Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Interspecific hybridization facilitates niche adaptation in beer yeast

Abstract

Hybridization between species often leads to non-viable or infertile offspring, yet examples of evolutionarily successful interspecific hybrids have been reported in all kingdoms of life. However, many questions on the ecological circumstances and evolutionary aftermath of interspecific hybridization remain unanswered. In this study, we sequenced and phenotyped a large set of interspecific yeast hybrids isolated from brewing environments to uncover the influence of interspecific hybridization in yeast adaptation and domestication. Our analyses demonstrate that several hybrids between Saccharomyces species originated and diversified in industrial environments by combining key traits of each parental species. Furthermore, posthybridization evolution within each hybrid lineage reflects subspecialization and adaptation to specific beer styles, a process that was accompanied by extensive chimerization between subgenomes. Our results reveal how interspecific hybridization provides an important evolutionary route that allows swift adaptation to novel environments.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Tanglegram depicting the relationships between Saccharomyces pure species and interspecific hybrids.
Fig. 2: Genome structure of Saccharomyces interspecific hybrids.
Fig. 3: Distribution of chimeric breakpoints across interspecific hybrids.
Fig. 4: Trait variation and niche adaptation of interspecific hybrids.
Fig. 5: The genetic basis of loss of 4-VG production in S.cer × S.eub hybrids.
Fig. 6: Time-calibrated phylogeny of S.cer Beer 1 clade.

Data availability

All raw sequencing reads generated in this study have been deposited to the NCBI Short Read Archive (BioProject accession: PRJNA516557).

References

  1. Mallet, J., Besansky, N. & Hahn, M. W. How reticulated are species? BioEssays 38, 140–149 (2016).

    PubMed  Article  Google Scholar 

  2. Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  4. Nolte, A. W. & Tautz, D. Understanding the onset of hybrid speciation. Trends Genet. 26, 54–58 (2010).

    CAS  PubMed  Article  Google Scholar 

  5. Baack, E. J. & Rieseberg, L. H. A genomic view of introgression and hybrid speciation. Curr. Opin. Genet. Dev. 17, 513–518 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. Rieseberg, L. H., Archer, M. A. & Wayne, R. K. Transgressive segregation, adaptation and speciation. Heredity 83, 363–372 (1999).

    PubMed  Article  Google Scholar 

  7. Lamichhaney, S. et al. Rapid hybrid speciation in Darwin’s finches. Science 359, 224–228 (2018).

    CAS  PubMed  Article  Google Scholar 

  8. Rieseberg, L. H. et al. Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129, 149–165 (2007).

    PubMed  Article  Google Scholar 

  9. Rieseberg, L. H. Homoploid reticulate evolution in Helianthus (Asteraceae): evidence from ribosomal genes. Am. J. Bot. 78, 1218–1237 (1991).

    Article  Google Scholar 

  10. Schwarzbach, A. E. & Rieseberg, L. H. Likely multiple origins of a diploid hybrid sunflower species. Mol. Ecol. 11, 1703–1715 (2002).

    CAS  PubMed  Article  Google Scholar 

  11. Pryszcz, L. P. et al. The genomic aftermath of hybridization in the opportunistic pathogen Candida metapsilosis. PLoS Genet. 11, e1005626 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  12. Kellis, M., Patterson, N., Endrizzi, M., Birren, B. & Lander, E. S. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423, 241–254 (2003).

    CAS  Article  PubMed  Google Scholar 

  13. Greig, D. Reproductive isolation in Saccharomyces. Heredity 102, 39–44 (2009).

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. Hou, J., Friedrich, A., De Montigny, J. & Schacherer, J. Chromosomal rearrangements as a major mechanism in the onset of reproductive isolation in Saccharomyces cerevisiae. Curr. Biol. 24, 1153–1159 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 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  Article  Google Scholar 

  17. Naumov, G. I. et al. Natural polyploidization of some cultured yeast Saccharomyces sensu stricto: auto- and allotetraploidy. Syst. Appl. Microbiol. 23, 442–449 (2000).

    CAS  PubMed  Article  Google Scholar 

  18. Zhang, H., Skelton, A., Gardner, R. C. & Goddard, M. R. Saccharomyces paradoxus and Saccharomyces cerevisiae reside on oak trees in New Zealand: evidence for migration from Europe and interspecies hybrids. FEMS Yeast Res. 10, 941–947 (2010).

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. Nakao, Y. et al. Genome sequence of the lager brewing yeast, an interspecies hybrid. DNA Res. 16, 115–129 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. Walther, A., Hesselbart, A. & Wendland, J. Genome sequence of Saccharomyces carlsbergensis, the world’s first pure culture lager yeast. G3 4, 783–793 (2014).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  22. Dunn, B. & Sherlock, G. Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res. 18, 1610–1623 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 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  Article  Google Scholar 

  24. Cavalieri, D., McGovern, P. E., Hartl, D. L., Mortimer, R. & Polsinelli, M. Evidence for S. cerevisiae fermentation in ancient wine. J. Mol. Evol. 57 S226–S232 (2003).

    CAS  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 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  Article  Google Scholar 

  28. Gallone, B. et al. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166, 1397–1410.e16 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  30. 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  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 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  Article  Google Scholar 

  34. 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  Article  CAS  Google Scholar 

  35. 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  Article  Google Scholar 

  36. Barbosa, R. et al. Multiple rounds of artificial selection promote microbe secondary domestication—the case of cachaça yeasts. Genome Biol. Evol. 10, 1939–1955 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. 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  Article  PubMed Central  Google Scholar 

  38. Eizaguirre, J. I. et al. Phylogeography of the wild lager-brewing ancestor (Saccharomyces eubayanus) in Patagonia. Environ. Microbiol. 20, 3732–3743 (2018).

    CAS  PubMed  Article  Google Scholar 

  39. Gibson, B. R., Storgårds, E., Krogerus, K. & Vidgren, V. Comparative physiology and fermentation performance of Saaz and Frohberg lager yeast strains and the parental species Saccharomyces eubayanus. Yeast 30, 255–266 (2013).

    CAS  PubMed  Article  Google Scholar 

  40. González, S. S., Barrio, E. & Querol, A. Molecular characterization of new natural hybrids of Saccharomyces cerevisiae and S. kudriavzevii in brewing. Appl. Environ. Microbiol. 74, 2314–2320 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  41. González, S. S., Barrio, E., Gafner, J. & Querol, A. Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Res. 6, 1221–1234 (2006).

    PubMed  Article  CAS  Google Scholar 

  42. Masneuf, I., Hansen, J., Groth, C., Piskur, J. & Dubourdieu, D. New hybrids between Saccharomyces sensu stricto yeast species found among wine and cider production strains. Appl. Environ. Microbiol. 64, 3887–3892 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Peris, D., Lopes, Ca, Belloch, C., Querol, A. & Barrio, E. Comparative genomics among Saccharomyces cerevisiae × Saccharomyces kudriavzevii natural hybrid strains isolated from wine and beer reveals different origins. BMC Genomics 13, 407 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. Peris, D., Pérez-Torrado, R., Hittinger, C. T., Barrio, E. & Querol, A. On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids. Yeast 35, 51–69 (2018).

    CAS  PubMed  Article  Google Scholar 

  45. Lopes, C. A., Barrio, E. & Querol, A. Natural hybrids of S. cerevisiae × S. kudriavzevii share alleles with European wild populations of Saccharomyces kudriavzevii. FEMS Yeast Res. 10, 412–421 (2010).

    CAS  PubMed  Article  Google Scholar 

  46. Peris, D. et al. The molecular characterization of new types of Saccharomyces cerevisiae × S. kudriavzevii hybrid yeasts unveils a high genetic diversity. Yeast 29, 81–91 (2012).

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  49. Steensels, J., Gallone, B., Voordeckers, K. & Verstrepen, K. J. Domestication of industrial microbes. Curr. Biol. 29, R381–R393 (2019).

    CAS  PubMed  Article  Google Scholar 

  50. Wendland, J. Lager yeast comes of age. Eukaryot. Cell 13, 1256–1265 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  51. G Gibson, B. & Liti, G. Saccharomyces pastorianus: genomic insights inspiring innovation for industry. Yeast 32, 17–27 (2015).

    Google Scholar 

  52. 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  Article  CAS  Google Scholar 

  53. Okuno, M. et al. Next-generation sequencing analysis of lager brewing yeast strains reveals the evolutionary history of interspecies hybridization. DNA Res. 23, dsv037 (2016).

    Article  CAS  Google Scholar 

  54. Dai, F. et al. Tibet is one of the centers of domestication of cultivated barley. Proc. Natl Acad. Sci. USA 109, 16969–16973 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  55. Meußdoerffer, F. & Zarnkow, M. Das Bier: Eine Geschichte von Hopfen und Malz (Beck, 2014).

  56. 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  Article  Google Scholar 

  57. Monerawela, C. & Bond, U. Recombination sites on hybrid chromosomes in Saccharomyces pastorianus share common sequence motifs and define a complex evolutionary relationship between group I and II lager yeasts. FEMS Yeast Res. 17, fox047 (2017).

    Google Scholar 

  58. Belloch, C. et al. Chimeric genomes of natural hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii. Appl. Environ. Microbiol. 75, 2534–2544 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. Hewitt, S. K., Donaldson, I. J., Lovell, S. C. & Delneri, D. Sequencing and characterisation of rearrangements in three S. pastorianus strains reveals the presence of chimeric genes and gives evidence of breakpoint reuse. PLoS ONE 9, e92203 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  60. 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  Article  Google Scholar 

  61. Peŕez-Través, L., Lopes, C. A., Querol, A. & Barrio, E. On the complexity of the Saccharomyces bayanus taxon: hybridization and potential hybrid speciation. PLoS ONE 9, e93729 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  62. Back, W. Colour Atlas and Handbook of Beverage Biology (Fachverlag Hans Carl, 2005).

  63. Krogerus, K., Magalhães, F., Vidgren, V. & Gibson, B. Novel brewing yeast hybrids: creation and application. Appl. Microbiol. Biotechnol. 101, 65–78 (2017).

    CAS  PubMed  Article  Google Scholar 

  64. van den Broek, M. et al. Chromosomal copy number variation in Saccharomyces pastorianus is evidence for extensive genome dynamics in industrial lager brewing strains. Appl. Environ. Microbiol. 81, 6253–6267 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  65. Monerawela, C. & Bond, U. The hybrid genomes of Saccharomyces pastorianus: a current perspective. Yeast 35, 39–50 (2017).

    PubMed  Article  CAS  Google Scholar 

  66. Fisher, K. J., Buskirk, S. W., Vignogna, R. C., Marad, D. A. & Lang, G. I. Adaptive genome duplication affects patterns of molecular evolution in Saccharomyces cerevisiae. PLoS Genet. 14, e1007396 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  68. Todd, R. T., Forche, A. & Selmecki, A. in The Fungal Kingdom (eds Heitman, J. et al.) Ch. 28 (ASM Press, 2017).

  69. Baker, E. C. P. et al. Mitochondrial DNA and temperature tolerance in lager yeasts. Sci. Adv. 5, eaav1869 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  70. Li, X. C., Peris, D., Hittinger, C. T., Sia, E. A. & Fay, J. C. Mitochondria-encoded genes contribute to evolution of heat and cold tolerance in yeast. Sci. Adv. 5, eaav1848 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  71. De Roos, J. & De Vuyst, L. Microbial acidification, alcoholization, and aroma production during spontaneous lambic beer production. J. Sci. Food Agric. 99, 25–38 (2019).

    PubMed  Article  CAS  Google Scholar 

  72. Steensels, J. & Verstrepen, K. J. Taming wild yeast: potential of conventional and nonconventional yeasts in industrial fermentations. Annu. Rev. Microbiol. 68, 61–80 (2014).

    CAS  PubMed  Article  Google Scholar 

  73. Dzialo, M. C., Park, R., Steensels, J., Lievens, B. & Verstrepen, K. J. Physiology, ecology and industrial applications of aroma formation in yeast. FEMS Microbiol. Rev. 41, S95–S128 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  74. Mukai, N., Masaki, K., Fujii, T., Kawamukai, M. & Iefuji, H. PAD1 and FDC1 are essential for the decarboxylation of phenylacrylic acids in Saccharomyces cerevisiae. J. Biosci. Bioeng. 109, 564–569 (2010).

    CAS  PubMed  Article  Google Scholar 

  75. Mukai, N., Masaki, K., Fujii, T. & Iefuji, H. Single nucleotide polymorphisms of PAD1 and FDC1 show a positive relationship with ferulic acid decarboxylation ability among industrial yeasts used in alcoholic beverage production. J. Biosci. Bioeng. 118, 50–55 (2014).

    CAS  PubMed  Article  Google Scholar 

  76. Pasteur, L. Etudes sur la bière, ses maladies, causes qui les provoquent, procédé pour la rendre inaltérable, avec une théorie nouvelle de la fermentation (Gauthier-Villars, 1876).

  77. Teich, M. Bier, Wissenschaft und Wirtschaft in Deutschland 1800–1914. Ein Beitrag zur Deutschen Industrialisierungsgeschichte (Böhlau, 2000).

  78. Hansen, E. Recherches sur la physiologie et la morphologie des ferments alcooliques V. methodes pour obtenir des cultures pures de Saccharomyces et de mikroorganismes analogues. C. R. Trav. Lab. Carlsberg 2, 92–105 (1883).

    Google Scholar 

  79. 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  Article  Google Scholar 

  80. Peris, D. et al. Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. Biotechnol. Biofuels 10, 78 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  81. 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 1, 11–25 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  82. Liti, G. et al. High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome. BMC Genomics 14, 69 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  83. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. Pryszcz, L. P. & Gabaldón, T. Redundans: an assembly pipeline for highly heterozygous genomes. Nucleic Acids Res. 44, e113 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  87. Kolmogorov, M., Raney, B., Paten, B. & Pham, S. Ragout—a reference-assisted assembly tool for bacterial genomes. Bioinformatics 30, i302–i309 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  88. Wapinski, I., Pfeffer, A., Friedman, N. & Regev, A. Natural history and evolutionary principles of gene duplication in fungi. Nature 449, 54–61 (2007).

    CAS  PubMed  Article  Google Scholar 

  89. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    CAS  Article  PubMed  Google Scholar 

  90. Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  91. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  92. Kück, P. & Meusemann, K. FASconCAT: convenient handling of data matrices. Mol. Phylogenet. Evol. 56, 1115–1118 (2010).

    PubMed  Article  CAS  Google Scholar 

  93. Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  94. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. Kozlov, A. M., Aberer, A. J. & Stamatakis, A. ExaML version 3: a tool for phylogenomic analyses on supercomputers. Bioinformatics 31, 2577–2579 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  96. Pattengale, N. D., Alipour, M., Bininda-Emonds, O. R. P., Moret, B. M. E. & Stamatakis, A. How many bootstrap replicates are necessary? J. Comput. Biol. 17, 337–354 (2010).

    CAS  PubMed  Article  Google Scholar 

  97. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2011).

  98. Yu, G., Smith, D. K., Zhu, H., Guan, Y. & Lam, T. T. Y. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 8, 28–36 (2017).

    Article  Google Scholar 

  99. Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  100. Raj, A., Stephens, M. & Pritchard, J. K. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197, 573–589 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  101. Ayres, D. L. et al. BEAGLE: an application programming interface and high-performance computing library for statistical phylogenetics. Syst. Biol. 61, 170–173 (2012).

    PubMed  Article  Google Scholar 

  102. Drummond, A. J., Ho, S. Y., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  103. Drummond, A. J. & Suchard, M. A. Bayesian random local clocks, or one rate to rule them all. BMC Biol. 8, 114 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  104. Worobey, M., Han, G.-Z. & Rambaut, A. A synchronized global sweep of the internal genes of modern avian influenza virus. Nature 508, 254–257 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  105. Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst. Biol. 67, 901–904 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. Baele, G., Lemey, P. & Suchard, M. A. Genealogical working distributions for Bayesian model testing with phylogenetic uncertainty. Syst. Biol. 65, 250–264 (2016).

    PubMed  Article  Google Scholar 

  107. Angiuoli, S. V. & Salzberg, S. L. Mugsy: fast multiple alignment of closely related whole genomes. Bioinformatics 27, 334–342 (2011).

    CAS  PubMed  Article  Google Scholar 

  108. Venables, W. N. & Ripley, B. D. Modern applied statistics with S. Technometrics 45, 111–111 (2003).

    Google Scholar 

  109. Warnes, G. R. et al. gplots: Various R programming tools for plotting data. R version 3.0.0 http://CRAN.R-project.org/package=gplots (2016).

  110. Murtagh, F. & Legendre, P. Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? J. Classif. 31, 274–295 (2014).

    Article  Google Scholar 

  111. Calahan, D., Dunham, M., Desevo, C. & Koshland, D. E. Genetic analysis of desiccation tolerance in Saccharomyces cerevisiae. Genetics 189, 507–519 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  112. Muir, A., Harrison, E. & Wheals, A. A multiplex set of species-specific primers for rapid identification of members of the genus Saccharomyces. FEMS Yeast Res. 11, 552–563 (2011).

    CAS  PubMed  Article  Google Scholar 

  113. Pengelly, R. J. & Wheals, A. E. Rapid identification of Saccharomyces eubayanus and its hybrids. FEMS Yeast Res. 13, 156–161 (2013).

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

We thank all K.J.V. and S.Maere laboratory members for their help and suggestions. We thank AB InBev, White Labs Inc. and R. S. Wagner (Central Washington University) for isolating and sharing various hybrid yeasts from the beer environment. We thank M. Zarnkow (Research Center Weihenstephan for Brewing and Food Quality) for sharing historical facts on lager brewing. B.G. acknowledges funding from the VIB International PhD Program in Life Sciences. J.S. acknowledges funding from Research Foundation-Flanders (FWO) (grant no. 12W3918N). Research in the laboratory of K.J.V. is supported by KU Leuven Program Financing, European Research Council Consolidator Grant (no. CoG682009), Human Frontier Science program grant (no. RGP0050/2013), VIB, FWO (grant no. G.0C59.14N) and Vlaams Agentschap Innoveren en Ondernemen (grant no. HBC.2018.0097). Research in the laboratory of S.Maere is supported by VIB, Ghent University and FWO (grant no. G018915N).

Author information

Authors and Affiliations

Authors

Contributions

B.G., J.S., S.Maere and K.J.V. conceived the project. B.G. and J.S. performed the data collection. B.G., J.S. and G.B. carried out the formal analysis. B.G., J.S., S.Mertens, J.L.G., R.W., F.A.T., F.B., V.S., B.H.-M. and G.B. carried out the investigations. B.G. and J.S. performed data visualization. M.H., F.M., P.M., B.S., L.D., T.P., C.W. and K.J.V. provided resources. B.G., J.S., M.C.D., S.Maere and K.J.V. wrote the paper. S.Maere and K.J.V. supervised the project.

Corresponding authors

Correspondence to Steven Maere or Kevin J. Verstrepen.

Ethics declarations

Competing interests

AB InBev partially funded the experiments performed in this study. AB InBev had no role in conceptualization, design, data collection, analysis, decision to publish or preparation of the manuscript. B.S., P.M. and L.D. are employed by AB InBev.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–5, Tables 1–3, Note 1 and Dataset 1.

Reporting Summary

Supplementary Table 1

List of strains included in this study.

Supplementary Table 2

Chimeric breakpoints identified in Saccharomyces interspecific hybrids.

Supplementary Table 3

Phenotypic variation of Saccharomyces interspecific hybrids and Saccharomyces pure species.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gallone, B., Steensels, J., Mertens, S. et al. Interspecific hybridization facilitates niche adaptation in beer yeast. Nat Ecol Evol 3, 1562–1575 (2019). https://doi.org/10.1038/s41559-019-0997-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-0997-9

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing