b014a404386fa375bd22ab83a |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-09T15:12:32Z |
| publishDate | 2023-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-2e80e12b014a404386fa375bd22ab83a2023-11-26T13:16:56ZengNature PortfolioScientific Reports2045-23222023-11-0113111210.1038/s41598-023-47208-3Genetic architecture of individual meiotic crossover rate and distribution in Atlantic SalmonCathrine Brekke0Susan E. Johnston1Tim M. Knutsen2Peer Berg3Institute of Ecology and Evolution, School of Biology, University of EdinburghInstitute of Ecology and Evolution, School of Biology, University of EdinburghAquaGen ASDepartment of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life SciencesAbstract 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 (h2 = 0.11) and males (h2 = 0.10), and shuffling was also heritable in both sex but with a lower heritability in females (h2 = 0.06) than in males (h2 = 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.https://doi.org/10.1038/s41598-023-47208-3 |
| spellingShingle | Cathrine Brekke Susan E. Johnston Tim M. Knutsen Peer Berg Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon Scientific Reports |
| 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 |
| url | https://doi.org/10.1038/s41598-023-47208-3 |
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