Abstract

Hybridization can result in reproductively isolated and phenotypically distinct lineages that evolve as independent hybrid species. How frequently hybridization leads to speciation remains largely unknown. Here we examine the potential recurrence of hybrid speciation in the wild yeast Saccharomyces paradoxus in North America, which comprises two endemic lineages SpB and SpC, and an incipient hybrid species, SpC*. Using whole-genome sequences from more than 300 strains, we uncover the hybrid origin of another group, SpD, that emerged from hybridization between SpC* and one of its parental species, the widespread SpB. We show that SpD has the potential to evolve as a novel hybrid species, because it displays phenotypic novelties that include an intermediate transcriptome profile, and partial reproductive isolation with its most abundant sympatric parental species, SpB. Our findings show that repetitive cycles of divergence and hybridization quickly generate diversity and reproductive isolation, providing the raw material for speciation by hybridization.

Highlights

  • Hybridization among species is considered as a stimulating force in evolution[1], but its consequences are difficult to predict

  • We examined whether the origin of SpD can be traced back to a hybridization event between the previously described endemic S. paradoxus species

  • In agreement with previous phylogenetic analyses[16,17], we found that the strains form five clusters corresponding to SpA, SpB, SpC, SpC*, and SpD (Fig. 1b, c, Supplementary Figure 2)

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Summary

Introduction

Hybridization among species is considered as a stimulating force in evolution[1], but its consequences are difficult to predict. A recent population genomics study of Saccharomyces paradoxus, a budding yeast found worldwide on the bark of deciduous trees and their associated soils[13,14], showed that a novel North American species evolved through hybridization about 10,000 years ago[15]. Genome sequencing and systematic phenotyping, we find that SpD strains are recent hybrids between the hybrid species SpC* and the most abundant North American lineage, SpB This backcross between a hybrid and one of its parental species generated novel growth phenotypes, intermediate transcriptional profiles, a novel genome architecture and partial reproductive isolation. These results highlight that speciation in yeast may result from repeated cycles of divergence and hybridization

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