Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation

  1. Anna-Liisa Laine  Is a corresponding author
  2. Benoit Barrès
  3. Elina Numminen
  4. Jukka P Siren
  1. University of Zürich, Switzerland
  2. Université de Lyon, France
  3. University of Helsinki, Finland
  4. Aalto University, Finland

Abstract

Many pathogens possess the capacity for sex through outcrossing, despite being able to reproduce also asexually and/or via selfing. Given that sex is assumed to come at a cost, these mixed reproductive strategies typical of pathogens have remained puzzling. While the ecological and evolutionary benefits of outcrossing are theoretically well-supported, support for such benefits in pathogen populations are still scarce. Here, we analyze the epidemiology and genetic structure of natural populations of an obligate fungal pathogen, Podosphaera plantaginis. We find that the opportunities for outcrossing vary spatially. Populations supporting high levels of coinfection -a prerequisite of sex - result in hotspots of novel genetic diversity. Pathogen populations supporting coinfection also have a higher probability of surviving winter. Jointly our results show that outcrossing has direct epidemiological consequences as well as a major impact on pathogen population genetic diversity, thereby providing evidence of ecological and evolutionary benefits of outcrossing in pathogens.

Data availability

All data and scripts used to perform the analyses presented in this paper are available in the git repository at https://github.com/ComputerBlue/FungalSex.git.

The following data sets were generated

Article and author information

Author details

  1. Anna-Liisa Laine

    Department of Evolutionary Biology and Environmental Studies, University of Zürich, Zürich, Switzerland
    For correspondence
    anna-liisa.laine@ieu.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0703-5850
  2. Benoit Barrès

    Anses, INRA, USC CASPER, Université de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6777-0275
  3. Elina Numminen

    Organismal and Evolutionary Biology, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  4. Jukka P Siren

    Department of Computer Science, Aalto University, Espoo, Finland
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Research Council (281517)

  • Anna-Liisa Laine

European Research Council (724508)

  • Anna-Liisa Laine

Academy of Finland (296686)

  • Anna-Liisa Laine

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

Reviewing Editor

  1. Kayla King, University of Oxford, United Kingdom

Publication history

  1. Received: March 22, 2019
  2. Accepted: June 18, 2019
  3. Accepted Manuscript published: June 18, 2019 (version 1)
  4. Version of Record published: July 30, 2019 (version 2)

Copyright

© 2019, Laine 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. Anna-Liisa Laine
  2. Benoit Barrès
  3. Elina Numminen
  4. Jukka P Siren
(2019)
Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation
eLife 8:e47091.
https://doi.org/10.7554/eLife.47091
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