Modelling the consequences of the dikaryotic life cycle of mushroom-forming fungi on genomic conflict

  1. Benjamin Auxier
  2. Tamás L Czárán
  3. Duur K Aanen  Is a corresponding author
  1. Wageningen University, Netherlands
  2. Eötvös Loránd University, Hungary

Abstract

Generally, sexual organisms contain two haploid genomes, one from each parent, united in a single diploid nucleus of the zygote which links their fate during growth. A fascinating exception to this are Basidiomycete fungi, where the two haploid genomes remain separate in a dikaryon, retaining the option to fertilize subsequent monokaryons encountered. How the ensuing nuclear competition influences the balance of selection within and between individuals is largely unexplored. We test the consequences of the dikaryotic lifecycle for mating success and mycelium-level fitness components. We assume a trade-off between mating fitness at the level of the haploid nucleus and fitness of the fungal mycelium. We show that the maintenance of fertilization potential by dikaryons leads to a higher proportion of fertilized monokaryons, but that the ensuing intra-dikaryon selection for increased nuclear mating fitness leads to reduced mycelium fitness relative to a diploid life cycle. However, this fitness reduction is lower compared to a hypothetical life cycle where dikaryons can also exchange nuclei. Prohibition of fusion between dikaryons therefore reduces the level of nuclear parasitism. The number of loci influencing fitness is an important determinant of the degree to which average mycelium-level fitness is reduced. The results of this study crucially hinge upon a trade-off between nucleus and mycelium-level fitness. We discuss the evidence for this assumption and the implications of an alternative that there is a positive relationship between nucleus and mycelium-level fitness.

Data availability

The current manuscript is a computational study, so no data have been generated. Simulation code for performing simulations as well as scripts to produce figures and analyses are available in Github repository https://github.com/BenAuxier/Basid.Sex.Sim

Article and author information

Author details

  1. Benjamin Auxier

    Laboratory of Genetics, Wageningen University, Wageningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7743-0610
  2. Tamás L Czárán

    Eötvös Loránd University, Budapest, Hungary
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2722-6208
  3. Duur K Aanen

    Laboratory of Genetics, Wageningen University, Wageningen, Netherlands
    For correspondence
    duur.aanen@wur.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5702-1617

Funding

National Research Development and Innovation Office (K124438)

  • Tamás L Czárán

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (ALGR.2017.010)

  • Benjamin Auxier

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO86514007)

  • Duur K Aanen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Publication history

  1. Preprint posted: May 30, 2020 (view preprint)
  2. Received: November 30, 2021
  3. Accepted: April 14, 2022
  4. Accepted Manuscript published: April 20, 2022 (version 1)
  5. Version of Record published: May 9, 2022 (version 2)

Copyright

© 2022, Auxier 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. Benjamin Auxier
  2. Tamás L Czárán
  3. Duur K Aanen
(2022)
Modelling the consequences of the dikaryotic life cycle of mushroom-forming fungi on genomic conflict
eLife 11:e75917.
https://doi.org/10.7554/eLife.75917

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