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Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts

Nature volume 440, pages 341345 (16 March 2006) | Download Citation

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Abstract

A whole-genome duplication occurred in a shared ancestor of the yeast species Saccharomyces cerevisiae, Saccharomyces castellii and Candida glabrata. Here we trace the subsequent losses of duplicated genes, and show that the pattern of loss differs among the three species at 20% of all loci. For example, several transcription factor genes, including STE12, TEC1, TUP1 and MCM1, are single-copy in S. cerevisiae but are retained in duplicate in S. castellii and C. glabrata. At many loci, different species have lost different members of a duplicated gene pair, so that 4–7% of single-copy genes compared between any two species are not orthologues. This pattern of gene loss provides strong evidence for speciation through a version of the Bateson–Dobzhansky–Muller mechanism, in which the loss of alternative copies of duplicated genes leads to reproductive isolation1,2. We show that the lineages leading to the three species diverged shortly after the whole-genome duplication, during a period of precipitous gene loss. The set of loci at which single-copy paralogues are retained is biased towards genes involved in ribosome biogenesis and genes that evolve slowly, consistent with the hypothesis that reciprocal gene loss is more likely to occur between duplicated genes that are functionally indistinguishable. We propose a simple, unified model in which a single mechanism—passive gene loss—enabled whole-genome duplication and led to the rapid emergence of new yeast species.

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Acknowledgements

We are grateful to D. Bradley, G. Conant, J. Conery, B. Cusack, H. Fraser, N. Khaldi, W.-H. Li, A. Lloyd, A. McLysaght, G. Singer, R. Vilgalys and M. Woolfit for discussion. This study was supported by Science Foundation Ireland. Author Contributions S.W. and K.H.W. did pilot studies. K.P.B. developed the YGOB and the scoring scheme. D.R.S. did all analyses except those of gene function (K.P.B.) and chromosomal rearrangements (J.L.G.). Manual editing of data in YGOB was done equally by all authors. D.R.S. and K.H.W. wrote the manuscript.

Author information

Author notes

    • Devin R. Scannell
    •  & Kevin P. Byrne

    *These authors contributed equally to this work

Affiliations

  1. Smurfit Institute of Genetics, University of Dublin, Trinity College, Dublin 2, Ireland

    • Devin R. Scannell
    • , Kevin P. Byrne
    • , Jonathan L. Gordon
    • , Simon Wong
    •  & Kenneth H. Wolfe

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Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding author

Correspondence to Kenneth H. Wolfe.

Supplementary information

Excel files

  1. 1.

    Supplementary Table 1

    Biased representation of Gene Ontology (GO) terms in gene loss classes.

PDF files

  1. 1.

    Supplementary Note 2

    Phylogenetic relationship among S. castellii, S. cerevisiae and C. glabrata.

  2. 2.

    Supplementary Note 3

    Estimation of relative timing of speciation events.

  3. 3.

    Supplementary Note 4

    Model-based estimation of the number of genes still duplicated at phylogenetic nodes.

  4. 4.

    Supplementary Note 5

    Overrepresentation of slowly evolving genes and genes involved in highly conserved biological processes among genes that underwent RGL.

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DOI

https://doi.org/10.1038/nature04562

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