Fig 1. Macroevolutionary patterns in Saccharomycotina. A) Crabtree positive (green) and negative (red) yeasts associated with fermentative capacity, indicated here as ethanol yield (grams of ethanol production per gram of glucose consumed, horizontal bars). Two major genomic rearrangements that affected the lineage are denoted with the arrows, the purple diamond indicate the loss of the URA1 gene inEremothecium clade and the whole genomic duplication is indicated by the blue branches. B) A measure of phylogenetic signal for the Crabtree effect as a categorical trait. The arrow denotes the minimum number of transitions needed to explain the character state, which is significantly less than a randomized distribution (1000 randomizations; p<0.0001). LCP+ = Long-Term Crabtree positive yeast. LCP- = Long-Term Crabtree negative yeast.
Fig 2. A heatmap of trait values as a descriptive statistic for trait distribution (see Table A1 for the complete dataset).
Fig 3. Phenograms (i.e., plots combining trait values and phylogenetic relationship across time) showing the phenotypic differentiation between WGD- (black line) and WGD+ (blue line) species, in a) dry matter growth rate, b) rate of glycerol production, c) respiratory quotient and d) ethanol yield. The time scale corresponds to the original calibration, ordered backwards, where zero represents the origin of the clade.
Fig 4. Location of adaptive shifts, according to the OU-lasso method and assuming a maximum of k=3 shifts, for each variable: a) growth rate, b) glycerol production, c) respiratory quotient and d) ethanol yield. For growth rate, k=0 and k=3 were statistically indistinguishable (see Table 1).
References
Albertyn, J., Hohmann, S., Thevelein, J. M. & Prior, B. A. 1994. GPD1, WHICH ENCODES GLYCEROL-3-PHOSPHATE DEHYDROGENASE, IS ESSENTIAL FOR GROWTH UNDER OSMOTIC-STRESS IN SACCHAROMYCES-CEREVISIAE, AND ITS EXPRESSION IS REGULATED BY THE HIGH-OSMOLARITY GLYCEROL RESPONSE PATHWAY. Molecular and Cellular Biology 14 : 4135-4144.
Aslankoohi, E., Rezaei, M. N., Vervoort, Y., Courtin, C. M. & Verstrepen, K. J. 2015. Glycerol Production by Fermenting Yeast Cells Is Essential for Optimal Bread Dough Fermentation. Plos One10 : 13.
Blomberg, S. P., Garland, T. & Ives, A. R. 2003. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57 : 717-745.
Chen, H., Xu, L. & Gu, Z. L. 2008. Regulation Dynamics of WGD Genes during Yeast Metabolic Oscillation. Molecular Biology and Evolution 25 : 2513-2516.
Conant, G. C. & Wolfe, K. H. 2007. Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Molecular Systems Biology 3 : 12.
Cressler, C. E., Butler, M. A. & King, A. A. 2015. Detecting Adaptive Evolution in Phylogenetic Comparative Analysis Using the Ornstein-Uhlenbeck Model. Systematic Biology 64 : 953-968.
Dashko, S., Zhou, N., Compagno, C. & Piskur, J. 2014. Why, when, and how did yeast evolve alcoholic fermentation? Fems Yeast Research14 : 826-832.
Dong, D., Yuan, Z. N. & Zhang, Z. L. 2011. Evidences for increased expression variation of duplicate genes in budding yeast: from cis- to trans-regulation effects. Nucleic Acids Research 39 : 837-847.
Dujon, B. 2010. Yeast evolutionary genomics. Nature Reviews Genetics 11 : 512-524.
Ernst, A., Becker, S., Wollenzien, U. I. A. & Postius, C. 2003. Ecosystem-dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis. Microbiology-Sgm149 : 217-228.
Felsenstein, J. 1973. Maximum likelihood estimation of evolutionary trees from continuous characters. American Journal of Human Genetics 25 : 471-492.
Felsenstein, J. 1985. Phylogenies and the comparative method. The American Naturalist 125 : 1-15.
Fisher, K. J., Buskirk, S. W., Vignogna, R. C., Marad, D. A. & Lang, G. I. 2018. Adaptive genome duplication affects patterns of molecular evolution in Saccharomyces cerevisiae. Plos Genetics 14 : 22.
Gallone, B., Steensels, J., Prahl, T., Soriaga, L., Saels, V., Herrera-Malaver, B., Merlevede, A., Roncoroni, M., Voordeckers, K., Miraglia, L., Teiling, C., Steffy, B., Taylor, M., Schwartz, A., Richardson, T., White, C., Baele, G., Maere, S. & Verstrepen, K. J. 2016. Domestication and Divergence of Saccharomyces cerevisiae Beer Yeasts. Cell 166 : 1397-+.
Goddard, M. & Grieg, D. 2015. Saccharomyces cerevisiae: a nomadic yeast with no niche? Fems Yeast Research 15 : in press.
Gubry-Rangin, C., Kratsch, C., Williams, T. A., McHardy, A. C., Embley, T. M., Prosser, J. I. & Macqueen, D. J. 2015. Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota. Proceedings of the National Academy of Sciences of the United States of America 112 : 9370-9375.
Gutierrez, A., Sancho, M., Beltran, G., Guillamon, J. M. & Warringer, J. 2016. Replenishment and mobilization of intracellular nitrogen pools decouples wine yeast nitrogen uptake from growth. Applied Microbiology and Biotechnology 100 : 3255-3265.
Hagman, A. & Piskur, J. 2015. A Study on the Fundamental Mechanism and the Evolutionary Driving Forces behind Aerobic Fermentation in Yeast.Plos One 10 : 24.
Hagman, A., Sall, T., Compagno, C. & Piskur, J. 2013. Yeast ”Make-Accumulate-Consume” Life Strategy Evolved as a Multi-Step Process That Predates the Whole Genome Duplication. Plos One 8 : 12.
Hagman, A., Sall, T. & Piskur, J. 2014. Analysis of the yeast short-term Crabtree effect and its origin. Febs Journal281 : 4805-4814.
Hansen, T. F. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51 : 1341-1351.
James, T. Y., Kauff, F., Schoch, C. L., Matheny, P. B., Hofstetter, V., Cox, C. J., Celio, G., Gueidan, C., Fraker, E., Miadlikowska, J., Lumbsch, H. T., Rauhut, A., Reeb, V., Arnold, A. E., Amtoft, A., Stajich, J. E., Hosaka, K., Sung, G. H., Johnson, D., O’Rourke, B., Crockett, M., Binder, M., Curtis, J. M., Slot, J. C., Wang, Z., Wilson, A. W., Schussler, A., Longcore, J. E., O’Donnell, K., Mozley-Standridge, S., Porter, D., Letcher, P. M., Powell, M. J., Taylor, J. W., White, M. M., Griffith, G. W., Davies, D. R., Humber, R. A., Morton, J. B., Sugiyama, J., Rossman, A. Y., Rogers, J. D., Pfister, D. H., Hewitt, D., Hansen, K., Hambleton, S., Shoemaker, R. A., Kohlmeyer, J., Volkmann-Kohlmeyer, B., Spotts, R. A., Serdani, M., Crous, P. W., Hughes, K. W., Matsuura, K., Langer, E., Langer, G., Untereiner, W. A., Lucking, R., Budel, B., Geiser, D. M., Aptroot, A., Diederich, P., Schmitt, I., Schultz, M., Yahr, R., Hibbett, D. S., Lutzoni, F., McLaughlin, D. J., Spatafora, J. W. & Vilgalys, R. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature443 : 818-822.
Kawecki, T. J. & Ebert, D. 2004. Conceptual issues in local adaptation.Ecology Letters 7 : 1225-1241.
Khabbazian, M., Kriebel, R., Rohe, K. & Ane, C. 2016. Fast and accurate detection of evolutionary shifts in Ornstein-Uhlenbeck models.Methods in Ecology and Evolution 7 : 811-824.
Kurtzman, C. P., Fell, J. W. & Boekhout, T. 2011. The Yeasts: a taxonomic study . Elsevier, London.
Kurtzman, C. P. & Robnett, C. J. 2003. Phylogenetic relationships among yeasts of the ’Saccharomyces complex’ determined from multigene sequence analyses. Fems Yeast Research 3 : 417-432.
Libkind, D., Hittinger, C. T., Valerio, E., Goncalves, C., Dover, J., Johnston, M., Goncalves, P. & Sampaio, J. P. 2011. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proceedings of the National Academy of Sciences of the United States of America 108 : 14539-14544.
Lin, Z. G. & Li, W. H. 2011. Expansion of Hexose Transporter Genes Was Associated with the Evolution of Aerobic Fermentation in Yeasts.Molecular Biology and Evolution 28 : 131-142.
Linhart, Y. B. & Grant, M. C. 1996. Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 27 : 237-277.
Luyten, K., Riou, C. & Blondin, B. 2002. The hexose transporters of Saccharomyces cerevisiae play different roles during enological fermentation. Yeast 19 : 713-726.
Maddison, D. R. & Maddison, W. P. 2000. MacClade 4 . Sinauer.
Marcet-Houben, M. & Gabaldon, T. 2015. Beyond the Whole-Genome Duplication: Phylogenetic Evidence for an Ancient Interspecies Hybridization in the Baker’s Yeast Lineage. Plos Biology13 : 26.
Marcet-Houben, M., Marceddu, G. & Gabaldon, T. 2009. Phylogenomics of the oxidative phosphorylation in fungi reveals extensive gene duplication followed by functional divergence. Bmc Evolutionary Biology 9 : 12.
Nakov, T., Theriot, E. C. & Alverson, A. J. 2014. Using phylogeny to model cell size evolution in marine and freshwater diatoms.Limnology and Oceanography 59 : 79-86.
Nurcholis, M., Lertwattanasakul, N., Rodrussamee, N., Kosaka, T., Murata, M. & Yamada, M. Integration of comprehensive data and biotechnological tools for industrial applications of Kluyveromyces marxianus. Applied Microbiology and Biotechnology : 14.
Paleo-Lopez, R., Quintero-Galvis, J. F., Solano-Iguaran, J. J., Sanchez-Salazar, A. M., Gaitan-Espitia, J. D. & Nespolo, R. F. 2016. A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts. Ecology and Evolution 6 : 3851-3861.
Paradis, E. 2012. Analysis of phylogenetics and evolution with R. Second Edition . Springer.
Piskur, J. 2001. Origin of the duplicated regions in the yeast genomes.Trends in Genetics 17 : 302-303.
Piskur, J., Rozpedowska, E., Polakova, S., Merico, A. & Compagno, C. 2006. How did Saccharomyces evolve to become a good brewer? Trends in Genetics 22 : 183-186.
Querol, A., Fernandez-Espinar, M. T., del Olmo, M. & Barrio, E. 2003. Adaptive evolution of wine yeast. International Journal of Food Microbiology 86 : 3-10.
Ravot, G., Ollivier, B., Fardeau, M. L., Patel, B. K. C., Andrews, K. T., Magot, M. & Garcia, J. L. 1996. L-Alanine production from glucose fermentation by hyperthermophilic members of the domains Bacteria and Archaea: A remnant of an ancestral metabolism? Applied and Environmental Microbiology 62 : 2657-2659.
Salichos, L. & Rokas, A. 2013. Inferring ancient divergences requires genes with strong phylogenetic signals. Nature 497 : 327-+.
Scannell, D. R., Butler, G. & Wolfe, K. H. 2007. Yeast genome evolution - the origin of the species. Yeast 24 : 929-942.
Shen, X. X., Opulente, D. A., Kominek, J., Zhou, X., Steenwyk, J. L., Buh, K. V., Haase, M. A. B., Wisecaver, J. H., Wang, M., Doering, D. T., Boudouris, J. T., Schneider, R. M., Langdon, Q. K., Ohkuma, M., Endoh, R., Takashima, M., Manabe, R., Cadez, N., Libkind, D., Rosa, C. A., DeVirgilio, J., Hulfachor, A. B., Groenewald, M., Kurtzman, C. P., Hittinger, C. T. & Rokas, A. 2018. Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum. Cell 175 : 1533-+.
Starmer, W. T., Schmedicke, R. A. & Lachance, M. A. 2003. The origin of the cactus-yeast community. Fems Yeast Research 3 : 441-448.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.Molecular Biology and Evolution 30 : 2725-2729.
Thompson, D. A., Roy, S., Chan, M., Styczynski, M. P., Pfiffner, J., French, C., Socha, A., Thielke, A., Napolitano, S., Muller, P., Kellis, M., Konieczka, J. H., Wapinski, I. & Regev, A. 2013. Evolutionary principles of modular gene regulation in yeasts. Elife2 : 37.
Thomson, J. M., Gaucher, E. A., Burgan, M. F., De Kee, D. W., Li, T., Aris, J. P. & Benner, S. A. 2005. Resurrecting ancestral alcohol dehydrogenases from yeast. Nature Genetics 37 : 630-635.
Tibshirani, R. 1996. Regression shrinkage and selection via the Lasso.Journal of the Royal Statistical Society Series B-Methodological58 : 267-288.
Voordeckers, K., Kominek, J., Das, A., Espinosa-Cantu, A., De Maeyer, D., Arslan, A., Van Pee, M., van der Zande, E., Meert, W., Yang, Y. D., Zhu, B., Marchal, K., DeLuna, A., Van Noort, V., Jelier, R. & Verstrepen, K. J. 2015. Adaptation to High Ethanol Reveals Complex Evolutionary Pathways. Plos Genetics 11 : 31.
Wagenmakers, E. J. & Farrell, S. 2004. AIC model selection using Akaike weights. Psychonomic Bulletin & Review 11 : 192-196.
Williams, K. M., Liu, P. & Fay, J. C. 2015. Evolution of ecological dominance of yeast species in high-sugar environments. Evolution69 : 2079-2093.
Wolfe, K. H. & Shields, D. C. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387 : 708-713.
Zhang, J. Z. 2003. Evolution by gene duplication: an update.Trends in Ecology & Evolution 18 : 292-298.
Zhou, N., Swamy, K. B. S., Leu, J. Y., McDonald, M. J., Galafassi, S., Compagno, C. & Piskur, J. 2017. Coevolution with bacteria drives the evolution of aerobic fermentation in Lachancea kluyveri. Plos One12 : 19.