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Domestication reprogrammed the budding yeast life cycle

Abstract

Domestication of plants and animals is the foundation for feeding the world human population but can profoundly alter the biology of the domesticated species. Here we investigated the effect of domestication on one of our prime model organisms, the yeast Saccharomyces cerevisiae, at a species-wide level. We tracked the capacity for sexual and asexual reproduction and the chronological life span across a global collection of 1,011 genome-sequenced yeast isolates and found a remarkable dichotomy between domesticated and wild strains. Domestication had systematically enhanced fermentative and reduced respiratory asexual growth, altered the tolerance to many stresses and abolished or impaired the sexual life cycle. The chronological life span remained largely unaffected by domestication and was instead dictated by clade-specific evolution. We traced the genetic origins of the yeast domestication syndrome using genome-wide association analysis and genetic engineering and disclosed causative effects of aneuploidy, gene presence/absence variations, copy number variations and single-nucleotide polymorphisms. Overall, we propose domestication to be the most dramatic event in budding yeast evolution, raising questions about how much domestication has distorted our understanding of the natural biology of this key model species.

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Fig. 1: Genomic and phenomic portraits of domesticated and wild yeast.
Fig. 2: Domestication promoted fermentative over respiratory growth.
Fig. 3: Domestication abolished or impaired yeast sporulation.
Fig. 4: Genetic control of sporulation efficiency.
Fig. 5: Domestication only weakly extended the yeast CLS.
Fig. 6: HPF1-like and WHI2 loss-of-function variants impairs yeast CLS.

Data availability

All data generated or analysed during this study are included in this article and the Supplementary Information. Source data are provided with this paper.

References

  1. Driscoll, C. A., Macdonald, D. W. & O’Brien, S. J. From wild animals to domestic pets, an evolutionary view of domestication. Proc. Natl Acad. Sci. USA 106, 9971–9978 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Zeder, M. A. The origins of agriculture in the Near East. Curr. Anthropol. 52, S221–S235 (2011).

    Google Scholar 

  3. Darwin, C. The Variation of Animals and Plants under Domestication (John Murray, 1868).

  4. Pontes, A., Čadež, N., Gonçalves, P. & Sampaio, J. P. A quasi-domesticate relic hybrid population of Saccharomyces cerevisiae × S. paradoxus adapted to olive brine. Front. Genet. 10, 449 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Brown, T. A., Jones, M. K., Powell, W. & Allaby, R. G. The complex origins of domesticated crops in the Fertile Crescent. Trends Ecol. Evol. 24, 103–109 (2009).

    PubMed  Google Scholar 

  6. Wilkins, A. S., Wrangham, R. W. & Fitch, W. T. The ‘domestication syndrome’ in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics 197, 795–808 (2014).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Gallone, B. et al. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166, 1397–1410 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Gonçalves, M. et al. Distinct domestication trajectories in top-fermenting beer yeasts and wine yeasts. Curr. Biol. 26, 2750–2761 (2016).

    PubMed  Google Scholar 

  10. Gallone, B. et al. Origins, evolution, domestication and diversity of Saccharomyces beer yeasts. Curr. Opin. Biotechnol. 49, 148–155 (2018).

    CAS  PubMed  Google Scholar 

  11. Duan, S.-F. et al. Reverse evolution of a classic gene network in yeast offers a competitive advantage. Curr. Biol. 29, 1126–1136 (2019).

    CAS  PubMed  Google Scholar 

  12. Jespersen, L., Nielsen, D. S., Hønholt, S. & Jakobsen, M. Occurrence and diversity of yeasts involved in fermentation of West African cocoa beans. FEMS Yeast Res. 5, 441–453 (2005).

    CAS  PubMed  Google Scholar 

  13. 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 

  14. 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 

  15. Ezeronye, O. U. & Legras, J.-L. Genetic analysis of Saccharomyces cerevisiae strains isolated from palm wine in eastern Nigeria. Comparison with other African strains. J. Appl. Microbiol. 106, 1569–1578 (2009).

    CAS  PubMed  Google Scholar 

  16. Oliva Hernández, A. A., Taillandier, P., Reséndez Pérez, D., Narváez Zapata, J. A. & Larralde Corona, C. P. The effect of hexose ratios on metabolite production in Saccharomyces cerevisiae strains obtained from the spontaneous fermentation of mezcal. Antonie Van Leeuwenhoek 103, 833–843 (2013).

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  19. 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 

  20. 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 

  21. 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 

  22. Barnett, J. A. A history of research on yeasts 10: foundations of yeast genetics. Yeast 24, 799–845 (2007).

    CAS  PubMed  Google Scholar 

  23. Engel, S. R. et al. The reference genome sequence of Saccharomyces cerevisiae: then and now. G3 4, 389–398 (2014).

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  25. Liti, G. The fascinating and secret wild life of the budding yeast S. cerevisiae. eLife 4, e05835 (2015).

  26. Peter, J. et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature 556, 339–344 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Bergström, A. et al. A high-definition view of functional genetic variation from natural yeast genomes. Mol. Biol. Evol. 31, 872–888 (2014).

    PubMed  PubMed Central  Google Scholar 

  28. Yue, J.-X. et al. Contrasting evolutionary genome dynamics between domesticated and wild yeasts. Nat. Genet. 49, 913–924 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Brown, C. A., Murray, A. W. & Verstrepen, K. J. Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr. Biol. 20, 895–903 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Legras, J.-L. et al. Adaptation of S. cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. Mol. Biol. Evol. 35, 1712–1727 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Pietrzak, U. & McPhail, D. C. Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia. Geoderma 122, 151–166 (2004).

    CAS  Google Scholar 

  33. Bencko, V. & Yan Li Foong, F. The history of arsenical pesticides and health risks related to the use of Agent Blue. Ann. Agric. Environ. Med. 24, 312–316 (2017).

    CAS  PubMed  Google Scholar 

  34. 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 

  35. Bell, P. J., Higgins, V. J. & Attfield, P. V. Comparison of fermentative capacities of industrial baking and wild-type yeasts of the species Saccharomyces cerevisiae in different sugar media. Lett. Appl. Microbiol. 32, 224–229 (2001).

    CAS  PubMed  Google Scholar 

  36. Hazelwood, L. A., Daran, J.-M., van Maris, A. J. A., Pronk, J. T. & Dickinson, J. R. The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl. Environ. Microbiol. 74, 2259–2266 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Bonander, N. et al. Transcriptome analysis of a respiratory Saccharomyces cerevisiae strain suggests the expression of its phenotype is glucose insensitive and predominantly controlled by Hap4, Cat8 and Mig1. BMC Genomics 9, 365 (2008).

    PubMed  PubMed Central  Google Scholar 

  38. Carlson, M. & Botstein, D. Two differentially regulated mRNAs with different 5′ ends encode secreted with intracellular forms of yeast invertase. Cell 28, 145–154 (1982).

    CAS  PubMed  Google Scholar 

  39. Rai, R., Genbauffe, F. S., Sumrada, R. A. & Cooper, T. G. Identification of sequences responsible for transcriptional activation of the allantoate permease gene in Saccharomyces cerevisiae. Mol. Cell. Biol. 9, 602–608 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Naumov, G. I., Naumova, E. S. & Michels, C. A. Genetic variation of the repeated MAL loci in natural populations of Saccharomyces cerevisiae and Saccharomyces paradoxus. Genetics 136, 803–812 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Honigberg, S. M. & Purnapatre, K. Signal pathway integration in the switch from the mitotic cell cycle to meiosis in yeast. J. Cell Sci. 116, 2137–2147 (2003).

    CAS  PubMed  Google Scholar 

  42. Zaman, S., Lippman, S. I., Zhao, X. & Broach, J. R. How Saccharomyces responds to nutrients. Annu. Rev. Genet. 42, 27–81 (2008).

    CAS  PubMed  Google Scholar 

  43. Coluccio, A. E., Rodriguez, R. K., Kernan, M. J. & Neiman, A. M. The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS ONE 3, e2873 (2008).

    PubMed  PubMed Central  Google Scholar 

  44. Gerke, J., Lorenz, K. & Cohen, B. Genetic interactions between transcription factors cause natural variation in yeast. Science 323, 498–501 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Duan, S.-F. et al. The origin and adaptive evolution of domesticated populations of yeast from Far East Asia. Nat. Commun. 9, 2690 (2018).

    PubMed  PubMed Central  Google Scholar 

  46. Taxis, C. et al. Spore number control and breeding in Saccharomyces cerevisiae: a key role for a self-organizing system. J. Cell Biol. 171, 627–640 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Magwene, P. M. et al. Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 108, 1987–1992 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Fay, J. C. The molecular basis of phenotypic variation in yeast. Curr. Opin. Genet. Dev. 23, 672–677 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Ben-Ari, G. et al. Four linked genes participate in controlling sporulation efficiency in budding yeast. PLoS Genet. 2, e195 (2006).

    PubMed  PubMed Central  Google Scholar 

  50. Tomar, P. et al. Sporulation genes associated with sporulation efficiency in natural isolates of yeast. PLoS ONE 8, e69765 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Galardini, M. et al. The impact of the genetic background on gene deletion phenotypes in Saccharomyces cerevisiae. Mol. Syst. Biol. 15, e8831 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Allen, C. et al. Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J. Cell Biol. 174, 89–100 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Aragon, A. D. et al. Characterization of differentiated quiescent and nonquiescent cells in yeast stationary-phase cultures. Mol. Biol. Cell 19, 1271–1280 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Davidson, G. S. et al. The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures. Mol. Biol. Cell 22, 988–998 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Klosinska, M. M., Crutchfield, C. A., Bradley, P. H., Rabinowitz, J. D. & Broach, J. R. Yeast cells can access distinct quiescent states. Genes Dev. 25, 336–349 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Bigey, F. et al. Evidence for two main domestication trajectories in Saccharomyces cerevisiae linked to distinct bread-making processes. Curr. Biol. 31, 722–732 (2021).

    CAS  PubMed  Google Scholar 

  57. Sunshine, A. B. et al. Aneuploidy shortens replicative lifespan in Saccharomyces cerevisiae. Aging Cell 15, 317–324 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Chen, X. et al. Mek1 coordinates meiotic progression with DNA break repair by directly phosphorylating and inhibiting the yeast pachytene exit regulator Ndt80. PLoS Genet. 14, e1007832 (2018).

    PubMed  PubMed Central  Google Scholar 

  59. Leadsham, J. E. et al. Whi2p links nutritional sensing to actin-dependent Ras-cAMP-PKA regulation and apoptosis in yeast. J. Cell Sci. 122, 706–715 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Longo, V. D., Shadel, G. S., Kaeberlein, M. & Kennedy, B. Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab. 16, 18–31 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. van Leeuwen, J. et al. Exploring genetic suppression interactions on a global scale. Science https://www.science.org/doi/10.1126/science.aag0839 (2016).

  62. Offei, B., Vandecruys, P., De Graeve, S., Foulquié-Moreno, M. R. & Thevelein, J. M. Unique genetic basis of the distinct antibiotic potency of high acetic acid production in the probiotic yeast Saccharomyces cerevisiae var. boulardii. Genome Res. 29, 1478–1494 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Barré, B. P. et al. Intragenic repeat expansion in the cell wall protein gene HPF1 controls yeast chronological aging. Genome Res. 30, 697–710 (2020).

    PubMed  PubMed Central  Google Scholar 

  64. Verstrepen, K. J., Jansen, A., Lewitter, F. & Fink, G. R. Intragenic tandem repeats generate functional variability. Nat. Genet. 37, 986–990 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Gemayel, R., Vinces, M. D., Legendre, M. & Verstrepen, K. J. Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu. Rev. Genet. 44, 445–477 (2010).

    CAS  PubMed  Google Scholar 

  66. Stern, D. L. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764 (2013).

    CAS  PubMed  Google Scholar 

  67. Jambhekar, A. & Amon, A. Control of meiosis by respiration. Curr. Biol. 18, 969–975 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Zhao, H. et al. A role for the respiratory chain in regulating meiosis initiation in Saccharomyces cerevisiae. Genetics 208, 1181–1194 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Zörgö, E. et al. Life history shapes trait heredity by accumulation of loss-of-function alleles in yeast. Mol. Biol. Evol. 29, 1781–1789 (2012).

    PubMed  Google Scholar 

  70. Shen, X.-X. et al. Tempo and mode of genome evolution in the budding yeast subphylum. Cell 175, 1533–1545 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  72. Tattini, L. et al. Accurate tracking of the mutational landscape of diploid hybrid genomes. Mol. Biol. Evol. 36, 2861–2877 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  75. Gutierrez, H., Taghizada, B. & Meneghini, M. D. Nutritional and meiotic induction of transiently heritable stress resistant states in budding yeast. Micro. Cell 5, 511–521 (2018).

    CAS  Google Scholar 

  76. Kupiec, M. & Steinlauf, R. Damage-induced ectopic recombination in the yeast Saccharomyces cerevisiae. Mutat. Res. 384, 33–44 (1997).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Wang, Q.-M., Liu, W.-Q., Liti, G., Wang, S.-A. & Bai, F.-Y. Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21, 5404–5417 (2012).

    PubMed  Google Scholar 

  79. D’Angiolo, M. et al. A yeast living ancestor reveals the origin of genomic introgressions. Nature 587, 420–425 (2020).

    PubMed  Google Scholar 

  80. Heslop-Harrison, J. S. & Schwarzacher, T. Domestication, genomics and the future for banana. Ann. Bot. 100, 1073–1084 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Shemesh-Mayer, E. et al. Garlic (Allium sativum L.) fertility: transcriptome and proteome analyses provide insight into flower and pollen development. Front. Plant Sci. 6, 271 (2015).

    PubMed  PubMed Central  Google Scholar 

  82. Zackrisson, M. et al. Scan-o-matic: high-resolution microbial phenomics at a massive scale. G3 6, 3003–3014 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Gerke, J. P., Chen, C. T. L. & Cohen, B. A. Natural isolates of Saccharomyces cerevisiae display complex genetic variation in sporulation efficiency. Genetics 174, 985–997 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Fabrizio, P. & Longo, V. D. The chronological life span of Saccharomyces cerevisiae. Methods Mol. Biol. 371, 89–95 (2007).

    CAS  PubMed  Google Scholar 

  85. Herker, E. et al. Chronological aging leads to apoptosis in yeast. J. Cell Biol. 164, 501–507 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Wlodkowic, D., Skommer, J. & Darzynkiewicz, Z. Flow cytometry-based apoptosis detection. Methods Mol. Biol. 559, 19–32 (2009).

    CAS  PubMed  Google Scholar 

  87. Matecic, M. et al. A microarray-based genetic screen for yeast chronological aging factors. PLoS Genet. 6, e1000921 (2010).

    PubMed  PubMed Central  Google Scholar 

  88. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Kumar, P., Henikoff, S. & Ng, P. C. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4, 1073–1081 (2009).

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank F. van Werven, G. Fisher and B. Llorente for the helpful discussions and B. Cohen for the kind gift of the SPS2::GFP tagged strains. This work was supported by Agence Nationale de la Recherche (ANR-15-IDEX-01, ANR-18-CE12-0004, ANR-20-CE13-0010, ANR-20-CE12-0020), Fondation pour la Recherche Médicale (EQU202003010413), CEFIPRA, Fondation ARC (no. ARCPJA32020070002320), the Swedish Research Council (2014-6547, 2014-4605, 2018-03638 and 2018-03453) and the Slovenian Research Agency (P1-0207), COFUND BoostUrCAreer programme (funded by EU Horizon 2020, Marie Curie grant agreement no. 847581, Région SUD PACA and IDEX UCAjedi).

Author information

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Authors

Contributions

M.D.C., B.P.B., U.P., J.W. and G.L. designed the experiments. M.D.C., B.P.B., K.P., A.I., C.V., S.K., S.S., O.C.A., G.Ž. and K.D. performed and analysed the experiments. J.S., C.T., J.W. and G.L. contributed with resources and reagents. M.D.C., B.P.B., J.W. and G.L. conceived and supervised the project. M.D.C., B.P.B., J.W. and G.L. wrote the paper.

Corresponding authors

Correspondence to Matteo De Chiara, Jonas Warringer or Gianni Liti.

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Nature Ecology & Evolution thanks José Sampaio and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Wild yeast strains grow better in presence of most stresses.

Re-analysis of the asexual growth data were taken from Peter et al. 201826. a, PCA based on all data from asexual growth largely separates wild and domesticated clades. Each clade is represented by the median value for each phenotypes. b, Boxplot of asexual growth in the 16 environments in which wild (W) are superior to domesticated (D) strains. c, Boxplot of asexual growth in the five environments in which domesticated are superior to wild strains. Box: IQR. Whiskers: 1.5x IQR. Significances (1-sided Mann–Whitney is reported in Supplementary Table 2). n = 565 and 58 for, respectively, domesticated and wild isolates, with the exception of domesticated isolates in galactose, where n = 564.

Source data

Extended Data Fig. 2 Sporulation efficiency is excellent in all wild yeast clades.

a, Distribution of sporulation efficiencies after 24 h (upper panel) and 72 h (lower panel) in traditional sporulation environment (KAc) for each phylogenetic clade. Clades are ordered according to the phylogeny26, with mosaic and long branch strains at the end. Colours indicate domesticated (red) or wild (blue). The unassigned clades are left white. Box: IQR. Whiskers: 1.5x IQR. Number of data point for each boxplot are as following: Wine/European, 312; Alpechin, 12; Brazilian bioethanol, 27; Mediterranean oak, 8; French dairy, 32; African beer, 19; Mosaic beer, 12; Mixed origin, 66; Mexican agave, 7, French Guiana human, 30; Ale beer, 17; West African Cocoa beans fermentation, 12; African palm wine, 24; CHNIII, 2; CHNII, 2; CHNI, 1; Taiwanese, 3; Far East Asia, 8; Malaysian, 5; CHNV, 2; Ecuadorean, 8; Russian, 4; North American, 11; Asian islands, 7; Sake, 41; Asian fermentation, 29; Mosaic region 1, 12; Mosaic region 2, 16; Mosaic region 3, 83; Unclustered, 38. b, Distribution of the sporulation efficiency at 24 h and 72 h for the four subclades within the Wine/European clade. The S. boulardii subgroup has completely lost the ability to sporulate. Box: IQR. Whiskers: 1.5 X IQR. n = 17,10,24,29 and 232 for, respectively, Feral wine, clinical Y’ amplification, S. boulardii, Georgian and other wine isolates. c, Sporulation efficiency in water. S. cerevisiae and S. paradoxus wild strains sporulate well, S. cerevisiae domesticated strains do not. Boxplot of the distribution of asci production (only sporulating isolates, that is asci production > 0) after 8 days in water. Box: IQR. Whiskers: 1.5x IQR. n = 4, 19 and 6 for, respectively domesticated, wild and S. paradoxus. d, Fraction of S. cerevisiae domesticated, wild and S. paradoxus isolates able to sporulate (that is sporulation efficiency > 0 after 8 days) in water.

Source data

Extended Data Fig. 3 IME1 variants control yeast sporulation variation.

a, Schematic representation of the locus of the meiotic regulator and the upstream IRT1, which overlaps the IME1 promoter. GWAS revealed that six SNPs at five sites (green stars) in the IME1 and its promoter associate to sporulation efficiency after 24 h in standard KAc. None of these correspond to the SNPs identified in Gerke et al 200944 (grey stars), which do not pass the MAF > 0.05. b, Upper panel: Distribution of IME1 GWAS sporulation hits across the sequenced strain collection (y-axis, ordered as in the tree phylogeny reported in Peter et al 201826). Several SNPs appear to be linked. Lower panel: Sporulation of strains homo- or heterozygotic for the six IME1 SNPs associated to sporulation. Box: IQR. Whiskers: 1.5x IQR. All minor SNPs, except H78R, associate to poor spore production. Number of data point for each boxplot are as following: n = 759, 44 and 47 for, respectively isolates with genotype AA, AC and CC in position −325; n = 766, 40, 44 respectively for isolates with genotype CC, CT and TT in position −181; n = 568, 5 and 184 respectively for isolates with genotype HH, HR and RR on position 78; n = 791, 30 and 29 respectively for isolates with genotype NN, NY and YY in position 311; n = 742, 5, 33, 39, 30 respectively for isolates with genotype EE, EV, VV, EG, GG in position 316. c, H78R is here restricted to a subset of domesticated clades and promotes spore production. Box: IQR. Whiskers: 1.5x IQR. n = 293, 57 and 153 respectively for domesticated isolates with genotype HH, HR and RR on position 78. d, upper panels: Inserting the C-181T variant in the strain YPS128 strongly decreased its sporulation efficiency (from 86% to 4 % asci 9 hours after meiosis induction, and from 98% to 58% after 24 h), while introducing the C allele in the CIA isolate (WT for T) increased the efficiency (from 1.7% to 22.5% asci after 24 h and from 35% to 59% asci after 168 h); bottom panels: The substitution of the R allele to the H allele massively reduced the sporulation efficiency in the isolate DBVPG6765 (from 37% to 2% asci 72 hours post-induction and from 43% to 4% 168 h). The introduction of the H78R mutation in BY4743 improved the efficiency (from 0.3% to 2% asci 72 hours post-induction and from 3.5% to 7.7% after 240 h). Time points were selected to show the maximal phenotypic effect attributed to single mutations. The asterisks indicate statistical significance (Student´s t-test).

Source data

Extended Data Fig. 4 Loss-of-function variants in SPO12 and SPO13 trigger dyads-only spore production.

a, Sporulation efficiency after 3 days in traditional sporulation medium (KAc) and the percentage of produced asci that are dyads (x-axis), after 24 h (left panel) and 72 h (right panel). Nine strains, belonging to two clusters (indicated in green and orange) efficiently enter sporulation but interrupt the meiosis cycle after meiosis I, only producing dyads. b, Micrograph of asci produced in the strain BNL, after 72 h of sporulation, with staining of the spore wall (blue). Only dyads are produced. c, Schematic representation of the protein sequences for Spo12 and Spo13 showing the positions of homozygous loss-of-function variants that trigger dyads-only production during sporulation.

Source data

Extended Data Fig. 5 Yeast CLS is clade specific and not strongly influenced by domestication.

Boxplots showing surviving cells (%) for each clade in each CLS condition and time point. Clades are ordered according to the phylogeny26, with mosaic and long branch strains at the end. French Dairy (5.F) and African beer (6.A) yeasts have the lowest survival (median < 30% survival after 7 days in SDC) while French Guiana (10.F), Mexican agave (09.M) and West African Cocoa (12.W) have the highest (median > 60% survival after 7 days in SDC). Among wild clades, the Taiwanese and Malaysian strains were short-living (<30% survival in SDC after 7 days), while the Far East Russian and North American oak strains all were long-living (>60% survival after 7 days in SDC). Restricting the initially available calories from 2% sugar (SDC) to 0.5% sugar (CR) extended CLS of virtually all clades, and more particularly of those with poor survival in SDC. Box: IQR. Whiskers: 1.5 X IQR. Number of data point for each boxplot are as following: Wine/European, 306; Alpechin, 12; Brazilian bioethanol, 17; Mediterranean oak, 8; French dairy, 31; African beer, 19; Mosaic beer, 9; Mixed origin, 56; Mexican agave, 7, French Guiana human, 30; Ale beer, 8; West African Cocoa beans fermentation, 12; African palm wine, 22; CHNIII, 2; CHNII, 2; CHNI, 1; Taiwanese, 3; Far East Asia, 8; Malaysian, 4; CHNV, 2; Ecuadorean, 9; Russian, 4; North American, 11; Asian islands, 8; Sake, 43; Asian fermentation, 29; Mosaic region 1, 12; Mosaic region 2, 15; Mosaic region 3, 80; Unclustered, 37.

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Extended Data Fig. 6 Aneuploidy and polyploidy effects on CLS.

For each time point and medium (SDC, which is moderately calorie restricted, or CR, which is severely caloric restricted) the distribution of the fraction of surviving cells is shown. Both aneuploidy and polyploidy are associated with a shorter CLS. Box: IQR. Whiskers: 1.5 X IQR. n = 581, 34 and 132 for, respectively, diploid euploid (EU 2 N), aneuploid diploid (AN 2 N) and polyploid euploid (EU > 2 N).

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Extended Data Fig. 7 WHI2 loss-of-function variants and HPF1-like presence associate to a short CLS.

a, Predicted loss-of-function variants in WHI2 associate to a short life span in the 1011 strain collection. Significant 2-sided Mann–Whitney results are indicated (SDC at day 7, p = 8.6e-07, CR at day 7, p = 1.4e-12, CR at day 21, p = 5.0e-03. Box: IQR. Whiskers: 1.5 X IQR. n = 747 and 60 for, respectively, isolates with a functioning allele of WHI2 and isolates with a loss-of-function in WHI2. b, The presence of HPF1-like is associated with a short life span in a calorie restricted CR medium. Significant 2-sided Mann–Whitney results are indicated (CR at day 7, p = 1.9e-09, CR at day 21, p = 8.6e-09, CR at day 35, p = 1.6e-05. Box: IQR. Whiskers: 1.5 X IQR. n = 718 and 89 for, respectively, isolates without the HPF1-like ORF and isolates with it in the 1011 strain collection.

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Extended Data Fig. 8 Correlations among life cycle traits.

Although traits of the same class (cell doubling time, yield, sporulation and CLS) broadly correlated, traits of different classes remain poorly correlated.

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Extended Data Fig. 9 Genetic variants rarely associate to more than one class of life cycle traits.

a, Only few genetic variants detected by GWAS associate to more than one class of life cycle traits and no genetic variant associate to more than two. b, Genetic variants rarely affect more than one life cycle trait (environment, time point) even within the same trait class in more than one environment or at more than one time point. Arrows indicate the position of pleiotropic exceptions discussed in the text.

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Supplementary information

Supplementary Information

Supplementary Notes 1 and 2, Fig. 1 and references.

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Peer Review Information

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Supplementary Tables 1–13.

Supplementary Data

Variant matrix for GWAS generated by Plink in .bed, .bim and .fam formats. The matrix contains all biallelic positions known for the sequenced isolates with MAF > 5%, as well as LOF, presence and absence, and CNVs (for the latter, the ORFs absence has been coded as missing data).

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De Chiara, M., Barré, B.P., Persson, K. et al. Domestication reprogrammed the budding yeast life cycle. Nat Ecol Evol 6, 448–460 (2022). https://doi.org/10.1038/s41559-022-01671-9

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