Speciation driven by hybridization and chromosomal plasticity in a wild yeast

Abstract

Hybridization is recognized as a powerful mechanism of speciation and a driving force in generating biodiversity. However, only few multicellular species, limited to a handful of plants and animals, have been shown to fulfill all the criteria of homoploid hybrid speciation. This lack of evidence could lead to the misconception that speciation by hybridization has a limited role in eukaryotes, particularly in single-celled organisms. Laboratory experiments have revealed that fungi such as budding yeasts can rapidly develop reproductive isolation and novel phenotypes through hybridization, showing that in principle homoploid speciation could occur in nature. Here we report a case of homoploid hybrid speciation in natural populations of the budding yeast Saccharomyces paradoxus inhabiting the North American forests. We show that the rapid evolution of chromosome architecture and an ecological context that led to secondary contact between nascent species drove the formation of an incipient hybrid species with a potentially unique ecological niche.

Heterothallism and potential hybridization events inferred for twenty-two yellow morel species

“…Hybridization is now widely recognized to be an important evolutionary process which might play a crucial role in speciation (Gross and Rieseberg 2005;Mallet 2007;Schumer et al 2014;Taylor and Larson 2019). Hybridization followed by reproductive isolation has been reported to contribute to rapid speciation of yeast (Leducq et al 2016) and the same has been supposed to occur in some filamentous fungi (Kohn 2005;Gladieux et al 2014;Sillo et al 2019). Du et al (2012) reported the 85.2% of the species in the Esculenta Clade (including almost 90% of the Chinese species lineages) diversified and went through rapid speciation in East Asia since the middle Miocene, which might have contributed to the potential hybridization and gene transfer events detected in the Esculenta Clade.…”

The natural diversity and ecology of fission yeast

“…In contrast there is an extensive literature describing diversity and quantitative genetics in the budding yeast Saccharomyces cerevisiae and its wild relative Saccharomyces paradoxus, and a range of related species (Peter & Schacherer, ). These include QTL studies (Bloom, Ehrenreich, Loo, Lite & Kruglyak, ; Fay, ; Liti & Louis, ; Märtens, Hallin, Warringer, Liti, & Parts, ; Swinnen, Thevelein, & Nevoigt, ), genome‐scale analysis of diversity (Liti, Carter, Moses, et al, ; Schacherer, Shapiro, Ruderfer, & Kruglyak, ) and analysis of diversity and evolution in the natural environment (Leducq et al, ; Robinson, Pinharanda, & Bensasson, ). In this review, I survey fission yeast diversity research, and I discuss what little is known about the origins and natural ecology of this species.…”

First genome‐wide analysis of the endangered, endemic lichen Cetradonia linearis reveals isolation by distance and strong population structure

“…Population genomic studies have already added substantial depth and breadth to the knowledge of basic fungal biology, allowing researchers to address questions that were once intractable about the life history and evolution of reproductive systems. For example, fungi that have only been observed reproducing asexually show genomic evidence for sexual reproduction (Tsai et al., ; Stefanini et al., ); speciation through homoploid hybridization has been shown to occur rapidly, at least in yeast (Leducq et al., ); and Glomerales, arbuscular mycorrhizal fungi, have highly flexible levels of ploidy in the heterokaryotic cells within species (Wyss et al., ). Applying these methods to lichenized fungi holds great promise to rapidly advance knowledge of lichen population biology.…”