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Complex fitness landscape shapes variation in a hyperpolymorphic species

It is natural to assume that patterns of genetic variation in hyperpolymorphic species can reveal large-scale properties of the fitness landscape that are hard to detect by studying species with ordinary levels of genetic variation. Here, we study such patterns in a fungus Schizophyllum commune, the...

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Autores principales: Stolyarova, Anastasia V, Neretina, Tatiana V, Zvyagina, Elena A, Fedotova, Anna V, Kondrashov, Alexey S, Bazykin, Georgii A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9187340/
https://www.ncbi.nlm.nih.gov/pubmed/35532122
http://dx.doi.org/10.7554/eLife.76073
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author Stolyarova, Anastasia V
Neretina, Tatiana V
Zvyagina, Elena A
Fedotova, Anna V
Kondrashov, Alexey S
Bazykin, Georgii A
author_facet Stolyarova, Anastasia V
Neretina, Tatiana V
Zvyagina, Elena A
Fedotova, Anna V
Kondrashov, Alexey S
Bazykin, Georgii A
author_sort Stolyarova, Anastasia V
collection PubMed
description It is natural to assume that patterns of genetic variation in hyperpolymorphic species can reveal large-scale properties of the fitness landscape that are hard to detect by studying species with ordinary levels of genetic variation. Here, we study such patterns in a fungus Schizophyllum commune, the most polymorphic species known. Throughout the genome, short-range linkage disequilibrium (LD) caused by attraction of minor alleles is higher between pairs of nonsynonymous than of synonymous variants. This effect is especially pronounced for pairs of sites that are located within the same gene, especially if a large fraction of the gene is covered by haploblocks, genome segments where the gene pool consists of two highly divergent haplotypes, which is a signature of balancing selection. Haploblocks are usually shorter than 1000 nucleotides, and collectively cover about 10% of the S. commune genome. LD tends to be substantially higher for pairs of nonsynonymous variants encoding amino acids that interact within the protein. There is a substantial correlation between LDs at the same pairs of nonsynonymous mutations in the USA and the Russian populations. These patterns indicate that selection in S. commune involves positive epistasis due to compensatory interactions between nonsynonymous alleles. When less polymorphic species are studied, analogous patterns can be detected only through interspecific comparisons.
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spelling pubmed-91873402022-06-11 Complex fitness landscape shapes variation in a hyperpolymorphic species Stolyarova, Anastasia V Neretina, Tatiana V Zvyagina, Elena A Fedotova, Anna V Kondrashov, Alexey S Bazykin, Georgii A eLife Evolutionary Biology It is natural to assume that patterns of genetic variation in hyperpolymorphic species can reveal large-scale properties of the fitness landscape that are hard to detect by studying species with ordinary levels of genetic variation. Here, we study such patterns in a fungus Schizophyllum commune, the most polymorphic species known. Throughout the genome, short-range linkage disequilibrium (LD) caused by attraction of minor alleles is higher between pairs of nonsynonymous than of synonymous variants. This effect is especially pronounced for pairs of sites that are located within the same gene, especially if a large fraction of the gene is covered by haploblocks, genome segments where the gene pool consists of two highly divergent haplotypes, which is a signature of balancing selection. Haploblocks are usually shorter than 1000 nucleotides, and collectively cover about 10% of the S. commune genome. LD tends to be substantially higher for pairs of nonsynonymous variants encoding amino acids that interact within the protein. There is a substantial correlation between LDs at the same pairs of nonsynonymous mutations in the USA and the Russian populations. These patterns indicate that selection in S. commune involves positive epistasis due to compensatory interactions between nonsynonymous alleles. When less polymorphic species are studied, analogous patterns can be detected only through interspecific comparisons. eLife Sciences Publications, Ltd 2022-05-09 /pmc/articles/PMC9187340/ /pubmed/35532122 http://dx.doi.org/10.7554/eLife.76073 Text en © 2022, Stolyarova et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Stolyarova, Anastasia V
Neretina, Tatiana V
Zvyagina, Elena A
Fedotova, Anna V
Kondrashov, Alexey S
Bazykin, Georgii A
Complex fitness landscape shapes variation in a hyperpolymorphic species
title Complex fitness landscape shapes variation in a hyperpolymorphic species
title_full Complex fitness landscape shapes variation in a hyperpolymorphic species
title_fullStr Complex fitness landscape shapes variation in a hyperpolymorphic species
title_full_unstemmed Complex fitness landscape shapes variation in a hyperpolymorphic species
title_short Complex fitness landscape shapes variation in a hyperpolymorphic species
title_sort complex fitness landscape shapes variation in a hyperpolymorphic species
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9187340/
https://www.ncbi.nlm.nih.gov/pubmed/35532122
http://dx.doi.org/10.7554/eLife.76073
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