Complex fitness landscape shapes variation in a hyperpolymorphic species

  1. Anastasia V Stolyarova  Is a corresponding author
  2. Tatiana V Neretina
  3. Elena A Zvyagina
  4. Anna V Fedotova
  5. Alexey Kondrashov
  6. Georgii A. Bazykin  Is a corresponding author
  1. Skolkovo Institute of Science and Technology, Russian Federation
  2. Lomonosov Moscow State University, Russian Federation
  3. University of Michigan-Ann Arbor, United States
  4. Russian Academy of Sciences, Russian Federation

Abstract

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.

Data availability

Whole-genome alignment of 55 genomes of S. commune is available at https://makarich.fbb.msu.ru/astolyarova/schizophyllum_data/. Genome sequence data are deposited at DDBJ/ENA/GenBank under accession numbers JAGVRL000000000-JAGVSI000000000, BioProject PRJNA720428. Sequencing data are deposited at SRA with accession numbers SRR14467839-SRR14467862.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Anastasia V Stolyarova

    Skolkovo Institute of Science and Technology, Moscow, Russian Federation
    For correspondence
    anastasia.v.stolyarova@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6546-3052
  2. Tatiana V Neretina

    Biological Faculty, Lomonosov Moscow State University, Moscow, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  3. Elena A Zvyagina

    Biological Faculty, Lomonosov Moscow State University, Moscow, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  4. Anna V Fedotova

    Skolkovo Institute of Science and Technology, Moscow, Russian Federation
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexey Kondrashov

    Department of Ecology and Evolutionary Biology, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Georgii A. Bazykin

    Institute for Information Transmission Problems (Kharkevich Institute), Russian Academy of Sciences, Moscow, Russian Federation
    For correspondence
    gbazykin@iitp.ru
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2334-2751

Funding

No external funding was received for this work.

Reviewing Editor

  1. Emilia Huerta-Sanchez, Brown University, United States

Version history

  1. Preprint posted: October 10, 2021 (view preprint)
  2. Received: December 3, 2021
  3. Accepted: May 9, 2022
  4. Accepted Manuscript published: May 9, 2022 (version 1)
  5. Version of Record published: June 10, 2022 (version 2)

Copyright

© 2022, Stolyarova et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Anastasia V Stolyarova
  2. Tatiana V Neretina
  3. Elena A Zvyagina
  4. Anna V Fedotova
  5. Alexey Kondrashov
  6. Georgii A. Bazykin
(2022)
Complex fitness landscape shapes variation in a hyperpolymorphic species
eLife 11:e76073.
https://doi.org/10.7554/eLife.76073

Share this article

https://doi.org/10.7554/eLife.76073

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