Performance, genomic rearrangements, and signatures of adaptive evolution: lessons from fermentative yeasts
Open accessAbstract
and ethanol (=fermentation), even in the presence of oxygen, is known as the Crabtree effect. This phenomenon represents an important adaptation as it allowed the utilization of the ecological niche given by modern fruits, an abundant source of food that emerged in the terrestrial environment in the Cretaceous. However, identifying the evolutionary events that triggered fermentative capacity in Crabtree-positive species is challenging, as microorganisms do not leave fossil evidence. Thus, key innovations should be inferred based only on traits measured under culture conditions. Here, we reanalyzed data from a common garden experiment where several proxies of fermentative capacity were recorded in Crabtree-positive and Crabtree-negative species, representing yeast phylogenetic diversity. In particular, we applied the "lasso-OU" algorithm which detects points of adaptive shifts, using traits that are proxies of fermentative performance. We tested whether multiple events or a single event explains the actual fermentative capacity of yeasts. According to the lasso-OU procedure, evolutionary changes in the three proxies of fermentative capacity that we considered (i.e., glycerol production, ethanol yield, and respiratory quotient) are consistent with a single evolutionary episode (a whole-genomic duplication, WGD), instead of a series of small genomic rearrangements. Thus, the WGD appears as the key event behind the diversification of fermentative yeasts, which by increasing gene dosage, and maximized their capacity of energy extraction for exploiting the new ecological niche provided by single sugars.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Many aspects of S. cerevisiae energy metabolism are relatively recent evolutionary adaptations to the predominantly fermentative lifestyle and are not typical of other yeast lineages.
“many aspects of its energy metabolism are relatively recent evolutionary adaptations to the predominantly fermentative lifestyle and are not typical of other yeast lineages”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Nespolo et al. 2020
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Regression shrinkage and selection via the lasso
Tibshirani, R. (1996) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1996.tb02080.x · Cited by 51,482 · see citing works
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013) · Molecular biology and evolution · doi:10.1093/molbev/mst197 · Cited by 41,174 · see citing works
Phylogenies and the Comparative Method
Felsenstein, J. (1985) · The American Naturalist · doi:10.1086/284325 · Cited by 9,793 · see citing works
MacClade 4.0: analysis of phylogeny and character evolution
(2001) · Choice Reviews Online · doi:10.5860/choice.39-2183 · Cited by 5,533 · see citing works
TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE
Blomberg, S. P., Garland, T., & Ives, A. R. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb00285.x · Cited by 4,678 · see citing works
Conceptual issues in local adaptation
Kawecki, T. J., & Ebert, D. (2004) · Ecology Letters · doi:10.1111/j.1461-0248.2004.00684.x · Cited by 3,746 · see citing works
Kurtzman, C. P., & Lodder, J. (1972) · Mycologia · doi:10.2307/3758036 · Cited by 3,441 · see citing works
AIC model selection using Akaike weights
Wagenmakers, E.-J., & Farrell, S. (2004) · Psychonomic Bulletin & Review · doi:10.3758/bf03206482 · Cited by 2,684 · see citing works
Evolution by gene duplication: An update
Zhang, J. (2003) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(03)00033-8 · Cited by 2,201 · see citing works
Reconstructing the early evolution of Fungi using a six-gene phylogeny
James, T. Y., Kauff, F., Schoch, C. L., Matheny, P. B., Hofstetter, V., Cox, C. J., Celio, G. J., Gueidan, C., Fraker, E., Miądlikowska, J., et al. (2006) · Nature · doi:10.1038/nature05110 · Cited by 1,807 · see citing works
Molecular evidence for an ancient duplication of the entire yeast genome
Wolfe, K. H., & Shields, D. C. (1997) · Nature · doi:10.1038/42711 · Cited by 1,785 · see citing works
Stabilizing selection and the comparative analysis of adaptation
Hansen, T. F. (1997) · Evolution · doi:10.1111/j.1558-5646.1997.tb01457.x · Cited by 1,361 · see citing works
EVOLUTIONARY SIGNIFICANCE OF LOCAL GENETIC DIFFERENTIATION IN PLANTS
Linhart, Y. B., & Grant, M. C. (1996) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.27.1.237 · Cited by 1,328 · see citing works
Albertyn, J., Hohmann, S., Thevelein, J. M., & Prior, B. A. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.6.4135-4144.1994 · Cited by 731 · see citing works
Analysis of Phylogenetics and Evolution with R
Paradis, E. (2011) · Springer eBooks · doi:10.1007/978-1-4614-1743-9 · Cited by 713 · see citing works
Maximum-likelihood estimation of evolutionary trees from continuous characters.
(1973) · Europe PMC (PubMed Central) · Cited by 700 · see citing works
Domestication and Divergence of Saccharomyces cerevisiae Beer Yeasts
Gallone, B., Steensels, J., Prahl, T., Soriaga, L., Saels, V., Herrera-Malaver, B., Merlevede, A., Roncoroni, M., Voordeckers, K., Miraglia, L., et al. (2016) · Cell · doi:10.1016/j.cell.2016.08.020 · Cited by 679 · see citing works
Kurtzman, C. P., & Robnett, C. J. (2003) · FEMS Yeast Research · doi:10.1016/s1567-1356(03)00012-6 · Cited by 652 · see citing works
Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast
Libkind, D., Hittinger, C. T., Valério, E., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105430108 · Cited by 643 · see citing works
Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
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., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.023 · Cited by 619 · see citing works
Inferring ancient divergences requires genes with strong phylogenetic signals
Salichos, L., & Rokas, A. (2013) · Nature · doi:10.1038/nature12130 · Cited by 616 · see citing works
Huey, R. B., Garland, T., & Turelli, M. (2019) · The American Naturalist · doi:10.1086/703055 · Cited by 598 · see citing works
How did Saccharomyces evolve to become a good brewer?
Piškur, J., Rozpędowska, E., Poláková, S., Merico, A., & Compagno, C. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.02.002 · Cited by 514 · see citing works
Resurrecting ancestral alcohol dehydrogenases from yeast
Thomson, J. M., Gaucher, E. A., Burgan, M. F., De Kee, D. W., Li, T., Aris, J. P., & Benner, S. A. (2005) · Nature Genetics · doi:10.1038/ng1553 · Cited by 341 · see citing works
Marcet‐Houben, M., & Gabaldón, T. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002220 · Cited by 322 · see citing works
Dujon, B. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2811 · Cited by 316 · see citing works
Why, when, and how did yeast evolve alcoholic fermentation?
Dashko, S., Zhou, N., Compagno, C., & Piškur, J. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12161 · Cited by 313 · see citing works
Fast and accurate detection of evolutionary shifts in Ornstein–Uhlenbeck models
Khabbazian, M., Kriebel, R., Rohe, K., & Ané, C. (2016) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.12534 · Cited by 245 · see citing works
Increased glycolytic flux as an outcome of whole-genome duplication in yeast
Conant, G. C., & Wolfe, K. H. (2007) · Molecular Systems Biology · doi:10.1038/msb4100170 · Cited by 222 · see citing works
Hagman, A., Säll, T., Compagno, C., & Piskur, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068734 · Cited by 219 · see citing works
Adaptive evolution of wine yeast
Querol, A. (2003) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(03)00244-7 · Cited by 190 · see citing works
Adaptation to High Ethanol Reveals Complex Evolutionary Pathways
Voordeckers, K., Kominek, J., Das, A. J., Espinosa‐Cantú, A., Maeyer, D. D., Arslan, A., Pee, M. V., van der Zande, E., Meert, W., Yang, Y., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005635 · Cited by 167 · see citing works
Ernst, A. (2003) · Microbiology · doi:10.1099/mic.0.25475-0 · Cited by 161 · see citing works
Saccharomyces cerevisiae: a nomadic yeast with no niche?
Goddard, M. R., & Greig, D. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov009 · Cited by 158 · see citing works
Yeast genome evolution—the origin of the species
Scannell, D. R., Butler, G., & Wolfe, K. H. (2007) · Yeast · doi:10.1002/yea.1515 · Cited by 134 · see citing works
Hagman, A., & Piškur, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116942 · Cited by 130 · see citing works
Detecting Adaptive Evolution in Phylogenetic Comparative Analysis Using the Ornstein–Uhlenbeck Model
Cressler, C. E., Butler, M. A., & King, A. A. (2015) · Systematic Biology · doi:10.1093/sysbio/syv043 · Cited by 128 · see citing works
Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota
Gubry‐Rangin, C., Kratsch, C., Williams, T. A., McHardy, A. C., Embley, T. M., Prosser, J. I., & Macqueen, D. J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419329112 · Cited by 113 · see citing works
Glycerol Production by Fermenting Yeast Cells Is Essential for Optimal Bread Dough Fermentation
Aslankoohi, E., Rezaei, M. N., Vervoort, Y., Courtin, C. M., & Verstrepen, K. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119364 · Cited by 108 · see citing works
Analysis of the yeast short‐term Crabtree effect and its origin
Hagman, A., Säll, T., & Piškur, J. (2014) · FEBS Journal · doi:10.1111/febs.13019 · Cited by 97 · see citing works
Lin, Z., & Li, W. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq184 · Cited by 89 · see citing works
Adaptive genome duplication affects patterns of molecular evolution in Saccharomyces cerevisiae
Fisher, K. J., Buskirk, S. W., Vignogna, R. C., Marad, D. A., & Lang, G. I. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007396 · Cited by 79 · see citing works
Evolutionary principles of modular gene regulation in yeasts
Thompson, D. A., Roy, S., Chan, M., Styczynsky, M. P., Pfiffner, J., French, C., Socha, A., Thielke, A., Napolitano, S., Muller, P., et al. (2013) · eLife · doi:10.7554/elife.00603 · Cited by 78 · see citing works
Marcet-Houben, M., Marceddu, G., & Gabaldón, T. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-295 · Cited by 75 · see citing works
Luyten, K., Riou, C., & Blondin, B. (2002) · Yeast · doi:10.1002/yea.869 · Cited by 73 · see citing works
Ravot, G., Ollivier, B., Fardeau, M., et al. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.7.2657-2659.1996 · Cited by 71 · see citing works
Evolution of ecological dominance of yeast species in high-sugar environments
Williams, K. M., Liu, P., & Fay, J. C. (2015) · Evolution · doi:10.1111/evo.12707 · Cited by 59 · see citing works
Origin of the duplicated regions in the yeast genomes
Piškur, J. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02308-3 · Cited by 53 · see citing works
Shimizu, J. F., Pereira, C. M., Bittar, C., Batista, M. N., Campos, G. R. F., da Silva, S., Cintra, A. C. O., Zothner, C., Harris, M., Sampaio, S. V., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0187857 · Cited by 50 · see citing works
Nurcholis, M., Lertwattanasakul, N., Rodrussamee, N., Kosaka, T., Murata, M., & Yamada, M. C. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10224-3 · Cited by 46 · see citing works
The origin of the cactus-yeast community
Starmer, W. T., SCHMEDICKE, R., & Lachance, M. (2003) · FEMS Yeast Research · doi:10.1016/s1567-1356(03)00056-4 · Cited by 44 · see citing works
Coevolution with bacteria drives the evolution of aerobic fermentation in Lachancea kluyveri
Zhou, N., Swamy, K. B. S., Leu, J., McDonald, M. J., Galafassi, S., Compagno, C., & Piškur, J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173318 · Cited by 31 · see citing works
Dong, D., Yuan, Z., & Zhang, Z. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq874 · Cited by 23 · see citing works
Using phylogeny to model cell size evolution in marine and freshwater diatoms
Nakov, T., Theriot, E. C., & Alverson, A. J. (2013) · Limnology and Oceanography · doi:10.4319/lo.2014.59.1.0079 · Cited by 22 · see citing works
Gutiérrez, A., Sancho, M., Beltran, G., et al. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-7273-y · Cited by 18 · see citing works
A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts
Paleo‐López, R., Quintero‐Galvis, J. F., Solano‐Iguaran, J. J., Sánchez-Salazar, Á. M., Gaitán‐Espitía, J. D., & Nespolo, R. F. (2016) · Ecology and Evolution · doi:10.1002/ece3.2097 · Cited by 18 · see citing works
Self-citationRegulation Dynamics of WGD Genes during Yeast Metabolic Oscillation
Chen, H., Xu, L., & Gu, Z. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn212 · Cited by 13 · see citing works
Correction: Evolutionary principles of modular gene regulation in yeasts
Thompson, D. A., Roy, S., Chan, M. M., Styczynski, M. P., Pfiffner, J., French, C. E., Socha, A. L., Thielke, A. L., Napolitano, S., Muller, P. A., et al. (2013) · eLife · doi:10.7554/elife.01114 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Łabędzka-Dmoch, K., Bui, T. H. D., Piątkowski, J., Dilling, M., Jagiełło, P., Kabza, W., & Golik, P. (2026) · Molecular Biology and Evolution · doi:10.1093/molbev/msag005 · Cited by 1 · see citing works
- Authors
- Nespolo, R. F., Solano‐Iguaran, J. J., Paleo‐López, R., Quintero‐Galvis, J. F., Cubillos, F. A., & Bozinovic, F.
- Affiliations
- Pontificia Universidad Católica de Chile (CL)
- Austral University of Chile (CL)
- Universidad de Santiago de Chile (CL)
- Corresponding author
- Nespolo, Roberto F.
- ORCID
- Venue
- Ecology and Evolution
- Publisher
- Wiley
- Published
- 2020-06
- Volume
- 10
- Issue
- 12
- Pages
- 5240-5250
- ISSN
- 2045-7758 (ISSN-L)
- PMC
- PMC7319171
- OpenAlex
- W3033311253
- Cited by
- 9
- References
- 58
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2022: 1 · 2021: 1 · 2020: 2
- FWCI
- 0.32
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Ecology and Evolution (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Fondo Nacional de Desarrollo Científico y Tecnológico (1180917)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- Crabtree effect, fermentative yeasts, whole-genome duplication, adaptive evolution, genome rearrangement, glycerol production, ethanol yield, respiratory quotient, common garden experiment, key innovations, gene dosage, Saccharomyces
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
