The effect of hybridization on transposable element accumulation in an undomesticated fungal species
- Université Laval, Canada
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.
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Ploidy instability in experimental hybrid populationsNCBI BioProject, PRJNA515073.
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Saccharomyces paradoxus Raw sequence readsNCBI BioProject, PRJNA324830.
Article and author information
Author details
Christian R Landry
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.
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The effect of hybridization on transposable element accumulation in an undomesticated fungal species
eLife 9:e60474.
https://doi.org/10.7554/eLife.60474
Further reading
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- Evolutionary Biology
The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than 10 alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognised.
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- Computational and Systems Biology
- Evolutionary Biology
As pathogens spread in a population of hosts, immunity is built up, and the pool of susceptible individuals are depleted. This generates selective pressure, to which many human RNA viruses, such as influenza virus or SARS-CoV-2, respond with rapid antigenic evolution and frequent emergence of immune evasive variants. However, the host’s immune systems adapt, and older immune responses wane, such that escape variants only enjoy a growth advantage for a limited time. If variant growth dynamics and reshaping of host-immunity operate on comparable time scales, viral adaptation is determined by eco-evolutionary interactions that are not captured by models of rapid evolution in a fixed environment. Here, we use a Susceptible/Infected model to describe the interaction between an evolving viral population in a dynamic but immunologically diverse host population. We show that depending on strain cross-immunity, heterogeneity of the host population, and durability of immune responses, escape variants initially grow exponentially, but lose their growth advantage before reaching high frequencies. Their subsequent dynamics follows an anomalous random walk determined by future escape variants and results in variant trajectories that are unpredictable. This model can explain the apparent contradiction between the clearly adaptive nature of antigenic evolution and the quasi-neutral dynamics of high-frequency variants observed for influenza viruses.
