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 mostly 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.
Keywords: Saccharomyces paradoxus; evolutionary biology; experimental evolution; fungi; genetics; genomics; hybridization; transposable elements.
Hybrids arise when two populations of organisms that are related but genetically different mate and produce offspring. Hybridization has long been regarded as one of the many ways species evolve. Studying the changes in the genome that result from this process can provide insights into evolutionary history and predict the outcome of mixing between genetically different populations. In fact, the inability of two organisms to mate and produce viable and fertile hybrids has been used as a way to define species. It has been speculated that the infertility of many hybrids is due to short sequences of DNA in the genome called transposable elements. These elements are sequences of DNA that, when active, can move to a different position in the genome, causing mutations. It is thought that the process of hybridization may be activating transposable elements leading to the infertility often observed in hybrids. The activation of transposable elements in hybrids has been studied in animals and plants, and usually, the hybrids studied were either generated in the laboratory or found in the wild. Fungal species, such as the yeast Saccharomyces paradoxus, have hundreds of wild strains, including many hybrids, and can also be crossed in the laboratory to produce new hybrids, allowing a combined approach to studying the activation of transposable elements. Hénault et al. used this yeast to investigate whether hybridization leads to increased activity of transposable elements in fungi. To test this hypothesis, Hénault et al. analyzed the genomes of hundreds of natural strains of S. paradoxus to count and locate their transposable elements and establish evolutionary relationships between them. Next, they crossed different strains in the laboratory to see how the transposable elements would act upon hybridization. If transposable elements were activated by hybridization, then hybrids would accumulate more transposable elements. However, the analyses did not show increased numbers of transposable elements in wild hybrids of S. paradoxus. This could be explained by an actual absence of transposable element activation, or by natural selection eliminating individuals that accumulate more transposable elements. To determine which is the case, Hénault et al. next recreated several hybrids in the laboratory and reproduced them for hundreds of generations. Hybrids were grown in the laboratory such that natural selection was almost incapable of favoring some yeasts over others, allowing the hybrids to accumulate transposable elements. These experiments revealed that hybrids accumulated transposable elements at different and largely unpredictable rates. Indeed, closely related hybrids often had highly different numbers of transposable elements in their genomes after being reproduced in the laboratory. These observations indicate that the accumulation of transposable elements depends on various factors and cannot be easily predicted, and that hybridization may only be a small piece of the puzzle. Additionally, Hénault et al. demonstrated that undomesticated organisms like fungi can provide unique insights into evolutionary hypotheses.
© 2020, Hénault et al.