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Evolutionary biology through the lens of budding yeast comparative genomics

Key Points

  • The budding yeast Saccharomyces cerevisiae has become an important model for evolutionary genomics owing to the development of high-throughput sequencing technologies.

  • Comparative genomics analysis of S. cerevisiae and closely related species has contributed to our understanding of how new species emerge and has shed light on the various mechanisms that contribute to reproductive isolation.

  • Population genomics and comparative genomics of Saccharomyces yeasts have revealed that hybridization occurred frequently throughout, and has had substantial effects on, yeast evolution. Hybridization could itself be a mechanism of adaptation and speciation.

  • Genomic analysis of Saccharomyces yeasts has provided a better understanding of the mechanisms underlying large-scale genomic changes, such as polyploidy, and their consequences for genome evolution and cell physiology.

  • Genomic analysis of yeast strains associated with humans has revealed the history of yeast domestication and the mechanisms that have contributed to its adaptation to anthropogenic environments.

  • Genomic approaches are increasingly contributing to our understanding of how budding yeasts adapt to natural environments by identifying the genes that are involved in adaptation within natural substrates.


The budding yeast Saccharomyces cerevisiae is a highly advanced model system for studying genetics, cell biology and systems biology. Over the past decade, the application of high-throughput sequencing technologies to this species has contributed to this yeast also becoming an important model for evolutionary genomics. Indeed, comparative genomic analyses of laboratory, wild and domesticated yeast populations are providing unprecedented detail about many of the processes that govern evolution, including long-term processes, such as reproductive isolation and speciation, and short-term processes, such as adaptation to natural and domestication-related environments.

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Figure 1: Mechanisms of postzygotic reproductive isolation in Saccharomyces.
Figure 2: Genomic mechanisms of introgression and loss of heterozygosity (LOH) in Saccharomyces.
Figure 3: Diversification of the galactose utilization network after the budding yeast whole-genome duplication (WGD).
Figure 4: The history of yeast domestication for beer, wine, sake, cocoa and coffee fermentation.
Figure 5: Hallmarks of adaptation in domesticated yeasts.
Figure 6: Functional genomics tools for identifying fitness determinants in natural environments.


  1. 1

    Mortimer, R. K. & Johnston, J. R. Genealogy of principal strains of the yeast genetic stock center. Genetics 113, 35–43 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2

    Haase, S. B. & Wittenberg, C. Topology and control of the cell-cycle-regulated transcriptional circuitry. Genetics 196, 65–90 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Teixeira, M. T. Saccharomyces cerevisiae as a model to study replicative senescence triggered by telomere shortening. Front. Oncol. 3, 101 (2013).

    PubMed  PubMed Central  Google Scholar 

  4. 4

    Reggiori, F. & Klionsky, D. J. Autophagic processes in yeast: mechanism, machinery and regulation. Genetics 194, 341–361 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. 5

    Goffeau, A. et al. Life with 6000 genes. Science 274, 563–567 (1996).

    Google Scholar 

  6. 6

    Kavscek, M., Strazar, M., Curk, T., Natter, K. & Petrovic, U. Yeast as a cell factory: current state and perspectives. Microb. Cell Fact. 14, 94 (2015).

    PubMed  PubMed Central  Google Scholar 

  7. 7

    Richardson, S. M. et al. Design of a synthetic yeast genome. Science 355, 1040–1044 (2017).

    CAS  PubMed  Google Scholar 

  8. 8

    Botstein, D. & Fink, G. R. Yeast: an experimental organism for 21 st century biology. Genetics 189, 695–704 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Duina, A. A., Miller, M. E. & Keeney, J. B. Budding yeast for budding geneticists: a primer on the Saccharomyces cerevisiae model system. Genetics 197, 33–48 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Liu, L., Redden, H. & Alper, H. S. Frontiers of yeast metabolic engineering: diversifying beyond ethanol and Saccharomyces. Curr. Opin. Biotechnol. 24, 1023–1030 (2013).

    CAS  PubMed  Google Scholar 

  11. 11

    Dequin, S. & Casaregola, S. The genomes of fermentative Saccharomyces. C. R. Biol. 334, 687–693 (2011).

    CAS  PubMed  Google Scholar 

  12. 12

    Sicard, D. & Legras, J. L. Bread, beer and wine: yeast domestication in the Saccharomyces sensu stricto complex. C. R. Biol. 334, 229–236 (2011).

    PubMed  Google Scholar 

  13. 13

    Mortimer, R. K. Evolution and variation of the yeast (Saccharomyces) genome. Genome Res. 10, 403–409 (2000).

    CAS  PubMed  Google Scholar 

  14. 14

    Liti, G. et al. Population genomics of domestic and wild yeasts. Nature 458, 337–341 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Stefanini, I. et al. Social wasps are a Saccharomyces mating nest. Proc. Natl Acad. Sci. USA 113, 2247–2251 (2016).

    CAS  PubMed  Google Scholar 

  16. 16

    Boynton, P. J. & Greig, D. The ecology and evolution of non-domesticated Saccharomyces species. Yeast 31, 449–462 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Borneman, A. R. & Pretorius, I. S. Genomic insights into the Saccharomyces sensu stricto complex. Genetics 199, 281–291 (2015).

    PubMed  PubMed Central  Google Scholar 

  18. 18

    Scannell, D. R. et al. The awesome power of yeast evolutionary genetics: new genome sequences and strain resources for the Saccharomyces sensu stricto genus. G3 (Bethesda) 1, 11–25 (2011).

    CAS  Google Scholar 

  19. 19

    Leducq, J. B. et al. Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nat. Microbiol. 1, 15003 (2016). This study provides genomic evidence of incipient speciation by hybridization in natural S. paradoxus populations and shows the role of chromosomal translocations in initiating reproductive barriers.

    CAS  PubMed  Google Scholar 

  20. 20

    Dujon, B. Yeast evolutionary genomics. Nat. Rev. Genet. 11, 512–524 (2010).

    CAS  PubMed  Google Scholar 

  21. 21

    Galeote, V., Bigey, F., Devillers, H., Neuveglise, C. & Dequin, S. Genome sequence of the food spoilage yeast Zygosaccharomyces bailii CLIB 213T. Genome Announc. 1, e00606–13 (2013).

    PubMed  PubMed Central  Google Scholar 

  22. 22

    Genolevures, C. et al. Comparative genomics of protoploid Saccharomycetaceae. Genome Res. 19, 1696–1709 (2009).

    Google Scholar 

  23. 23

    Friedrich, A., Jung, P., Reisser, C., Fischer, G. & Schacherer, J. Population genomics reveals chromosome-scale heterogeneous evolution in a protoploid yeast. Mol. Biol. Evol. 32, 184–192 (2015).

    CAS  PubMed  Google Scholar 

  24. 24

    Gabaldon, T. et al. Comparative genomics of emerging pathogens in the Candida glabrata clade. BMC Genomics 14, 623 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

    Seehausen, O. et al. Genomics and the origin of species. Nat. Rev. Genet. 15, 176–192 (2014).

    CAS  PubMed  Google Scholar 

  26. 26

    Shapiro, B. J., Leducq, J. B. & Mallet, J. What Is speciation? PLoS Genet. 12, e1005860 (2016).

    PubMed  PubMed Central  Google Scholar 

  27. 27

    Maclean, C. J. & Greig, D. Prezygotic reproductive isolation between Saccharomyces cerevisiae and Saccharomyces paradoxus. BMC Evol. Biol. 8, 1 (2008).

    PubMed  PubMed Central  Google Scholar 

  28. 28

    Liti, G., Barton, D. B. & Louis, E. J. Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174, 839–850 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Rayssiguier, C., Thaler, D. S. & Radman, M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342, 396–401 (1989).

    CAS  PubMed  Google Scholar 

  30. 30

    Chambers, S. R., Hunter, N., Louis, E. J. & Borts, R. H. The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss. Mol. Cell. Biol. 16, 6110–6120 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    Greig, D., Travisano, M., Louis, E. J. & Borts, R. H. A role for the mismatch repair system during incipient speciation in Saccharomyces. J. Evol. Biol. 16, 429–437 (2003).

    CAS  PubMed  Google Scholar 

  32. 32

    Cutter, A. D. The polymorphic prelude to Bateson-Dobzhansky-Muller incompatibilities. Trends Ecol. Evol. 27, 209–218 (2012).

    PubMed  Google Scholar 

  33. 33

    Paliwal, S., Fiumera, A. C. & Fiumera, H. L. Mitochondrial-nuclear epistasis contributes to phenotypic variation and coadaptation in natural isolates of Saccharomyces cerevisiae. Genetics 198, 1251–1265 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Hou, J., Friedrich, A., Gounot, J. S. & Schacherer, J. Comprehensive survey of condition-specific reproductive isolation reveals genetic incompatibility in yeast. Nat. Commun. 6, 7214 (2015). This study provides experimental and genomic evidence that BDMIs are widespread within S. cerevisiae and may help to initiate reproductive barriers in fluctuating environments.

    PubMed  PubMed Central  Google Scholar 

  35. 35

    Chou, J. Y., Hung, Y. S., Lin, K. H., Lee, H. Y. & Leu, J. Y. Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol. 8, e1000432 (2010).

    PubMed  PubMed Central  Google Scholar 

  36. 36

    Jhuang, H. Y., Lee, H. Y. & Leu, J. Y. Mitochondrial-nuclear co-evolution leads to hybrid incompatibility through pentatricopeptide repeat proteins. EMBO Rep. 18, 87–101 (2017).

    CAS  PubMed  Google Scholar 

  37. 37

    Lee, H. Y. et al. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135, 1065–1073 (2008).

    CAS  PubMed  Google Scholar 

  38. 38

    Anderson, J. B. et al. Determinants of divergent adaptation and Dobzhansky-Muller interaction in experimental yeast populations. Curr. Biol. 20, 1383–1388 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39

    Delneri, D. et al. Engineering evolution to study speciation in yeasts. Nature 422, 68–72 (2003).

    CAS  PubMed  Google Scholar 

  40. 40

    Fischer, G., James, S. A., Roberts, I. N., Oliver, S. G. & Louis, E. J. Chromosomal evolution in Saccharomyces. Nature 405, 451–454 (2000).

    CAS  PubMed  Google Scholar 

  41. 41

    Charron, G., Leducq, J. B. & Landry, C. R. Chromosomal variation segregates within incipient species and correlates with reproductive isolation. Mol. Ecol. 23, 4362–4372 (2014).

    PubMed  Google Scholar 

  42. 42

    Livingstone, K. & Rieseberg, L. Chromosomal evolution and speciation: a recombination-based approach. New Phytol. 161, 107–112 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43

    Ayala, F. J. & Coluzzi, M. Chromosome speciation: humans, Drosophila, and mosquitoes. Proc. Natl Acad. Sci. USA 102 (Suppl. 1), 6535–6542 (2005).

    CAS  PubMed  Google Scholar 

  44. 44

    Greig, D., Louis, E. J., Borts, R. H. & Travisano, M. Hybrid speciation in experimental populations of yeast. Science 298, 1773–1775 (2002).

    CAS  PubMed  Google Scholar 

  45. 45

    Schumer, M., Rosenthal, G. G. & Andolfatto, P. How common is homoploid hybrid speciation? Evolution 68, 1553–1560 (2014).

    PubMed  Google Scholar 

  46. 46

    Barbosa, R. et al. Evidence of natural hybridization in Brazilian wild lineages of Saccharomyces cerevisiae. Genome Biol. Evol. 8, 317–329 (2016). This study reports that introgression from S. paradoxus to S. cerevisiae in natural populations could be a rapid mode of adaptation to new environments.

    PubMed  PubMed Central  Google Scholar 

  47. 47

    Peris, D. et al. Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus. PLoS Genet. 12, e1006155 (2016).

    PubMed  PubMed Central  Google Scholar 

  48. 48

    Leducq, J. B. et al. Mitochondrial recombination and introgression during speciation by hybridization. Mol. Biol. Evol. (2017).

  49. 49

    Morales, L. & Dujon, B. Evolutionary role of interspecies hybridization and genetic exchanges in yeasts. Microbiol. Mol. Biol. Rev. 76, 721–739 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50

    Antunovics, Z., Nguyen, H. V., Gaillardin, C. & Sipiczki, M. Gradual genome stabilisation by progressive reduction of the Saccharomyces uvarum genome in an interspecific hybrid with Saccharomyces cerevisiae. FEMS Yeast Res. 5, 1141–1150 (2005).

    CAS  PubMed  Google Scholar 

  51. 51

    Dunn, B., Levine, R. P. & Sherlock, G. Microarray karyotyping of commercial wine yeast strains reveals shared, as well as unique, genomic signatures. BMC Genomics 6, 53 (2005).

    PubMed  PubMed Central  Google Scholar 

  52. 52

    Querol, A. & Bond, U. The complex and dynamic genomes of industrial yeasts. FEMS Microbiol. Lett. 293, 1–10 (2009).

    CAS  PubMed  Google Scholar 

  53. 53

    Mertens, S. et al. A large set of newly created interspecific Saccharomyces hybrids increases aromatic diversity in lager beers. Appl. Environ. Microbiol. 81, 8202–8214 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    Laureau, R. et al. Extensive recombination of a yeast diploid hybrid through meiotic reversion. PLoS Genet. 12, e1005781 (2016).

    PubMed  PubMed Central  Google Scholar 

  55. 55

    Heil, C. S. D. et al. Loss of heterozygosity drives adaptation in hybrid yeast. Mol. Biol. Evol. (2017).

  56. 56

    Bui, D. T., Dine, E., Anderson, J. B., Aquadro, C. F. & Alani, E. E. A. Genetic incompatibility accelerates adaptation in yeast. PLoS Genet. 11, e1005407 (2015).

    PubMed  PubMed Central  Google Scholar 

  57. 57

    Bui, D. T. et al. Mismatch repair incompatibilities in diverse yeast populations. Genetics 205, 1459–1471 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58

    Kunicka-Styczynska, A. & Rajkowska, K. Physiological and genetic stability of hybrids of industrial wine yeasts Saccharomyces sensu stricto complex. J. Appl. Microbiol. 110, 1538–1549 (2011).

    CAS  PubMed  Google Scholar 

  59. 59

    Bellon, J. R., Schmid, F., Capone, D. L., Dunn, B. L. & Chambers, P. J. Introducing a new breed of wine yeast: interspecific hybridisation between a commercial Saccharomyces cerevisiae wine yeast and Saccharomyces mikatae. PLoS ONE 8, e62053 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. 60

    Clowers, K. J., Will, J. L. & Gasch, A. P. A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae. Mol. Ecol. 24, 5886–5898 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61

    Dunn, B. et al. Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet. 9, e1003366 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. 62

    Otto, S. P. The evolutionary consequences of polyploidy. Cell 131, 452–462 (2007).

    CAS  PubMed  Google Scholar 

  63. 63

    Albertin, W. & Marullo, P. Polyploidy in fungi: evolution after whole-genome duplication. Proc. Biol. Sci. 279, 2497–2509 (2012).

    PubMed  PubMed Central  Google Scholar 

  64. 64

    Lynch, M. et al. A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl Acad. Sci. USA 105, 9272–9277 (2008).

    CAS  PubMed  Google Scholar 

  65. 65

    Zhu, Y. O., Siegal, M. L., Hall, D. W. & Petrov, D. A. Precise estimates of mutation rate and spectrum in yeast. Proc. Natl Acad. Sci. USA 111, E2310–E2318 (2014). This study provides a direct estimation of the molecular mutation rates in S. cerevisiae from many mutation accumulation lines and different mutation classes.

    CAS  PubMed  Google Scholar 

  66. 66

    Hong, J. & Gresham, D. Molecular specificity, convergence and constraint shape adaptive evolution in nutrient-poor environments. PLoS Genet. 10, e1004041 (2014).

    PubMed  PubMed Central  Google Scholar 

  67. 67

    Mayer, V. W. & Aguilera, A. High levels of chromosome instability in polyploids of Saccharomyces cerevisiae. Mutat. Res. 231, 177–186 (1990).

    CAS  PubMed  Google Scholar 

  68. 68

    Gerstein, A. C., Chun, H. J., Grant, A. & Otto, S. P. Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet. 2, e145 (2006).

    PubMed  PubMed Central  Google Scholar 

  69. 69

    Gerstein, A. C., McBride, R. M. & Otto, S. P. Ploidy reduction in Saccharomyces cerevisiae. Biol. Lett. 4, 91–94 (2008).

    PubMed  Google Scholar 

  70. 70

    Forche, A. et al. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 6, e110 (2008).

    PubMed  PubMed Central  Google Scholar 

  71. 71

    Zorgo, E. et al. Ancient evolutionary trade-offs between yeast ploidy states. PLoS Genet. 9, e1003388 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72

    Ezov, T. K. et al. Molecular-genetic biodiversity in a natural population of the yeast Saccharomyces cerevisiae from “Evolution Canyon”: microsatellite polymorphism, ploidy and controversial sexual status. Genetics 174, 1455–1468 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. 73

    Selmecki, A. M. et al. Polyploidy can drive rapid adaptation in yeast. Nature 519, 349–352 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 74

    Madlung, A. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity (Edinb.) 110, 99–104 (2013).

    CAS  Google Scholar 

  75. 75

    Anderson, C. A. et al. Ploidy variation in multinucleate cells changes under stress. Mol. Biol. Cell 26, 1129–1140 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76

    Giam, M. & Rancati, G. Aneuploidy and chromosomal instability in cancer: a jackpot to chaos. Cell Div. 10, 3 (2015).

    PubMed  PubMed Central  Google Scholar 

  77. 77

    Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. (2017).

  78. 78

    Kellis, M., Birren, B. W. & Lander, E. S. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428, 617–624 (2004).

    CAS  PubMed  Google Scholar 

  79. 79

    Gordon, J. L., Byrne, K. P. & Wolfe, K. H. Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet. 5, e1000485 (2009).

    PubMed  PubMed Central  Google Scholar 

  80. 80

    Wolfe, K. H. & Shields, D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708–713 (1997).

    CAS  PubMed  Google Scholar 

  81. 81

    Marcet-Houben, M. & Gabaldon, T. Beyond the whole-genome duplication: phylogenetic evidence for an ancient interspecies hybridization in the baker's yeast lineage. PLoS Biol. 13, e1002220 (2015). This paper reports that the Saccharomyces WGD event results from the mating of two different ancestral species rather than from the doubling of DNA from only one ancestor species.

    PubMed  PubMed Central  Google Scholar 

  82. 82

    Guan, Y., Dunham, M. J. & Troyanskaya, O. G. Functional analysis of gene duplications in Saccharomyces cerevisiae. Genetics 175, 933–943 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. 83

    Byrne, K. P. & Wolfe, K. H. The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 15, 1456–1461 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84

    Kondrashov, F. A., Rogozin, I. B., Wolf, Y. I. & Koonin, E. V. Selection in the evolution of gene duplications. Genome Biol. (2002).

  85. 85

    Kondrashov, F. A. Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc. Biol. Sci. 279, 5048–5057 (2012).

    PubMed  PubMed Central  Google Scholar 

  86. 86

    Brown, C. J., Todd, K. M. & Rosenzweig, R. F. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15, 931–942 (1998).

    CAS  PubMed  Google Scholar 

  87. 87

    Payen, C. et al. The dynamics of diverse segmental amplifications in populations of Saccharomyces cerevisiae adapting to strong selection. G3 (Bethesda) 4, 399–409 (2014).

    Google Scholar 

  88. 88

    Kito, K. et al. Yeast interspecies comparative proteomics reveals divergence in expression profiles and provides insights into proteome resource allocation and evolutionary roles of gene duplication. Mol. Cell. Proteomics 15, 218–235 (2016).

    CAS  PubMed  Google Scholar 

  89. 89

    Gout, J. F. & Lynch, M. Maintenance and loss of duplicated genes by dosage subfunctionalization. Mol. Biol. Evol. 32, 2141–2148 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. 90

    Papp, B., Pal, C. & Hurst, L. D. Dosage sensitivity and the evolution of gene families in yeast. Nature 424, 194–197 (2003).

    CAS  PubMed  Google Scholar 

  91. 91

    Kondrashov, F. A. & Kondrashov, A. S. Role of selection in fixation of gene duplications. J. Theor. Biol. 239, 141–151 (2006).

    CAS  PubMed  Google Scholar 

  92. 92

    Bleuven, C. & Landry, C. R. Molecular and cellular bases of adaptation to a changing environment in microorganisms. Proc. Biol. Sci. (2016).

  93. 93

    Lynch, M. & Katju, V. The altered evolutionary trajectories of gene duplicates. Trends Genet. 20, 544–549 (2004).

    CAS  PubMed  Google Scholar 

  94. 94

    Qian, W. & Zhang, J. Genomic evidence for adaptation by gene duplication. Genome Res. 24, 1356–1362 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95

    He, X. & Zhang, J. Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169, 1157–1164 (2005).

    PubMed  PubMed Central  Google Scholar 

  96. 96

    Force, A. et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531–1545 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. 97

    Landry, C. R., Oh, J., Hartl, D. L. & Cavalieri, D. Genome-wide scan reveals that genetic variation for transcriptional plasticity in yeast is biased towards multi-copy and dispensable genes. Gene 366, 343–351 (2006).

    CAS  PubMed  Google Scholar 

  98. 98

    Freschi, L., Courcelles, M., Thibault, P., Michnick, S. W. & Landry, C. R. Phosphorylation network rewiring by gene duplication. Mol. Syst. Biol. 7, 504 (2011).

    PubMed  PubMed Central  Google Scholar 

  99. 99

    Wapinski, I. et al. Gene duplication and the evolution of ribosomal protein gene regulation in yeast. Proc. Natl Acad. Sci. USA 107, 5505–5510 (2010).

    CAS  PubMed  Google Scholar 

  100. 100

    Parenteau, J. et al. Preservation of gene duplication increases the regulatory spectrum of ribosomal protein genes and enhances growth under stress. Cell Rep. 13, 2516–2526 (2015).

    CAS  PubMed  Google Scholar 

  101. 101

    Mattenberger, F., Sabater-Munoz, B., Toft, C. & Fares, M. A. The phenotypic plasticity of duplicated genes in Saccharomyces cerevisiae and the origin of adaptations. G3 (Bethesda) 7, 63–75 (2017). This study demonstrates that duplicate genes respond more specifically to stress than singletons, a transcriptional plasticity that is potentially involved in adaptation.

    CAS  Google Scholar 

  102. 102

    Diss, G. et al. Gene duplication can impart fragility, not robustness, in the yeast protein interaction network. Science 355, 630–634 (2017).

    CAS  PubMed  Google Scholar 

  103. 103

    Johnston, M. A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Microbiol. Rev. 51, 458–476 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. 104

    Kuang, M. C., Hutchins, P. D., Russell, J. D., Coon, J. J. & Hittinger, C. T. Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network. eLife 5, e19027 (2016). This paper illustrates the important involvement of duplication in the evolution of transcriptional and metabolic networks by investigating differences in the galactose utilization network among Saccharomyces species.

    PubMed  PubMed Central  Google Scholar 

  105. 105

    Warringer, J. et al. Trait variation in yeast is defined by population history. PLoS Genet. 7, e1002111 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. 106

    Eberlein, C. et al. The rapid evolution of an ohnolog contributes to the ecological specialization of incipient yeast species. Mol. Biol. Evol. (2017).

  107. 107

    Almeida, P. et al. A population genomics insight into the Mediterranean origins of wine yeast domestication. Mol. Ecol. 24, 5412–5427 (2015).

    PubMed  Google Scholar 

  108. 108

    Strope, P. K. et al. The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res. 25, 762–774 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. 109

    Gallone, B. et al. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166, 1397–1410.e16 (2016). The most recent paper using genomic and phenotypic analyses to study the origins, evolutionary history and domestication of industrial yeasts.

    CAS  PubMed  PubMed Central  Google Scholar 

  110. 110

    Borneman, A. R., Forgan, A. H., Kolouchova, R., Fraser, J. A. & Schmidt, S. A. Whole genome comparison reveals high levels of inbreeding and strain redundancy across the spectrum of commercial wine strains of Saccharomyces cerevisiae. G3 (Bethesda) 6, 957–971 (2016).

    CAS  Google Scholar 

  111. 111

    Goncalves, M. et al. Distinct domestication trajectories in top-fermenting beer yeasts and wine yeasts. Curr. Biol. 26, 2750–2761 (2016). The most recent leading paper that presents a comprehensive comparison of domestication hallmarks between beer and wine yeasts, using genome sequence analysis.

    CAS  PubMed  Google Scholar 

  112. 112

    Ludlow, C. L. et al. Independent origins of yeast associated with coffee and cacao fermentation. Curr. Biol. 26, 965–971 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. 113

    Fay, J. C. & Benavides, J. A. Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet. 1, 66–71 (2005).

    CAS  PubMed  Google Scholar 

  114. 114

    Legras, J. L., Merdinoglu, D., Cornuet, J. M. & Karst, F. Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol. Ecol. 16, 2091–2102 (2007).

    CAS  PubMed  Google Scholar 

  115. 115

    Schacherer, J., Shapiro, J. A., Ruderfer, D. M. & Kruglyak, L. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342–345 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. 116

    Cromie, G. A. et al. Genomic sequence diversity and population structure of Saccharomyces cerevisiae assessed by RAD-seq. G3 (Bethesda) 3, 2163–2171 (2013).

    Google Scholar 

  117. 117

    Marsit, S. & Dequin, S. Diversity and adaptive evolution of Saccharomyces wine yeast: a review. FEMS Yeast Res. 15, fov067 (2015).

    PubMed  PubMed Central  Google Scholar 

  118. 118

    Eberlein, C., Leducq, J. B. & Landry, C. R. The genomics of wild yeast populations sheds light on the domestication of man's best (micro) friend. Mol. Ecol. 24, 5309–5311 (2015).

    PubMed  Google Scholar 

  119. 119

    Alexandre, H. Flor yeasts of Saccharomyces cerevisiae their ecology, genetics and metabolism. Int. J. Food Microbiol. 167, 269–275 (2013).

    CAS  PubMed  Google Scholar 

  120. 120

    Coi, A. L. et al. Genomic signatures of adaptation to wine biological ageing conditions in biofilm-forming flor yeasts. Mol. Ecol. 26, 2150–2166 (2017).

    CAS  PubMed  Google Scholar 

  121. 121

    Randez-Gil, F., Corcoles-Saez, I. & Prieto, J. A. Genetic and phenotypic characteristics of baker's yeast: relevance to baking. Annu. Rev. Food Sci. Technol. 4, 191–214 (2013).

    CAS  PubMed  Google Scholar 

  122. 122

    Bokulich, N. A., Thorngate, J. H., Richardson, P. M. & Mills, D. A. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc. Natl Acad. Sci. USA 111, E139–E148 (2014).

    CAS  PubMed  Google Scholar 

  123. 123

    Christiaens, J. F. et al. The fungal aroma gene ATF1 promotes dispersal of yeast cells through insect vectors. Cell Rep. 9, 425–432 (2014).

    CAS  PubMed  Google Scholar 

  124. 124

    Baker, E. et al. The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Mol. Biol. Evol. 32, 2818–2831 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. 125

    Marsit, S. et al. Evolutionary advantage conferred by an eukaryote-to-eukaryote gene transfer event in wine yeasts. Mol. Biol. Evol. 32, 1695–1707 (2015). This study demonstrates the adaptive advantage of a large gene cluster that was recently acquired by HGT from more distant species in wine yeasts.

    CAS  PubMed  PubMed Central  Google Scholar 

  126. 126

    Marsit, S., Sanchez, I., Galeote, V. & Dequin, S. Horizontally acquired oligopeptide transporters favour adaptation of Saccharomyces cerevisiae wine yeast to oenological environment. Environ. Microbiol. 18, 1148–1161 (2016).

    CAS  PubMed  Google Scholar 

  127. 127

    Novo, M. et al. Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc. Natl Acad. Sci. USA 106, 16333–16338 (2009).

    CAS  PubMed  Google Scholar 

  128. 128

    Yue, J. X. et al. Contrasting evolutionary genome dynamics between domesticated and wild yeasts. Nat. Genet. 49, 913–924 (2017). The most recent leading paper that presents a comprehensive comparison of evolutionary genome dynamics between domesticated and wild yeasts, using long-read sequencing.

    CAS  PubMed  PubMed Central  Google Scholar 

  129. 129

    Zimmer, A. et al. QTL dissection of Lag phase in wine fermentation reveals a new translocation responsible for Saccharomyces cerevisiae adaptation to sulfite. PLoS ONE 9, e86298 (2014).

    PubMed  PubMed Central  Google Scholar 

  130. 130

    Perez-Ortin, J. E., Querol, A., Puig, S. & Barrio, E. Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res. 12, 1533–1539 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. 131

    Fay, J. C., McCullough, H. L., Sniegowski, P. D. & Eisen, M. B. Population genetic variation in gene expression is associated with phenotypic variation in Saccharomyces cerevisiae. Genome Biol. 5, R26 (2004).

    PubMed  PubMed Central  Google Scholar 

  132. 132

    Chang, S. L., Lai, H. Y., Tung, S. Y. & Leu, J. Y. Dynamic large-scale chromosomal rearrangements fuel rapid adaptation in yeast populations. PLoS Genet. 9, e1003232 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  133. 133

    Gerstein, A. C. et al. Too much of a good thing: the unique and repeated paths toward copper adaptation. Genetics 199, 555–571 (2015).

    PubMed  Google Scholar 

  134. 134

    Zhao, Y. et al. Structures of naturally evolved CUP1 tandem arrays in yeast indicate that these arrays are generated by unequal nonhomologous recombination. G3 (Bethesda) 4, 2259–2269 (2014).

    Google Scholar 

  135. 135

    Fidalgo, M., Barrales, R. R., Ibeas, J. I. & Jimenez, J. Adaptive evolution by mutations in the FLO11 gene. Proc. Natl Acad. Sci. USA 103, 11228–11233 (2006).

    CAS  PubMed  Google Scholar 

  136. 136

    Legras, J. L. et al. Flor yeast: new perspectives beyond wine aging. Front. Microbiol. 7, 503 (2016).

    PubMed  PubMed Central  Google Scholar 

  137. 137

    Borneman, A. R., Forgan, A. H., Pretorius, I. S. & Chambers, P. J. Comparative genome analysis of a Saccharomyces cerevisiae wine strain. FEMS Yeast Res. 8, 1185–1195 (2008).

    CAS  PubMed  Google Scholar 

  138. 138

    Borneman, A. R. et al. Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet. 7, e1001287 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  139. 139

    Galeote, V. et al. FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter. Microbiology 156, 3754–3761 (2010).

    CAS  PubMed  Google Scholar 

  140. 140

    Wu, H., Ito, K. & Shimoi, H. Identification and characterization of a novel biotin biosynthesis gene in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 71, 6845–6855 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. 141

    Hall, C. & Dietrich, F. S. The reacquisition of biotin prototrophy in Saccharomyces cerevisiae involved horizontal gene transfer, gene duplication and gene clustering. Genetics 177, 2293–2307 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  142. 142

    Cheeseman, K. et al. Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nat. Commun. 5, 2876 (2014).

    PubMed  PubMed Central  Google Scholar 

  143. 143

    Ropars, J. et al. Adaptive horizontal gene transfers between multiple cheese-associated fungi. Curr. Biol. 25, 2562–2569 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. 144

    Gonzalez, S. S., Gallo, L., Climent, M. A., Barrio, E. & Querol, A. Enological characterization of natural hybrids from Saccharomyces cerevisiae and S. kudriavzevii. Int. J. Food Microbiol. 116, 11–18 (2007).

    CAS  PubMed  Google Scholar 

  145. 145

    Arroyo-Lopez, F. N., Orlic, S., Querol, A. & Barrio, E. Effects of temperature, pH and sugar concentration on the growth parameters of Saccharomyces cerevisiae, S. kudriavzevii and their interspecific hybrid. Int. J. Food Microbiol. 131, 120–127 (2009).

    CAS  PubMed  Google Scholar 

  146. 146

    Gangl, H. et al. Exceptional fermentation characteristics of natural hybrids from Saccharomyces cerevisiae and S. kudriavzevii. N. Biotechnol. 25, 244–251 (2009).

    CAS  PubMed  Google Scholar 

  147. 147

    Libkind, D. et al. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc. Natl Acad. Sci. USA 108, 14539–14544 (2011).

    CAS  PubMed  Google Scholar 

  148. 148

    Bing, J., Han, P. J., Liu, W. Q., Wang, Q. M. & Bai, F. Y. Evidence for a Far East Asian origin of lager beer yeast. Curr. Biol. 24, R380–R381 (2014).

    CAS  PubMed  Google Scholar 

  149. 149

    Okuno, M. et al. Next-generation sequencing analysis of lager brewing yeast strains reveals the evolutionary history of interspecies hybridization. DNA Res. 23, 67–80 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  150. 150

    Sipiczki, M. Interspecies hybridization and recombination in Saccharomyces wine yeasts. FEMS Yeast Res. 8, 996–1007 (2008).

    CAS  PubMed  Google Scholar 

  151. 151

    Borneman, A. R. et al. The genome sequence of the wine yeast VIN7 reveals an allotriploid hybrid genome with Saccharomyces cerevisiae and Saccharomyces kudriavzevii origins. FEMS Yeast Res. 12, 88–96 (2012).

    CAS  PubMed  Google Scholar 

  152. 152

    Erny, C. et al. Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the northern European wine-making environment. Appl. Environ. Microbiol. 78, 3256–3265 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  153. 153

    Le Jeune, C. et al. Characterization of natural hybrids of Saccharomyces cerevisiae and Saccharomyces bayanus var. uvarum. FEMS Yeast Res. 7, 540–549 (2007).

    CAS  PubMed  Google Scholar 

  154. 154

    Stelkens, R. B., Brockhurst, M. A., Hurst, G. D., Miller, E. L. & Greig, D. The effect of hybrid transgression on environmental tolerance in experimental yeast crosses. J. Evol. Biol. 27, 2507–2519 (2014).

    CAS  PubMed  Google Scholar 

  155. 155

    Bernardes, J., Stelkens, R. B. & Greig, D. Heterosis in hybrids within and between yeast species. J. Evol. Biol. 30, 538–548 (2017).

    CAS  PubMed  Google Scholar 

  156. 156

    Lopandic, K. et al. Genetically different wine yeasts isolated from Austrian vine-growing regions influence wine aroma differently and contain putative hybrids between Saccharomyces cerevisiae and Saccharomyces kudriavzevii. FEMS Yeast Res. 7, 953–965 (2007).

    CAS  PubMed  Google Scholar 

  157. 157

    Replansky, T., Koufopanou, V., Greig, D. & Bell, G. Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol. Evol. 23, 494–501 (2008).

    PubMed  Google Scholar 

  158. 158

    Dunn, B., Richter, C., Kvitek, D. J., Pugh, T. & Sherlock, G. Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res. 22, 908–924 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  159. 159

    Brown, S. L. et al. Reducing haziness in white wine by overexpression of Saccharomyces cerevisiae genes YOL155c and YDR055w. Appl. Microbiol. Biotechnol. 73, 1363–1376 (2007).

    CAS  PubMed  Google Scholar 

  160. 160

    Almeida, P. et al. A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nat. Commun. 5, 4044 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  161. 161

    Goddard, M. R. & Greig, D. Saccharomyces cerevisiae: a nomadic yeast with no niche? FEMS Yeast Res. 15, fov009 (2015).

    PubMed  PubMed Central  Google Scholar 

  162. 162

    Xia, W. et al. Population genomics reveals structure at the individual, host-tree scale and persistence of genotypic variants of the undomesticated yeast Saccharomyces paradoxus in a natural woodland. Mol. Ecol. 26, 995–1007 (2017).

    CAS  PubMed  Google Scholar 

  163. 163

    Leducq, J. B. et al. Local climatic adaptation in a widespread microorganism. Proc. Biol. Sci. 281, 20132472 (2014).

    PubMed  PubMed Central  Google Scholar 

  164. 164

    Sylvester, K. et al. Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: a survey and the discovery of eight new yeast species. FEMS Yeast Res. 15, fov002 (2015).

    PubMed  Google Scholar 

  165. 165

    Kowallik, V., Miller, E. & Greig, D. The interaction of Saccharomyces paradoxus with its natural competitors on oak bark. Mol. Ecol. 24, 1596–1610 (2015).

    PubMed  PubMed Central  Google Scholar 

  166. 166

    Naranjo, S. et al. Dissecting the genetic basis of a complex cis-regulatory adaptation. PLoS Genet. 11, e1005751 (2015).

    PubMed  PubMed Central  Google Scholar 

  167. 167

    Pena-Castillo, L. & Hughes, T. R. Why are there still over 1000 uncharacterized yeast genes? Genetics 176, 7–14 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  168. 168

    Filteau, M., Charron, G. & Landry, C. R. Identification of the fitness determinants of budding yeast on a natural substrate. ISME J. 11, 959–971 (2017). This study investigates the genetic determinants and conditions that are required for optimal growth in maple sap, using a functional genomic screen.

    CAS  PubMed  Google Scholar 

  169. 169

    Ibstedt, S. et al. Concerted evolution of life stage performances signals recent selection on yeast nitrogen use. Mol. Biol. Evol. 32, 153–161 (2015).

    CAS  PubMed  Google Scholar 

  170. 170

    Treu, L. et al. The impact of genomic variability on gene expression in environmental Saccharomyces cerevisiae strains. Environ. Microbiol. 16, 1378–1397 (2014).

    CAS  PubMed  Google Scholar 

  171. 171

    Clowers, K. J., Heilberger, J., Piotrowski, J. S., Will, J. L. & Gasch, A. P. Ecological and genetic barriers differentiate natural populations of Saccharomyces cerevisiae. Mol. Biol. Evol. 32, 2317–2327 (2015). This study investigates genetic and phenotypic differences between vineyard and oak yeast populations, using genomic tools and high-throughput sequencing technologies.

    CAS  PubMed  PubMed Central  Google Scholar 

  172. 172

    Reuter, M., Bell, G. & Greig, D. Increased outbreeding in yeast in response to dispersal by an insect vector. Curr. Biol. 17, R81–R83 (2007).

    CAS  PubMed  Google Scholar 

  173. 173

    Lang, G. I. et al. Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500, 571–574 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  174. 174

    Levy, S. F. et al. Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519, 181–186 (2015). This paper shows how the fitness effect of each de novo mutation occurring during the evolution of experimental populations can be tracked to measure their contribution to the population fitness with extremely high precision.

    CAS  PubMed  PubMed Central  Google Scholar 

  175. 175

    Charron, G., Leducq, J. B., Bertin, C., Dube, A. K. & Landry, C. R. Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America. FEMS Yeast Res. 14, 281–288 (2014).

    CAS  PubMed  Google Scholar 

  176. 176

    Mortimer, R. K., Romano, P., Suzzi, G. & Polsinelli, M. Genome renewal: a new phenomenon revealed from a genetic study of 43 strains of Saccharomyces cerevisiae derived from natural fermentation of grape musts. Yeast 10, 1543–1552 (1994).

    CAS  PubMed  Google Scholar 

  177. 177

    Filteau, M. et al. Evolutionary rescue by compensatory mutations is constrained by genomic and environmental backgrounds. Mol. Syst. Biol. 11, 832 (2015).

    PubMed  PubMed Central  Google Scholar 

  178. 178

    Lynch, M. et al. Genetic drift, selection and the evolution of the mutation rate. Nat. Rev. Genet. 17, 704–714 (2016).

    CAS  PubMed  Google Scholar 

  179. 179

    Rolland, T. & Dujon, B. Yeasty clocks: dating genomic changes in yeasts. C. R. Biol. 334, 620–628 (2011).

    CAS  PubMed  Google Scholar 

  180. 180

    Martens, K., Hallin, J., Warringer, J., Liti, G. & Parts, L. Predicting quantitative traits from genome and phenome with near perfect accuracy. Nat. Commun. 7, 11512 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  181. 181

    Nishant, K. T. et al. The baker's yeast diploid genome is remarkably stable in vegetative growth and meiosis. PLoS Genet. 6, e1001109 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  182. 182

    Gerstein, A. C., Cleathero, L. A., Mandegar, M. A. & Otto, S. P. Haploids adapt faster than diploids across a range of environments. J. Evol. Biol. 24, 531–540 (2011).

    CAS  PubMed  Google Scholar 

  183. 183

    Lang, G. I. & Murray, A. W. Mutation rates across budding yeast chromosome VI are correlated with replication timing. Genome Biol. Evol. 3, 799–811 (2011).

    PubMed  PubMed Central  Google Scholar 

  184. 184

    Lang, G. I. & Murray, A. W. Estimating the per-base-pair mutation rate in the yeast Saccharomyces cerevisiae. Genetics 178, 67–82 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  185. 185

    Park, C., Qian, W. & Zhang, J. Genomic evidence for elevated mutation rates in highly expressed genes. EMBO Rep. 13, 1123–1129 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  186. 186

    Chen, X. & Zhang, J. Yeast mutation accumulation experiment supports elevated mutation rates at highly transcribed sites. Proc. Natl Acad. Sci. USA 111, E4062 (2014).

    CAS  PubMed  Google Scholar 

  187. 187

    Bensasson, D. Evidence for a high mutation rate at rapidly evolving yeast centromeres. BMC Evol. Biol. 11, 211 (2011).

    PubMed  PubMed Central  Google Scholar 

  188. 188

    Serero, A., Jubin, C., Loeillet, S., Legoix-Ne, P. & Nicolas, A. G. Mutational landscape of yeast mutator strains. Proc. Natl Acad. Sci. USA 111, 1897–1902 (2014).

    CAS  PubMed  Google Scholar 

  189. 189

    Hittinger, C. T. et al. Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464, 54–58 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  190. 190

    McGovern, P. E. et al. Fermented beverages of pre- and proto-historic China. Proc. Natl Acad. Sci. USA 101, 17593–17598 (2004).

    CAS  PubMed  Google Scholar 

  191. 191

    Michel, R. H., McGovern, P. E. & Badler, V. R. Chemical evidence for ancient beer. Nature 360, 24 (1992).

    Google Scholar 

  192. 192

    McGovern, P. E., Glusker, D. L., Exner, L. J. & Voigt, M. M. Neolithic resinated wine. Nature 381, 480–481 (1996).

    CAS  Google Scholar 

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The authors thank the members of the Landry laboratory, N. Aubin-Horth and the three anonymous reviewers for useful comments on the manuscript. This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Canadian Institutes of Health Research (CIHR). C.R.L. holds the Canada Research Chair in Evolutionary Cell and Systems Biology.

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Conditions related to human activities.

Whole-genome duplication

(WGD). Process by which the number of chromosomes is doubled.


A group of species that diverged from the group of interest before its most recent common ancestor.

Reproductive isolation

A mechanism that prevents the production of viable or fertile offspring between species.


Crosses between species or divergent populations.


The number of sets of homologous chromosomes in a cell for a given species, in which haploid cells have one set, diploid cells have two sets and polyploid cells have multiple (more than two) sets.

Postzygotic isolation

A mechanism that limits the reproductive success or survival of offspring.

Prezygotic isolation

A mechanism that prevents the fertilization of eggs or, in the case of yeast, the formation of zygotes.


The presence in a cell of an abnormal number of chromosomes that deviates from a multiple of the normal number.

Bateson–Dobzhansky–Muller incompatibilities

(BDMIs). Interactions between genetic elements that reduce the viability or the fertility of hybrids between populations or species. Mito-nuclear BDMIs involve components encoded by the mitochondrial genome and the nuclear genome.


The integration of genomic regions of one species or population into the genome of another species or population.

Loss of heterozygosity

(LOH). The loss of one allele at a heterozygous locus. This loss can occur by mutation, deletion or gene conversion, using the other allele as a template. LOH in yeast genomes often corresponds to large-scale chromosomal regions encompassing multiple neighbouring genes.


Interaction between alleles of genes leading to a lower (negative epitasis) or increased (positive epistasis) phenotypic value than expected from their single contributions.


Polyploidization event in which the chromosome sets derive from a single species.


Polyploidization event as a result of hybridization between distinct species.


The physical colocalization of orthologous genes on the same chromosomes between individuals or species.


Duplicated genes originating from a whole-genome duplication event.


Genes related by duplication within a species.

Single-nucleotide variation

(SNV). A single-nucleotide change observed by comparing genomes within or between populations.

Horizontal gene transfer

(HGT). A process by which an organism incorporates genetic material from another organism that does not belong to its line of ancestry.

Balanced rearrangements

Changes in chromosomal gene order that do not remove or duplicate any of the DNA of the chromosomes. For example, inversions, reciprocal translocations and transpositions.

Chromosomal cores

Internal parts of chromosomes that exclude subtelomeres and terminal chromosome ends.

Convergent evolution

Evolution that leads populations to the same phenotypic or genotypic outcomes from distinct initial genotypes or phenotypes.


Fitness advantage of hybrids over parental species or individuals.


A mechanism by which certain mutations increase in frequency because they are linked to advantageous mutations.

Clonal interference

Competition among cells of a population that acquire advantageous mutations. This competition may prevent the fixation of one allele or the other.

Standing genetic variation

Genetic variation that exists at a given point in time in a population.

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Marsit, S., Leducq, JB., Durand, É. et al. Evolutionary biology through the lens of budding yeast comparative genomics. Nat Rev Genet 18, 581–598 (2017).

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