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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.

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Figure 1: A cryptic S. paradoxus lineage revealed by a population structure and a distinct ecological niche from its sympatric close lineages.
Figure 2: The SpC* lineage is an incipient species, as revealed by its reduced reproductive success with its sister lineages.
Figure 3: The SpC* lineage is a mosaic of SpC and SpB genomes and results from past hybridization.
Figure 4: Chromosomal rearrangements and introgressed regions unevenly segregate in the SpC* × SpC hybrid progeny.
Figure 5: Chromosomal rearrangements and introgressed regions contribute to the decreasing viability of SpC*×SpC hybrid progeny.
Figure 6: A biogeographic scenario for the emergence of S. paradoxus lineages in North America.

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Acknowledgements

The authors thank A. K. Dubé, K. Lambert, R. Nuwal, S. Haughian, A.-E. Chrétien, M. Caouette, I. Kukavica-Ibrulj, R. Levesque and the IBIS sequencing platform (B. Boyle) for technical help, P. Sniegowski, M.-A. Lachance and J. Anderson for providing strains, I. Levade and C. Lemieux for discussions and N. Aubin-Horth, A. Moses, L. Bernatchez, J. Shapiro, S. Pavey, F. Rousseau-Brochu, I. Gagnon-Arsenault, A.K. Dubé, A.-M. Dion-Côté, H. Vignaud and M. Nigg for comments on the manuscript. Funding support was provided by a NSERC Discovery Grant and an HFSP grant (RGY0073/2010) to C.R.L., FRQS fellowships to J.-B.L., NSERC USRA summer scholarships to L.N.T., FRQNT and NSERC PhD fellowships to G.C. Some of this material (yeast collection) is based on work supported by the National Science Foundation under grant no. DEB-1253634 (C.T.H.) and by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02–07ER64494). C.T.H. is a Pew Scholar in the Biomedical Sciences, supported by the Pew Charitable Trusts. C.R.L. is a FRQS Junior Investigator and holds the Canada Research Chair in Evolutionary Cell and Systems Biology.

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Contributions

J.B.L., C.R.L., L.N.T. and G.C. planned the experiments. G.C., J.B.L. and C.E. performed experiments. J.B.L., L.N.T. and J.P.V. performed bioinformatic analyses. P.S., K.S., C.T.H. and G.B. provided strains and discussion in the early stages of this study. J.B.L. and C.R.L. drafted the manuscript with contributions from L.N.T., G.C., C.E., P.S. and G.B.

Corresponding authors

Correspondence to Jean-Baptiste Leducq or Christian R. Landry.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Tables 2–11, Figures 1–16, Methods, Text and References (PDF 8991 kb)

Supplementary Table 1

List of strains used in this study (XLSX 48 kb)

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Leducq, JB., Nielly-Thibault, L., Charron, G. et al. Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nat Microbiol 1, 15003 (2016). https://doi.org/10.1038/nmicrobiol.2015.3

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