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.

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.

Metrics

  • 1,580
    views
  • 219
    downloads
  • 11
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.47091

Further reading

    1. Computational and Systems Biology
    2. Ecology
    Lenore Pipes, Rasmus Nielsen
    Tools and Resources

    Environmental DNA (eDNA) is becoming an increasingly important tool in diverse scientific fields from ecological biomonitoring to wastewater surveillance of viruses. The fundamental challenge in eDNA analyses has been the bioinformatical assignment of reads to taxonomic groups. It has long been known that full probabilistic methods for phylogenetic assignment are preferable, but unfortunately, such methods are computationally intensive and are typically inapplicable to modern Next-Generation Sequencing data. We here present a fast approximate likelihood method for phylogenetic assignment of DNA sequences. Applying the new method to several mock communities and simulated datasets, we show that it identifies more reads at both high and low taxonomic levels more accurately than other leading methods. The advantage of the method is particularly apparent in the presence of polymorphisms and/or sequencing errors and when the true species is not represented in the reference database.

    1. Ecology
    Hao Wang, Kai He ... Chaolun Li
    Research Article

    Bathymodioline mussels dominate deep-sea methane seep and hydrothermal vent habitats and obtain nutrients and energy primarily through chemosynthetic endosymbiotic bacteria in the bacteriocytes of their gill. However, the molecular mechanisms that orchestrate mussel host–symbiont interactions remain unclear. Here, we constructed a comprehensive cell atlas of the gill in the mussel Gigantidas platifrons from the South China Sea methane seeps (1100 m depth) using single-nucleus RNA-sequencing (snRNA-seq) and whole-mount in situ hybridisation. We identified 13 types of cells, including three previously unknown ones, and uncovered unknown tissue heterogeneity. Every cell type has a designated function in supporting the gill’s structure and function, creating an optimal environment for chemosynthesis, and effectively acquiring nutrients from the endosymbiotic bacteria. Analysis of snRNA-seq of in situ transplanted mussels clearly showed the shifts in cell state in response to environmental oscillations. Our findings provide insight into the principles of host–symbiont interaction and the bivalves' environmental adaption mechanisms.