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Speciation driven by hybridization and chromosomal plasticity in a wild yeast

Nature Microbiology volume 1, Article number: 15003 (2016) Cite this article

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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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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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Author notes

  1. Jean-Baptiste Leducq

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

  2. Jean-Baptiste Leducq, Lou Nielly-Thibault and Guillaume Charron: These authors contributed equally to this work.

Authors and 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, G1V 0A6, Quebec, Canada

    Jean-Baptiste Leducq, Lou Nielly-Thibault, Guillaume Charron, Chris Eberlein, Jukka-Pekka Verta & Christian R. Landry

  2. Department of Biology, McGill University, Montreal, H3A 1B1, Quebec, 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, 53706, Wisconsin, 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.

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

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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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