Article

Speciation driven by hybridization and chromosomal plasticity in a wild yeast

  • Nature Microbiology 1, Article number: 15003 (2016)
  • doi:10.1038/nmicrobiol.2015.3
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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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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.

Author information

Author notes

    • Jean-Baptiste Leducq

    Present address: Département des Sciences Biologiques, Pavillon Marie-Victorin, 90 rue Vincent d'Indy, Université de Montréal, Montréal, Quebec H2V 2S9, Canada

    • Jean-Baptiste Leducq
    • , Lou Nielly-Thibault
    •  & Guillaume Charron

    These authors contributed equally to this work.

Affiliations

  1. Département de Biologie, Institut de Biologie Intégrative et des Systèmes, PROTEO, Pavillon Charles-Eugène-Marchand, 1030 avenue de la Médecine, Université Laval, Québec, Quebec G1V 0A6, Canada

    • Jean-Baptiste Leducq
    • , Lou Nielly-Thibault
    • , Guillaume Charron
    • , Chris Eberlein
    • , Jukka-Pekka Verta
    •  & Christian R. Landry
  2. Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada

    • Pedram Samani
    •  & Graham Bell
  3. Laboratory of Genetics, Genome Center of Wisconsin, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA

    • Kayla Sylvester
    •  & Chris Todd Hittinger

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

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

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Tables 2–11, Figures 1–16, Methods, Text and References

Excel files

  1. 1.

    Supplementary Table 1

    List of strains used in this study