Diverse mating phenotypes impact the spread of wtf meiotic drivers in Schizosaccharomyces pombe

  1. José Fabricio López Hernández
  2. Rachel M Helston
  3. Jeffrey J Lange
  4. R Blake Billmyre
  5. Samantha H Schaffner
  6. Michael T Eickbush
  7. Scott McCroskey
  8. Sarah E Zanders  Is a corresponding author
  1. Stowers Institute for Medical Research, United States
  2. Kenyon College, United States

Abstract

Meiotic drivers are genetic elements that break Mendel's law of segregation to be transmitted into more than half of the offspring produced by a heterozygote. The success of a driver relies on outcrossing (mating between individuals from distinct lineages) because drivers gain their advantage in heterozygotes. It is, therefore, curious that Schizosaccharomyces pombe, a species reported to rarely outcross, harbors many meiotic drivers. To address this paradox, we measured mating phenotypes in S. pombe natural isolates. We found that the propensity for cells from distinct clonal lineages to mate varies between natural isolates and can be affected both by cell density and by the available sexual partners. Additionally, we found that the observed levels of preferential mating between cells from the same clonal lineage can slow, but not prevent, the spread of a wtf meiotic driver in the absence of additional fitness costs linked to the driver. These analyses reveal parameters critical to understanding the evolution of S. pombe and help explain the success of meiotic drivers in this species.

Data availability

Original data underlying this manuscript can be accessed from the Stowers Original Data Repository at http://www.stowers.org/research/publications/libpbxxxx.Base called reads are available as fastq files at the SRA under project accession number PRJNA732453.

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

Article and author information

Author details

  1. José Fabricio López Hernández

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
  2. Rachel M Helston

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
  3. Jeffrey J Lange

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
  4. R Blake Billmyre

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4866-3711
  5. Samantha H Schaffner

    Kenyon College, Gambier, United States
    Competing interests
    No competing interests declared.
  6. Michael T Eickbush

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9057-9156
  7. Scott McCroskey

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
  8. Sarah E Zanders

    Stowers Institute for Medical Research, Kansas City, United States
    For correspondence
    sez@stowers.org
    Competing interests
    Sarah E Zanders, Inventor on patent application 834 serial 62/491,107 based on wtf killers..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1867-986X

Funding

Stowers Institute for Medical Research (NA)

  • Sarah E Zanders

National Institute of General Medical Sciences (DP2GM132936)

  • Sarah E Zanders

Searle Scholars Program (NA)

  • Sarah E Zanders

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

Reviewing Editor

  1. Tatiana Giraud, Université Paris-Sud, France

Publication history

  1. Preprint posted: May 29, 2021 (view preprint)
  2. Received: May 29, 2021
  3. Accepted: December 10, 2021
  4. Accepted Manuscript published: December 13, 2021 (version 1)
  5. Version of Record published: January 25, 2022 (version 2)

Copyright

© 2021, López Hernández 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

  • 1,408
    Page views
  • 168
    Downloads
  • 5
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

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. José Fabricio López Hernández
  2. Rachel M Helston
  3. Jeffrey J Lange
  4. R Blake Billmyre
  5. Samantha H Schaffner
  6. Michael T Eickbush
  7. Scott McCroskey
  8. Sarah E Zanders
(2021)
Diverse mating phenotypes impact the spread of wtf meiotic drivers in Schizosaccharomyces pombe
eLife 10:e70812.
https://doi.org/10.7554/eLife.70812

Further reading

    1. Developmental Biology
    2. Evolutionary Biology
    Joaquín Letelier, Lorena Buono ... Juan R Martínez-Morales
    Research Article

    Genetic studies in human and mice have established a dual role for Vsx genes in retina development: an early function in progenitors’ specification, and a later requirement for bipolar-cells fate determination. Despite their conserved expression patterns, it is currently unclear to which extent Vsx functions are also conserved across vertebrates, as mutant models are available only in mammals. To gain insight into vsx function in teleosts, we have generated vsx1 and vsx2 CRISPR/Cas9 double knockouts (vsxKO) in zebrafish. Our electrophysiological and histological analyses indicate severe visual impairment and bipolar cells depletion in vsxKO larvae, with retinal precursors being rerouted toward photoreceptor or Müller glia fates. Surprisingly, neural retina is properly specified and maintained in mutant embryos, which do not display microphthalmia. We show that although important cis-regulatory remodelling occurs in vsxKO retinas during early specification, this has little impact at a transcriptomic level. Our observations point to genetic redundancy as an important mechanism sustaining the integrity of the retinal specification network, and to Vsx genes regulatory weight varying substantially among vertebrate species.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Yuichiro Hara, Shigehiro Kuraku
    Research Article

    Functionally indispensable genes are likely to be retained and otherwise to be lost during evolution. This evolutionary fate of a gene can also be affected by factors independent of gene dispensability, including the mutability of genomic positions, but such features have not been examined well. To uncover the genomic features associated with gene loss, we investigated the characteristics of genomic regions where genes have been independently lost in multiple lineages. With a comprehensive scan of gene phylogenies of vertebrates with a careful inspection of evolutionary gene losses, we identified 813 human genes whose orthologs were lost in multiple mammalian lineages: designated ‘elusive genes.’ These elusive genes were located in genomic regions with rapid nucleotide substitution, high GC content, and high gene density. A comparison of the orthologous regions of such elusive genes across vertebrates revealed that these features had been established before the radiation of the extant vertebrates approximately 500 million years ago. The association of human elusive genes with transcriptomic and epigenomic characteristics illuminated that the genomic regions containing such genes were subject to repressive transcriptional regulation. Thus, the heterogeneous genomic features driving gene fates toward loss have been in place and may sometimes have relaxed the functional indispensability of such genes. This study sheds light on the complex interplay between gene function and local genomic properties in shaping gene evolution that has persisted since the vertebrate ancestor.