The dynamics of adaptation to stress from standing genetic variation and de novo mutations
Open accessPublished version of a preprint
Abstract
Adaptation from standing genetic variation is an important process underlying evolution in natural populations, but we rarely get the opportunity to observe the dynamics of fitness and genomic changes in real time. Here, we used experimental evolution and Pool-Seq to track the phenotypic and genomic changes of genetically diverse asexual populations of the yeast Saccharomyces cerevisiae in four environments with different fitness costs. We found that populations rapidly and in parallel increased in fitness in stressful environments. In contrast, allele frequencies showed a range of trajectories, with some populations fixing all their ancestral variation in <30 generations and others maintaining diversity across hundreds of generations. We detected parallelism at the genomic level (involving genes, pathways, and aneuploidies) within and between environments, with idiosyncratic changes recurring in the environments with higher stress. In particular, we observed a tendency of becoming haploid-like in one environment, whereas the populations of another environment showed low overall parallelism driven by standing genetic variation despite high selective pressure. This work highlights the interplay between standing genetic variation and the influx of de novo mutations in populations adapting to a range of selective pressures with different underlying trait architectures, advancing our understanding of the constraints and drivers of adaptation.
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?
This expected progression is seen in experimental yeast populations exposed to different stress-inducing substances; some populations rapidly depleted pre-existing variation in the first 30 generations, increasing their reliance on new mutations in later generations.
“This expected progression is seen in experimental yeast populations exposed to different stress-inducing substances; some populations (but not others) rapidly depleted pre-existing variation in the first 30 generations, increasing their reliance on new mutations in later generations (Ament-Velásquez et al., 2022).”
From Genomics of plant speciation (2023) · cites this paper as Ament-Velásquez et al., 2022
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
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
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
Trimmomatic: a flexible trimmer for Illumina sequence data
Bolger, A. M., Lohse, M., & Usadel, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu170 · Cited by 65,548 · see citing works
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
Wickham, H. (2016) · Use R! · doi:10.1007/978-3-319-24277-4 · Cited by 33,612 · see citing works
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al. (2010) · Genome Research · doi:10.1101/gr.107524.110 · Cited by 27,895 · see citing works
Modern Applied Statistics with S
Venables, W., & Ripley, B. (2010) · Statisctics and computing/Statistics and computing · doi:10.1007/978-0-387-21706-2 · Cited by 16,188 · see citing works
The variant call format and VCFtools
Danecek, P., Auton, A., Abecasis, G. R., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G. A., Marth, G., Sherry, S. T., et al. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr330 · Cited by 16,008 · see citing works
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li, H., & Durbin, R. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp698 · Cited by 12,063 · see citing works
Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (2012) · Fly · doi:10.4161/fly.19695 · Cited by 11,816 · see citing works
MultiQC: summarize analysis results for multiple tools and samples in a single report
Ewels, P., Magnusson, M., Lundin, S., & Käller, M. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw354 · Cited by 10,143 · see citing works
Szklarczyk, D., Gable, A. L., Nastou, K. C., Lyon, D., Kirsch, R., Pyysalo, S., Doncheva, N. T., Legeay, M., Fang, T., Bork, P., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1074 · Cited by 8,056 · see citing works
Genome sequence-based species delimitation with confidence intervals and improved distance functions
Meier‐Kolthoff, J. P., Auch, A. F., Klenk, H., & Göker, M. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-60 · Cited by 6,761 · see citing works
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method
Gietz, R. D., & Schiestl, R. H. (2007) · Nature Protocols · doi:10.1038/nprot.2007.13 · Cited by 2,785 · see citing works
Snakemake—a scalable bioinformatics workflow engine
Köster, J., & Rahmann, S. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts480 · Cited by 2,780 · see citing works
Meier‐Kolthoff, J. P., Carbasse, J. S., Peinado-Olarte, R. L., & Göker, M. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab902 · Cited by 2,252 · see citing works
Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data
Okonechnikov, K., Conesa, A., & García-Alcalde, F. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btv566 · Cited by 2,145 · see citing works
Adaptation from standing genetic variation
BARRETT, R., & SCHLUTER, D. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.09.008 · Cited by 2,091 · see citing works
Lenski, R. E., Rose, M. R., Simpson, S. C., & Tadler, S. C. (1991) · The American Naturalist · doi:10.1086/285289 · Cited by 1,582 · see citing works
Population genomics of domestic and wild yeasts
Liti, G., Carter, D. M., Moses, A. M., Warringer, J., Parts, L., James, S. A., Davey, R., Roberts, I. N., Burt, A., Koufopanou, V., et al. (2008) · Nature · doi:10.1038/nature07743 · Cited by 1,391 · see citing works
Variant Review with the Integrative Genomics Viewer
Robinson, J., Thorvaldsdóttir, H., Wenger, A. M., Zehir, A., & Mesirov, J. P. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-0337 · Cited by 1,118 · see citing works
vcfr : a package to manipulate and visualize variant call format data in R
Knaus, B. J., & Grünwald, N. J. (2016) · Molecular Ecology Resources · doi:10.1111/1755-0998.12549 · Cited by 1,061 · see citing works
Hermisson (2005) · doi:10.1534/genetics.104.036947 · Cited by 1,009 · see citing works
Effects of Aneuploidy on Cellular Physiology and Cell Division in Haploid Yeast
Torres, E. M., Sokolsky, T., Tucker, C. M., Chan, L. Y., Boselli, M., Dunham, M. J., & Amon, A. (2007) · Science · doi:10.1126/science.1142210 · Cited by 935 · see citing works
Maldonado, M., Guo, F., & Letts, J. A. (2021) · eLife · doi:10.7554/elife.62047 · Cited by 837 · see citing works
The Molecular Diversity of Adaptive Convergence
Tenaillon, O., Rodríguez-Verdugo, A., Gaut, R. L., McDonald, P., Bennett, A. F., Long, A. D., & Gaut, B. S. (2012) · Science · doi:10.1126/science.1212986 · Cited by 815 · see citing works
The fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Genetica · doi:10.1023/a:1017067816551 · Cited by 783 · see citing works
The dynamics of molecular evolution over 60,000 generations
Good, B. H., McDonald, M. J., Barrick, J. E., Lenski, R. E., & Desai, M. M. (2017) · Nature · doi:10.1038/nature24287 · Cited by 733 · see citing works
Long-Term Dynamics of Adaptation in Asexual Populations
Wiser, M. J., Ribeck, N., & Lenski, R. E. (2013) · Science · doi:10.1126/science.1243357 · Cited by 592 · see citing works
Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast
Pavelka, N., Rancati, G., Zhu, J., Bradford, W. D., Saraf, A., Florens, L., Sanderson, B. W., Hattem, G. L., & Li, R. (2010) · Nature · doi:10.1038/nature09529 · Cited by 577 · see citing works
Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations
Lang, G. I., Rice, D. P., Hickman, M. J., Sodergren, E. J., Weinstock, G. M., Botstein, D., & Desai, M. M. (2013) · Nature · doi:10.1038/nature12344 · Cited by 557 · see citing works
Adaptive responses of animals to climate change are most likely insufficient
Radchuk, V., Reed, T. E., Teplitsky, C., van de Pol, M., Charmantier, A., Hassall, C., Adamík, P., Adriaensen, F., Ahola, M., Arcese, P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10924-4 · Cited by 524 · see citing works
The fate of competing beneficial mutations in an asexual population.
Gerrish, P. J., & Lenski, R. E. (1998) · PubMed · Cited by 520 · see citing works
Global epistasis makes adaptation predictable despite sequence-level stochasticity
Kryazhimskiy, S., Rice, D. P., Jerison, E. R., & Desai, M. M. (2014) · Science · doi:10.1126/science.1250939 · Cited by 496 · see citing works
The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae
Stanley, D., Bandara, A., Fraser, S., Chambers, P. J., & Stanley, G. A. (2010) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2009.04657.x · Cited by 436 · see citing works
Sex speeds adaptation by altering the dynamics of molecular evolution
McDonald, M. J., Rice, D. P., & Desai, M. M. (2016) · Nature · doi:10.1038/nature17143 · Cited by 425 · see citing works
Polygenic adaptation: a unifying framework to understand positive selection
Barghi, N., Hermisson, J., & Schlötterer, C. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0250-z · Cited by 404 · see citing works
Aneuploidy Drives Genomic Instability in Yeast
Sheltzer, J. M., Blank, H. M., Pfau, S. J., Tange, Y., George, B. M., Humpton, T. J., Brito, I., Hiraoka, Y., Niwa, O., & Amon, A. (2011) · Science · doi:10.1126/science.1206412 · Cited by 398 · see citing works
McDonald, B. A., & Stukenbrock, E. H. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0026 · Cited by 381 · see citing works
Proft, M., & Struhl, K. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00557-9 · Cited by 350 · see citing works
Trait Variation in Yeast Is Defined by Population History
Warringer, J., Zörgö, E., Cubillos, F. A., Zia, A., Gjuvsland, A. B., Simpson, J. T., Forsmark, A., Durbin, R. M., Omholt, S. W., Louis, E. J., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002111 · Cited by 338 · see citing works
Contrasting evolutionary genome dynamics between domesticated and wild yeasts
Yue, J., Li, J., Aigrain, L., Hallin, J., Persson, K. O., Oliver, K. L., Bergström, A., Coupland, P. G., Warringer, J., Lagomarsino, M. C., et al. (2017) · Nature Genetics · doi:10.1038/ng.3847 · Cited by 332 · see citing works
Rapid assessment of S. cerevisiae mating type by PCR
Illuxley, C., Green, E. D., & Dunbam, I. (1990) · Trends in Genetics · doi:10.1016/0168-9525(90)90190-h · Cited by 326 · see citing works
Selmecki, A. M., Dulmage, K., Cowen, L. E., Anderson, J. B., & Berman, J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000705 · Cited by 319 · see citing works
The Isw2 Chromatin Remodeling Complex Represses Early Meiotic Genes upon Recruitment by Ume6p
Goldmark, J. P., Fazzio, T. G., Estep, P. W., Church, G. M., & Tsukiyama, T. (2000) · Cell · doi:10.1016/s0092-8674(00)00134-3 · Cited by 300 · see citing works
Genetic redundancy fuels polygenic adaptation in Drosophila
Barghi, N., Tobler, R., Nolte, V., Jakšić, A. M., Mallard, F., Otte, K. A., Dolezal, M., Taus, T., Kofler, R., & Schlötterer, C. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000128 · Cited by 293 · see citing works
Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy
Chen, G., Bradford, W. D., Seidel, C. W., & Li, R. (2012) · Nature · doi:10.1038/nature10795 · Cited by 274 · see citing works
Revealing the genetic structure of a trait by sequencing a population under selectionPreprint
Parts, L., Cubillos, F. A., Warringer, J., Jain, K., Salinas, F., Bumpstead, S. J., Molin, M., Zia, A., Simpson, J. T., Quail, M. A., et al. (2011) · Genome Research · doi:10.1101/gr.116731.110 · Cited by 269 · see citing works
Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae
Hohmann, S. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.10.069 · Cited by 258 · see citing works
GenMap: ultra-fast computation of genome mappability
Pockrandt, C., Alzamel, M., Iliopoulos, C. S., & Reinert, K. (2020) · Bioinformatics · doi:10.1093/bioinformatics/btaa222 · Cited by 232 · see citing works
A recyclableCandida albicans URA3 cassette for PCR product-directed gene disruptions
Wilson, R. B., Davis, D. A., Enloe, B. M., & Mitchell, A. P. (2000) · Yeast · doi:10.1002/(sici)1097-0061(20000115)16:1 · Cited by 228 · see citing works
Direct observation of adaptive tracking on ecological time scales in Drosophila
Rudman, S. M., Greenblum, S. I., Rajpurohit, S., Betancourt, N. J., Hanna, J., Tilk, S., Yokoyama, T., Petrov, D. A., & SCHMIDT, P. S. (2022) · Science · doi:10.1126/science.abj7484 · Cited by 192 · see citing works
Proft, M., & Serrano, R. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.1.537 · Cited by 180 · see citing works
THE PROBABILITY OF PARALLEL EVOLUTION
Orr, H. A. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb00907.x · Cited by 178 · see citing works
Adaptation of<i>Saccharomyces cerevisiae</i>to saline stress through laboratory evolution
DHAR, R., SÄGESSER, R., WEIKERT, C., YUAN, J., & WAGNER, A. (2011) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2011.02249.x · Cited by 165 · see citing works
Standing genetic variation as the predominant source for adaptation of a songbird
Lai, Y.-T., Yeung, C. K. L., Omland, K. E., Pang, E.-L., Hao, Y., Liao, B., Cao, H.-F., Zhang, B.-W., Yeh, C., Hung, C., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1813597116 · Cited by 160 · see citing works
Burke, M. K., Liti, G., & Long, A. D. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu256 · Cited by 158 · see citing works
An Evolutionary Advantage of Haploidy in Large Yeast Populations
Zeyl, C., Vanderford, T. H., & Carter, M. R. (2003) · Science · doi:10.1126/science.1078417 · Cited by 152 · see citing works
The Effect of Selection Environment on the Probability of Parallel Evolution
Bailey, S. F., Rodrigue, N., & Kassen, R. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv033 · Cited by 150 · see citing works
High-Resolution Mapping of Complex Traits with a Four-Parent Advanced Intercross Yeast Population
Cubillos, F. A., Parts, L., Salinas, F., Bergström, A., Scovacricchi, E., Zia, A., Illingworth, C. J. R., Mustonen, V., Ibstedt, S., Warringer, J., et al. (2013) · Genetics · doi:10.1534/genetics.113.155515 · Cited by 137 · see citing works
Yeast putative transcription factors involved in salt tolerance
Mendizabal, I., Rios, G., Mulet, J. M., Serrano, R., & de Larrinoa, I. F. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00249-x · Cited by 136 · see citing works
Iida, T., & Araki, H. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.24.1.217-227.2004 · Cited by 130 · see citing works
Catch Me if You Can: Adaptation from Standing Genetic Variation to a Moving Phenotypic Optimum
Matuszewski, S., Hermisson, J., & Kopp, M. (2015) · Genetics · doi:10.1534/genetics.115.178574 · Cited by 126 · see citing works
Haploids adapt faster than diploids across a range of environments
Gerstein, A. C., CLEATHERO, L. A., Mandegar, M. A., & Otto, S. P. (2010) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2010.02188.x · Cited by 125 · see citing works
What drives parallel evolution?
Bailey, S. F., Blanquart, F., Bataillon, T. M., & Kassen, R. (2016) · BioEssays · doi:10.1002/bies.201600176 · Cited by 124 · see citing works
Single-cell copy number variant detection reveals the dynamics and diversity of adaptation
Lauer, S. L., Avecilla, G., Spealman, P., Sethia, G., Brandt, N. J., Levy, S. F., & Gresham, D. (2018) · PLoS Biology · doi:10.1371/journal.pbio.3000069 · Cited by 121 · see citing works
Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations
Johnson, M. S., Gopalakrishnan, S., Goyal, J., Dillingham, M. E., Bakerlee, C. W., Humphrey, P. T., Jagdish, T., Jerison, E. R., Kosheleva, K., Lawrence, K. R., et al. (2021) · eLife · doi:10.7554/elife.63910 · Cited by 119 · see citing works
Experimental Evolution of Yeast for High-Temperature Tolerance
Huang, C.-J., Lu, M. J., Chang, Y.-W., & Li, W. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy077 · Cited by 117 · see citing works
Dr Jekyll and Mr Hyde: role of aneuploidy in cellular adaptation and cancer
Pavelka, N., Rancati, G. I., & Li, R. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2010.06.003 · Cited by 110 · see citing works
Aneuploidy in yeast: Segregation error or adaptation mechanism?
Gilchrist, C., & Stelkens, R. B. (2019) · Yeast · doi:10.1002/yea.3427 · Cited by 110 · see citing works
Self-citationSingle nucleotide mapping of trait space reveals Pareto fronts that constrain adaptation
Li, Y., Petrov, D. A., & Sherlock, G. J. (2019) · Nature Ecology & Evolution · doi:10.1038/s41559-019-0993-0 · Cited by 107 · see citing works
Higher-fitness yeast genotypes are less robust to deleterious mutations
Johnson, M. S., Martsul, A., Kryazhimskiy, S., & Desai, M. M. (2019) · Science · doi:10.1126/science.aay4199 · Cited by 96 · see citing works
Parallel genetic evolution and speciation from standing variation
Thompson, K. A., Osmond, M. M., & Schluter, D. (2019) · Evolution Letters · doi:10.1002/evl3.106 · Cited by 95 · see citing works
Effects of aneuploidy on gene expression: implications for cancer
Dürrbaum, M., & Štorchová, Z. (2015) · FEBS Journal · doi:10.1111/febs.13591 · Cited by 92 · see citing works
Activation of the HOG Pathway upon Cold Stress in Saccharomyces cerevisiae
Hayashi, M., & Maeda, T. (2006) · The Journal of Biochemistry · doi:10.1093/jb/mvj089 · Cited by 89 · see citing works
Spontaneous Changes in Ploidy Are Common in Yeast
Harari, Y., Ram, Y., Rappoport, N., Hadany, L., & Kupiec, M. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.062 · Cited by 81 · see citing works
The probability of parallel genetic evolution from standing genetic variation
MacPherson, A., & Nuismer, S. L. (2017) · Journal of Evolutionary Biology · doi:10.1111/jeb.13006 · Cited by 79 · see citing works
Ssn6–Tup1 requires the ISW2 complex to position nucleosomes in Saccharomyces cerevisiae
Zhang, Z., & Reese, J. C. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600227 · Cited by 78 · see citing works
Green, S. R., & Johnson, A. D. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-05-0412 · Cited by 72 · see citing works
Ruiz, A., Yenush, L., & Ariño, J. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.5.937-948.2003 · Cited by 71 · see citing works
Kosheleva, K., & Desai, M. M. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx278 · Cited by 71 · see citing works
Quantifying Selection Acting on a Complex Trait Using Allele Frequency Time Series Data
Illingworth, C. J. R., Parts, L., Schiffels, S., Liti, G., & Mustonen, V. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr289 · Cited by 61 · see citing works
A Double-Edged Sword: Aneuploidy is a Prevalent Strategy in Fungal Adaptation
Tsai, H.-J., & Nelliat, A. (2019) · Genes · doi:10.3390/genes10100787 · Cited by 60 · see citing works
Genomic evidence that resource-based trade-offs limit host-range expansion in a seed beetle
Gompert, Z., & Messina, F. J. (2016) · Evolution · doi:10.1111/evo.12933 · Cited by 59 · see citing works
Chaturvedi, A., Zhou, J., Raeymaekers, J. A. M., Czypionka, T., Orsini, L., Jackson, C. E., Spanier, K. I., Shaw, J. R., Colbourne, J. K., & Meester, L. D. (2021) · Nature Communications · doi:10.1038/s41467-021-24581-z · Cited by 56 · see citing works
Na+-ATPases and Na+/H+ antiporters in fungi
Rodríguez‐Navarro, A., Quintero, F. J., & Garcíadeblas, B. (1994) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(94)90111-2 · Cited by 52 · see citing works
Membrane fluidification by ethanol stress activates unfolded protein response in yeasts
Navarro‐Tapia, E., Querol, A., & Pérez‐Torrado, R. (2018) · Microbial Biotechnology · doi:10.1111/1751-7915.13032 · Cited by 51 · see citing works
Clonal Heterogeneity Influences the Fate of New Adaptive Mutations
Vázquez-Garćıa, I., Salinas, F., Li, J., Fischer, A., Barré, B. P., Hallin, J., Bergström, A., Alonso‐Perez, E., Warringer, J., Mustonen, V., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.046 · Cited by 50 · see citing works
Genomic Evidence of an Ancient East Asian Divergence Event in Wild Saccharomyces cerevisiae
Bendixsen, D. P., Gettle, N., Gilchrist, C., Zhang, Z., & Stelkens, R. B. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab001 · Cited by 49 · see citing works
Self-citationTup1 stabilizes promoter nucleosome positioning and occupancy at transcriptionally plastic genes
Rizzo, J. M., Mieczkowski, P. A., & Buck, M. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr557 · Cited by 48 · see citing works
Gasch, A. P., Hose, J., Newton, M. A., Sardi, M. I., Yong, M., & Wang, Z. (2016) · eLife · doi:10.7554/elife.14409 · Cited by 47 · see citing works
Genetic variation in aneuploidy prevalence and tolerance across Saccharomyces cerevisiae lineages
da Costa, E. S. F., Hose, J., Bensasson, D., & Gasch, A. P. (2021) · Genetics · doi:10.1093/genetics/iyab015 · Cited by 42 · see citing works
He, F., Steige, K. A., Kováčová, V., Göbel, U., Bouzid, M., Keightley, P. D., Beyer, A., & de Meaux, J. (2021) · Nature Communications · doi:10.1038/s41467-021-23558-2 · Cited by 37 · see citing works
Cell populations can use aneuploidy to survive telomerase insufficiency
Millet, C., Ausiannikava, D., Bihan, T. L., Granneman, S., & Makovets, S. (2015) · Nature Communications · doi:10.1038/ncomms9664 · Cited by 36 · see citing works
Harris, K. B., Flynn, K. M., & Cooper, V. S. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab248 · Cited by 30 · see citing works
Breeding systems and heterozygosity in populations of tetrad forming fungi
Kirby, G. C. (1984) · Heredity · doi:10.1038/hdy.1984.5 · Cited by 30 · see citing works
Biernat, E., Kinney, J., Dunlap, K. N., Rizza, C., & Govind, C. K. (2021) · Genetics · doi:10.1093/genetics/iyab021 · Cited by 27 · see citing works
Detecting selected haplotype blocks in evolve and resequence experiments
Otte, K. A., & Schlötterer, C. (2020) · Molecular Ecology Resources · doi:10.1111/1755-0998.13244 · Cited by 25 · see citing works
Linder, R. A., Majumder, A., Chakraborty, M., & Long, A. D. (2020) · Genetics · doi:10.1534/genetics.120.303202 · Cited by 23 · see citing works
Consequences of Cryopreservation in Diverse Natural Isolates of Saccharomyces cerevisiae
Wing, K., Phillips, M., Baker, A. R., & Burke, M. K. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa121 · Cited by 18 · see citing works
Phillips, M., Kutch, I. C., Long, A. D., & Burke, M. K. (2020) · Molecular Ecology · doi:10.1111/mec.15687 · Cited by 18 · see citing works
Adaptation in Outbred Sexual Yeast is Repeatable, Polygenic and Favors Rare Haplotypes
Linder, R. A., Zabanavar, B., Majumder, A., Hoang, H. C.-S., Delgado, V. G., Tran, R. V., La, V. T., Leemans, S. W., & Long, A. D. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac248 · Cited by 15 · see citing works
Eco-Evolutionary Dynamics in the Wild: Clonal Turnover and Stability in Daphnia Populations
Steiner, C. F., & Nowicki, C. J. (2019) · The American Naturalist · doi:10.1086/703484 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 105 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Trachtulcová P, Janatová I, Kohlwein SD, Hašek J. 2000. Saccharomyces cerevisiae gene ISW2 encodes a microtubule-interacting protein required for premeiotic DNA replication. Yeast 16(1): 35– 47. 10620773
- Wickham H. 2016. Ggplot2: elegant graphics for data analysis. New York: Springer-Verlag.
Cited by
Sorted by citations
Bock, D. G., Cai, Z., Elphinstone, C., González-Segovia, E., Hirabayashi, K., Huang, K., Keais, G. L., Kim, A., Owens, G. L., & Rieseberg, L. H. (2023) · Plant Communications · doi:10.1016/j.xplc.2023.100599 · Cited by 84 · see citing works
“This expected progression is seen in experimental yeast populations exposed to different stressinducing substances; some populations (but not others) rapidly depleted pre-existing variation in the first 30 generations, increasing their reliance on new mutations in later generations (Ament-Velásquez et al., 2022).”
Loss of Heterozygosity and Its Importance in Evolution
Heil, C. S. (2023) · Journal of Molecular Evolution · doi:10.1007/s00239-022-10088-8 · Cited by 43 · see citing works
Alkemade, J., Hawkins, N. J., Baraldi, E., Buddie, A. G., Cockerton, H. M., Corkley, I., FRAAIJE, B. A., Gaya, E., Gifford, D. R., Hartig, F., et al. (2025) · Fungal Biology Reviews · doi:10.1016/j.fbr.2025.100443 · Cited by 26 · see citing works
The evolutionary and ecological potential of yeast hybrids
Stelkens, R. B., & Bendixsen, D. P. (2022) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2022.101958 · Cited by 24 · see citing works
Self-citationHowe, N. S., Hale, M. C., Waters, C. D., Schaal, S. M., Shedd, K. R., & Larson, W. A. (2024) · Evolutionary Applications · doi:10.1111/eva.13656 · Cited by 19 · see citing works
Embracing Complexity: Yeast Evolution Experiments Featuring Standing Genetic Variation
Burke, M. K. (2023) · Journal of Molecular Evolution · doi:10.1007/s00239-023-10094-4 · Cited by 11 · see citing works
Estandía, A., Sendell‐Price, A. T., Robertson, B. C., & Clegg, S. M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.29.546893 · Cited by 10 · see citing works
A microbial perspective on speciation
Stelkens, R. B. (2024) · Evolutionary Journal of the Linnean Society · doi:10.1093/evolinnean/kzae023 · Cited by 7 · see citing works
Self-citationEvidence of landscape-driven repeated adaptation among 13 Eucalyptus species
Ahrens, C. W., Bragg, J. G., van der Merwe, M. M., & Rossetto, M. (2025) · Evolution · doi:10.1093/evolut/qpaf049 · Cited by 6 · see citing works
Progressive transcriptomic shifts in evolved yeast strains following gene knockout
Jiang, B., Xiao, C., & Liu, L. (2024) · iScience · doi:10.1016/j.isci.2024.111219 · Cited by 5 · see citing works
Can Transcriptomics Elucidate the Role of Regulation in Invasion Success?
Vaughan, A. L., & Dhami, M. K. (2024) · Molecular Ecology · doi:10.1111/mec.17583 · Cited by 5 · see citing works
Compensatory Evolution Following Deleterious Episodes of GC-biased Gene Conversion in Rodents
Riffis, M., Saclier, N., & Galtier, N. (2025) · Molecular Biology and Evolution · doi:10.1093/molbev/msaf168 · Cited by 5 · see citing works
Genetic Bottlenecks in Modern Beekeeping: Implications for Conservation and Sustainable Pollination
Lin, Z., Zhang, Y., Wang, K., Jiang, X., & Ji, T. (2025) · Conservation Letters · doi:10.1111/conl.13156 · Cited by 4 · see citing works
Marfurt, S. M., Chabanne, D. B. H., Wittwer, S., Bizzozzero, M. R., Allen, S. J., Gerber, L., Nicholson, K. E., & Krützen, M. (2024) · Molecular Ecology · doi:10.1111/mec.17555 · Cited by 3 · see citing works
Bendixsen, D. P., Gilchrist, C., Haberkorn, C., Persson, K. O., Geijer, C., Warringer, J., & Stelkens, R. B. (2025) · Molecular Ecology · doi:10.1111/mec.70110 · Cited by 3 · see citing works
Self-citationResource presentation dictates genetic and phenotypic adaptation in yeast
Ahlawat, N., Mahilkar, A., & Saini, S. (2025) · BMC Ecology and Evolution · doi:10.1186/s12862-025-02361-3 · Cited by 3 · see citing works
Network architecture of transcriptomic stress responses in zebrafish embryos
Beine, K., Feugere, L., Turner, A. P., & Valero, K. C. W. (2025) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1013164 · Cited by 2 · see citing works
Rêgo, A., Stajic, D., Bautista, C., Rouot, S., Celorio‐Mancera, M. D. L. P., & Stelkens, R. B. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.24.577006 · Cited by 2 · see citing works
Self-citationHow bottlenecks shape adaptive potential: from theory and microbiology to conservation biologyPreprint
Gamblin, J., Marrec, L., & Olazcuaga, L. (2024) · doi:10.32942/x2m608 · Cited by 2 · see citing works
Genetic Adaptation of Mesorhizobium Symbionts Associated With Caragana in Northern China Deserts
Yuan, X., Li, H., Yu, X., & Ji, Z. J. (2026) · Ecology and Evolution · doi:10.1002/ece3.73134 · Cited by 1 · see citing works
Addressing multi-generational non-genetic responses in experimental studies of evolution
Zilio, G., Bedhomme, S., Fronhofer, E. A., Jacob, S., Legrand, D., Philippe, H., & Chevin, L. (2026) · Evolution · doi:10.1093/evolut/qpag027 · Cited by 1 · see citing works
Marfurt, S. M., Adrien Tran Lu, Y., Dauphin, B., Bizzozzero, M. R., Hatakeyama, M., Chabanne, D. B. H., Allen, S. J., Smith, F., Parra, G. J., & Krützen, M. (2026) · Molecular Ecology · doi:10.1111/mec.70383 · Cited by 1 · see citing works
Pramono, A., Cahyadi, M., Tamartian, A. H., Fatonah, H., Alfara, I. R., Romadhon, S., & Barido, F. H. (2026) · Veterinary World · doi:10.14202/vetworld.2026.2264-2278 · Cited by 1 · see citing works
Haberkorn, C., Gettle, N., Elsen, J., Medina-Chávez, N. O., Sivigny, J., Baselga‐Cervera, B., Greig, D., Travisano, M., Saxer, G., & Stelkens, R. B. (2026) · Evolution · doi:10.1093/evolut/qpag108 · Cited by 1 · see citing works
Self-citationExaptation and de novo mutations transcend cryptic variations as drivers of adaptation in yeastPreprint
Routh, S., Lindsay, R. J., Gudelj, I., & Dhar, R. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.26.586634
Routh, S., Lindsay, R. J., Gudelj, I., & Dhar, R. (2025) · Evolution · doi:10.1093/evolut/qpaf019
Revealing the link between cell volume and evolution
García‐Ruano, D. (2023) · doi:10.70675/7df2b48az59e1z4bebzbdb4z10c070f0fc1c
Edwards, E. M., Akopyan, M., Mosher, B. A., Therkildsen, N. O., & Sullivan, P. (2026) · Conservation Genetics · doi:10.1007/s10592-026-01787-6
Appiah, P., & Yeboah, R. (2026) · Journal of Environmental Protection · doi:10.4236/jep.2026.177031
Aslam, M. T., Ghafoor, S., Mushtaq, W., Yang, X., Dong, S., Kang, Y., Alshamrani, R., EL-BELTAGI, H. S., Fang, S., & Wu, Z. (2026) · Industrial Crops and Products · doi:10.1016/j.indcrop.2026.124409
Understanding and managing ecological light pollution
Dickerson, A. L., Longcore, T., Jechow, A., Knop, E., Thiggins, B., & Hölker, F. (2026) · Nature Reviews Biodiversity · doi:10.1038/s44358-026-00206-5
- Authors
- Ament-Velásquez, S. L., Gilchrist, C., Rêgo, A., Bendixsen, D. P., Brice, C., Grosse-Sommer, J. M., Rafati, N., & Stelkens, R.
- Affiliations
- Division of Population Genetics, Department of Zoology, Stockholm University , Svante Arrheniusväg 18 B, 106 91 Stockholm , Sweden
- Stockholm University (SE)
- Uppsala University (SE)
- Corresponding author
- Stelkens, Rike
- ORCID
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2022-11-01
- Volume
- 39
- Issue
- 11
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- PMC
- PMC9703598
- OpenAlex
- W4308253979
- Cited by
- 31
- References
- 105
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 8 · 2023: 5 · 2022: 1
- FWCI
- 3.32
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Molecular Biology and Evolution (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- Swedish Research Council
- Knut and Alice Wallenberg Foundation
- Stockholm University
- SciLifeLab
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
- Keywords
- standing genetic variation, de novo mutations, stress adaptation, parallel evolution, Saccharomyces cerevisiae, asexual populations, allele frequency dynamics, aneuploidy, fitness cost, experimental evolution, pool-seq
- MeSH terms
- Adaptation, Physiological, Mutation, Saccharomyces cerevisiae, Stress, Physiological, Genetic Variation, Evolution, Molecular, Genetic Fitness
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
