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 fulfil all the criteria of homoploid hybrid speciation. This lack of evidence could lead to the interpretation 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.

Hybridization in Plants: Old Ideas, New Techniques

“…A recent review found that 11% of species across 47 plant genera were likely of allopolyploid origin (Barker et al, 2016). Meanwhile, only a handful of examples of homoploid hybrid speciation have been identified in animals (Mavárez et al, 2006;Lukhtanov et al, 2015), fungi (Leducq et al, 2016), and plants (Rieseberg et al, 2003a). In agreement with the paucity of well-supported examples, simulations suggest that hybridization more likely results in stable hybrid zones or the extinction of a parental species than homoploid hybrid speciation (Buerkle et al, 2003).…”

The high turnover of ribosome-associated transcripts fromde novoORFs produces gene-like characteristics available forde novogene emergence in wild yeast populations

“…We used genomes from 24 strains that are structured in three main lineages named SpA, SpB and SpC (Charron et al 2014; Leducq et al 2016). Two S. cerevisiae strains were included as outgroups: the wild isolate YPS128 (Sniegowski et al 2002;Peter et al 2018) and the reference strain S288C.…”

“…Two S. cerevisiae strains were included as outgroups: the wild isolate YPS128 (Sniegowski et al 2002;Peter et al 2018) and the reference strain S288C. These lineages cover different levels of nucleotide divergence, ranging from ~ 13 % between S. cerevisiae and S. paradoxus to ~2.27 % between the two closest SpB and SpC lineages (Kellis et al 2003;Leducq et al 2016). We used microsynteny to identify and align homologous non-genic regions between pairs of conserved annotated genes ( Fig.…”

“…Because polymorphism within lineages (SpA, SpB or SpC) (Leducq et al 2016) may affect the topology of the phylogeny (although most diversity in this group is among lineage divergence) we used only one strain per lineage (YPS128 (S. cerevisiae), YPS744 (SpA), MSH-604 (SpB) and MSH-587-1 (SpC)) to reconstruct ancestral sequences at two divergence nodes that we labeled . CC-BY-NC-ND 4.0 International license It is made available under a (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.…”

“…We investigate intergenic ORF (iORF) diversity in wild Saccharomyces paradoxus populations, which are structured in 3 main lineages named SpA, SpB and SpC (Charron et al 2014;Leducq et al 2016). The wild S. cerevisiae strain YPS128 was used in our experiments and the reference S288C (version R64-2-1) was added in our analysis for the functional annotation.…”