The effect of hybridization on transposable element accumulation in an undomesticated fungal species

Abstract

Transposable elements (TEs) are mobile genetic elements that can profoundly impact the evolution of genomes and species. A long-standing hypothesis suggests that hybridization could deregulate TEs and trigger their accumulation, although it received mixed support from studies in plants and animals. Here, we tested this hypothesis in fungi using incipient species of the undomesticated yeast Saccharomyces paradoxus. Population genomic data revealed no signature of higher transposition in natural hybrids. As we could not rule out the elimination of past transposition increase signatures by natural selection, we performed a laboratory evolution experiment on a panel of artificial hybrids to measure TE accumulation in the near absence of selection. Changes in TE copy numbers were not predicted by the level of evolutionary divergence between the parents of a hybrid genotype. Rather, they were highly dependent on the individual hybrid genotypes, showing that strong genotype-specific deterministic factors govern TE accumulation in yeast hybrids.

Data availability

Illumina short read sequencing data of the MA lines is available at NCBI under accession PRJNA515073. Genome assemblies and Nanopore long read sequencing data of wild isloates are available at NCBI under accession PRJNA514804. Illumina short read sequencing data of wild isolates is available at NCBI under accessions PRJNA277692, PRJNA324830 and PRJNA479851.

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

Article and author information

Author details

  1. Mathieu Hénault

    Département de biochimie, microbiologie et bio-informatique, Département de biologie, PROTEO, BDRC_UL, Université Laval, Québec, Canada
    For correspondence
    mathieu.henault.1@ulaval.ca
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0760-7545
  2. Souhir Marsit

    Département de biochimie, microbiologie et bio-informatique, PROTEO, BDRC_UL, Université Laval, Québec, Canada
    Competing interests
    No competing interests declared.
  3. Guillaume Charron

    Département de biologie, PROTEO, BDRC_UL, Université Laval, Québec, Canada
    Competing interests
    No competing interests declared.
  4. Christian R Landry

    Département de biologie, Université Laval, Québec, Canada
    Competing interests
    Christian R Landry, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3028-6866

Funding

Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-03755)

  • Christian R Landry

Natural Sciences and Engineering Research Council of Canada (NSERC Alexander Graham-Bell doctoral scholarship)

  • Mathieu Hénault
  • Guillaume Charron

Fonds de recherche du Québec – Nature et technologies (FRQNT doctoral scholarship)

  • Mathieu Hénault
  • Guillaume Charron

Fonds de Recherche du Québec - Santé (FRQS postdoctoral scholarship)

  • Souhir Marsit

Canada Research Chairs (Canada Research Chair in Evolutionary Cell and Systems Biology)

  • Christian R Landry

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

Copyright

© 2020, Hénault 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

  • 2,569
    views
  • 272
    downloads
  • 36
    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. Mathieu Hénault
  2. Souhir Marsit
  3. Guillaume Charron
  4. Christian R Landry
(2020)
The effect of hybridization on transposable element accumulation in an undomesticated fungal species
eLife 9:e60474.
https://doi.org/10.7554/eLife.60474

Share this article

https://doi.org/10.7554/eLife.60474

Further reading

    1. Evolutionary Biology
    Nagatoshi Machii, Ryo Hatashima ... Masato Nikaido
    Research Article

    Cichlid fishes inhabiting the East African Great Lakes, Victoria, Malawi, and Tanganyika, are textbook examples of parallel evolution, as they have acquired similar traits independently in each of the three lakes during the process of adaptive radiation. In particular, ‘hypertrophied lip’ has been highlighted as a prominent example of parallel evolution. However, the underlying molecular mechanisms remain poorly understood. In this study, we conducted an integrated comparative analysis between the hypertrophied and normal lips of cichlids across three lakes based on histology, proteomics, and transcriptomics. Histological and proteomic analyses revealed that the hypertrophied lips were characterized by enlargement of the proteoglycan-rich layer, in which versican and periostin proteins were abundant. Transcriptome analysis revealed that the expression of extracellular matrix-related genes, including collagens, glycoproteins, and proteoglycans, was higher in hypertrophied lips, regardless of their phylogenetic relationships. In addition, the genes in Wnt signaling pathway, which is involved in promoting proteoglycan expression, was highly expressed in both the juvenile and adult stages of hypertrophied lips. Our comprehensive analyses showed that hypertrophied lips of the three different phylogenetic origins can be explained by similar proteomic and transcriptomic profiles, which may provide important clues into the molecular mechanisms underlying phenotypic parallelisms in East African cichlids.

    1. Evolutionary Biology
    Mauna R Dasari, Kimberly E Roche ... Elizabeth A Archie
    Research Article

    Mammalian gut microbiomes are highly dynamic communities that shape and are shaped by host aging, including age-related changes to host immunity, metabolism, and behavior. As such, gut microbial composition may provide valuable information on host biological age. Here, we test this idea by creating a microbiome-based age predictor using 13,563 gut microbial profiles from 479 wild baboons collected over 14 years. The resulting ‘microbiome clock’ predicts host chronological age. Deviations from the clock’s predictions are linked to some demographic and socio-environmental factors that predict baboon health and survival: animals who appear old-for-age tend to be male, sampled in the dry season (for females), and have high social status (both sexes). However, an individual’s ‘microbiome age’ does not predict the attainment of developmental milestones or lifespan. Hence, in our host population, gut microbiome age largely reflects current, as opposed to past, social and environmental conditions, and does not predict the pace of host development or host mortality risk. We add to a growing understanding of how age is reflected in different host phenotypes and what forces modify biological age in primates.