Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations
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Adaptive laboratory evolution was already performed about a hundred years ago by William Dallinger and during the middle of the last century.
“Hence, adaptive laboratory evolution was already performed about a hundred years ago by William Dallinger [22] and during the middle of the last century [24,25];”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [25]
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BackgroundInfluentialThe Properties of Adaptive Walks in Evolving Populations of Fungus
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BackgroundResultInfluentialHunger Artists: Yeast Adapted to Carbon Limitation Show Trade-Offs under Carbon Sufficiency
Wenger, J. W., Piotrowski, J., Nagarajan, S., Chiotti, K., Sherlock, G., & Rosenzweig, F. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002202 · Cited by 154 · see citing works
“Evolved Clones Outperform Their Ancestor in Diverse Carbon-Limited Environments Paquin & Adams [8,9] and Ferea et al. [13] isolated end-clones from independent evolution experiments originating from a Author Summary Microorganisms such as yeast have been used for decades to study adaptive evolution by natural selectio…”
BackgroundMethodResultInfluentialAn Evolutionary Advantage of Haploidy in Large Yeast Populations
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“In addition, since diploids carry twice as much DNA as haploids, they might be expected to accumulate new beneficial mutations at a higher rate (Paquin and Adams 1983).”
BackgroundDoes diploidy increase the rate of adaptation?
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BackgroundImproved use of a public good selects for the evolution of undifferentiated multicellularity
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MethodPloidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution
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“These properties include the rate of bene fi cial mutations, the fi tness effect of these mutations, the dominance of mutant alleles, and effective population size (147 – 153).”
Mitotic Recombination Accelerates Adaptation in the Fungus Aspergillus nidulans
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“Seminal studies by Paquin and Adams in the 1980s established the use of budding yeast in experimental evolution studies in chemostats [37,38].”
BackgroundClonal Interference and the Periodic Selection of New Beneficial Mutations in Escherichia coli
de Visser, J. A. G. M., & Rozen, D. E. (2006) · Genetics · doi:10.1534/genetics.105.052373 · Cited by 128 · see citing works
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BackgroundResultInfluentialThe enduring utility of continuous culturing in experimental evolution
Gresham, D., & Dunham, M. J. (2014) · Genomics · doi:10.1016/j.ygeno.2014.09.015 · Cited by 120 · see citing works
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The functional basis of adaptive evolution in chemostats
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“To distinguish the two strains and estimate their relative abundances , they are typically marked by neutral markers such as a drug (Paquin & Adams, 1983a, b; Gresham et al., 2008) or phage resistance (Novick & Szilard, 1950b) allele, which facilitates genotype estimation by plating.”
Lin, X., Patel, S., Litvintseva, A. P., Floyd, A. M., Mitchell, T. G., & Heitman, J. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000283 · Cited by 120 · see citing works
“different environments [12,52,86,91,92], and differences in ploidy”
The dynamics of adaptation on correlated fitness landscapes
Kryazhimskiy, S., Tkačik, G., & Plotkin, J. B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905497106 · Cited by 120 · see citing works
“Experimental studies of microbial evolution typically report the mean fitness of the population (21, 22) and the mean number of accumulated substitutions (23, 24) over time; therefore we develop a theory that predicts these dynamic quantities, which we call the fitness and substitution trajectories, in terms of the un…”
BackgroundHaploidy, diploidy and evolution of antifungal drug resistance in Saccharomyces cerevisiae
Anderson, J. B., Sirjusingh, C., & Ricker, N. (2004) · Genetics · doi:10.1534/genetics.104.033266 · Cited by 111 · see citing works
“…haploid drugs could potentially be deployed to manage resistance in fungal pathogens if the fitness effects of theirpopulations in adapting to glucose limitation in chemo- stats (Paquin and Adams 1983), while haploid popula- resistance mutations in the host mirror those of S. cerevisiae seen here.”
BackgroundReyes, L. H., Almario, M. P., Winkler, J. D., Orozco, M. M., & Kao, K. C. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.05.002 · Cited by 112 · see citing works
Population Genomics of Herbicide Resistance: Adaptation via Evolutionary Rescue
Kreiner, J. M., Stinchcombe, J. R., & Wright, S. (2017) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042817-040038 · Cited by 111 · see citing works
Cancer in Light of Experimental Evolution
Sprouffske, K., Merlo, L. M. F., Gerrish, P. J., Maley, C. C., & Sniegowski, P. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.065 · Cited by 108 · see citing works
Histone H1 in Saccharomyces cerevisiae
Ushinsky, S. C., Bussey, H., Ahmed, A., Wang, Y., Friesen, J. D., Williams, B. A., & Storms, R. K. (1997) · Yeast · doi:10.1002/(sici)1097-0061(199702)13:2 · Cited by 106 · see citing works
The genetics of aging in the yeastSaccharomyces cerevisiae
Jazwinski, S. M. (1993) · Genetica · doi:10.1007/bf01435986 · Cited by 98 · see citing works
“Yeast populations evolving in a chemostat acquire adaptive changes (mutations) in a limited number of loci that display rather complex epistatic or functional interactions ( Paquin & Adams, 1983, 1983a; Adams et al., 1985).”
BackgroundBeneficial Mutations, Hitchhiking and the Evolution of Mutation Rates in Sexual Populations
Johnson, T. (1999) · Genetics · doi:10.1093/genetics/151.4.1621 · Cited by 97 · see citing works
Janko, K., Bohlen, J., Lamatsch, D. K., Flajšhans, M., Epplen, J. T., Ráb, P., Kotlı́k, P., & Šlechtová, V. (2007) · Genetica · doi:10.1007/s10709-006-9130-5 · Cited by 96 · see citing works
“beneficial alleles, (Paquin and Adams 1993), mask the effects of deleterious mutations (Kondrashov and Crow 1991; but see Kondrashov 1997), or allow for the”
BackgroundDelneri, D., Hoyle, D. C., Gkargkas, K., Cross, E. J. M., Rash, B. M., Zeef, L. A. H., Leong, H. S., Davey, H. M., Hayes, A., Kell, D. B., et al. (2007) · Nature Genetics · doi:10.1038/ng.2007.49 · Cited by 95 · see citing works
“In practice, the period of competition should not exceed 50 generations; otherwise, spontaneous mutations may complicate the analysi”
BackgroundBond, U., Neal, C. L., Donnelly, D., & James, T. C. (2004) · Current Genetics · doi:10.1007/s00294-004-0504-x · Cited by 93 · see citing works
“It was previously shown that the laboratory strain of S. cerevisiae, when grown under selection pressure, acquired advantageous genetic traits (Paquin and Adams 1983).”
BackgroundInfluentialGenomic investigations of evolutionary dynamics and epistasis in microbial evolution experiments
Jerison, E. R., & Desai, M. M. (2015) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.08.008 · Cited by 92 · see citing works
Geographic components of linkage disequilibrium in natural populations of Escherichia coli.
Whittam, T. S., Ochman, H., & Selander, R. K. (1984) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040302 · Cited by 92 · see citing works
The unforeseen challenge: from genotype-to-phenotype in cell populations
Braun, E. (2015) · Reports on Progress in Physics · doi:10.1088/0034-4885/78/3/036602 · Cited by 88 · see citing works
“A different type of experiments on evolving yeast populations in chemostats, utilized drug resistance as a neutral marker allowing to follow population sweeps which were shown to occur on timescales of approximately 100 generations [46].”
BackgroundHigh-Throughput Identification of Adaptive Mutations in Experimentally Evolved Yeast Populations
Payen, C., Sunshine, A. B., Ong, G. T., Pogachar, J. L., Zhao, W. D., & Dunham, M. J. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006339 · Cited by 83 · see citing works
Co-infection Weakens Selection Against Epistatic Mutations in RNA Viruses
Froissart, R., Wilke, C. O., Montville, R., Remold, S. K., Chao, L., & Turner, P. E. (2004) · Genetics · doi:10.1534/genetics.104.030205 · Cited by 89 · see citing works
“Different (Paquin and Adams 1983; Kondrashov and Crow hypotheses have been proposed to explain this genome 1991; Orr and Otto 1994).”
Historical perspective on airway smooth muscle: the saga of a frustrated cell
Seow, C. Y., & Fredberg, J. J. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.2.938 · Cited by 87 · see citing works
Measuring Selection Coefficients Below 10−3: Method, Questions, and Prospects
Gallet, R., Cooper, T. F., Elena, S. F., & Lenormand, T. (2011) · Genetics · doi:10.1534/genetics.111.133454 · Cited by 86 · see citing works
“This assumption has been evaluated on several occasions and in different High-Precision Fitness Measures 183 organisms (Richmond et al. 1975; Goodman 1979; Paquin and Adams 1983; De Visser and Lenski 2002; Bell 2008).”
MethodAltered access to beneficial mutations slows adaptation and biases fixed mutations in diploids
Marad, D. A., Buskirk, S. W., & Lang, G. I. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0503-9 · Cited by 84 · see citing works
Mating systems and the evolutionary transition between haploidy and diploidy
Otto, S. P., & Marks, J. C. (1996) · Biological Journal of the Linnean Society · doi:10.1006/bijl.1996.0011 · Cited by 83 · see citing works
Generation of Novel Wine Yeast Strains by Adaptive Evolution
McBryde, C., Gardner, J. M., Lopes, M. D. B., & Jiranek, V. (2006) · American Journal of Enology and Viticulture · doi:10.5344/ajev.2006.57.4.423 · Cited by 79 · see citing works
ASYMMETRIC, BIMODAL TRADE-OFFS DURING ADAPTATION OFMETHYLOBACTERIUMTO DISTINCT GROWTH SUBSTRATES
Lee, M.-C., Chou, H.-H. D., & Marx, C. J. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00757.x · Cited by 79 · see citing works
“One possible alternative could be the emergence of nontransitive interactions, which has previously been shown to be capable of even causing apparent decreases in mean fitness when in competition against the common ancestor (Paquin and Adams 1983).”
BackgroundToward a General Theory of Adaptive Radiation
Kassen, R. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04574.x · Cited by 79 · see citing works
“…work from microbial systems largely supports this view: experiments in bacteria (Elena et al. 2006; Lenski et al. 1991) and yeast (Zeyl 2005; Paquin & Adams 1983) have inferred that between three and six mutations were involved in adaptation over the course of between a few hundred and…”
BackgroundResource competition and adaptive radiation in a microbial microcosm
MacLean, R. C., Dickson, A., & Bell, G. (2004) · Ecology Letters · doi:10.1111/j.1461-0248.2004.00689.x · Cited by 78 · see citing works
“A number of selection experiments have reported results that are consistent with this paradigm (Novick & Szilard 1950; Atwood et al. 1951; Paquin & Adams 1983; Lenski & Travisano 1994).”
ResultThe spectrum of adaptive mutations in experimental evolution
Lang, G. I., & Desai, M. M. (2014) · Genomics · doi:10.1016/j.ygeno.2014.09.011 · Cited by 75 · see citing works
Characterizing polyploidy inArabidopsis lyratausing chromosome counts and flow cytometry
Dart, S. R., Kron, P., & Mable, B. K. (2004) · Canadian Journal of Botany · doi:10.1139/b03-134 · Cited by 78 · see citing works
Evolution of isoprene emission capacity in plants
Dani, K. G. S., Jamie, I. M., Prentice, I. C., & Atwell, B. J. (2014) · Trends in Plant Science · doi:10.1016/j.tplants.2014.01.009 · Cited by 71 · see citing works
Hitchhiking and epistasis give rise to cohort dynamics in adapting populations
Buskirk, S. W., Peace, R. E., & Lang, G. I. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1702314114 · Cited by 65 · see citing works
“Early theoretical models assume that beneficial mutations are rare, such that once a beneficial 39 mutation escapes drift, it will fix (3-5).”
BackgroundThe Evolutionary Consequences of Selection at the Haploid Gametic Stage
Immler, S., & Otto, S. P. (2018) · The American Naturalist · doi:10.1086/698483 · Cited by 68 · see citing works
Zhou, N., Bottagisi, S., Katz, M., Schacherer, J., Friedrich, A., Gojkovic, Z., Swamy, K. B. S., Knecht, W., Compagno, C., & Piškur, J. (2017) · FEMS Yeast Research · doi:10.1093/femsyr/fox060 · Cited by 67 · see citing works
Couceiro, L., Gac, M. L., Hunsperger, H. M., Mauger, S., Destombe, C., Cock, J. M., Ahmed, S., Coelho, S. M., Valéro, M., & Peters, A. F. (2015) · Evolution · doi:10.1111/evo.12702 · Cited by 66 · see citing works
“…hypotheses, based on the genetic advantages of having two sets of homologous chromosomes, were thus advanced to explain the evolution of an extended diploid phase: the masking hypothesis (Crow and Kimura 1965) and the hypothesis of the higher rate of beneficial mutations (Paquin and Adams 1983).”
BackgroundWyatt, R., Odrzykoski, I. J., & Stoneburner, A. (1992) · Systematic Botany · doi:10.2307/2419725 · Cited by 66 · see citing works
Somatic mutation favors the evolution of diploidy.
Orr, H. A. (1995) · Genetics · doi:10.1093/genetics/139.3.1441 · Cited by 65 · see citing works
Weikert, C., Sauer, U., & Bailey, J. E. (1997) · Microbiology · doi:10.1099/00221287-143-5-1567 · Cited by 63 · see citing works
Boisselier‐Dubayle, M., Jubier, M.-F., Lejeune, B., & Bischler, H. (1995) · Taxon · doi:10.2307/1223406 · Cited by 63 · see citing works
Evolution of the life cycle in land plants
Qiu, Y., TAYLOR, A. B., & McManus, H. A. (2012) · Journal of Systematics and Evolution · doi:10.1111/j.1759-6831.2012.00188.x · Cited by 62 · see citing works
“For this reason, beneficial mutations may be fixed faster in diploids, a conjecture that has received some experimental support (Paquin & Adams, 1983).”
BackgroundGenome evolution mediated by Ty elements in Saccharomyces
Garfinkel, D. J. (2005) · Cytogenetic and Genome Research · doi:10.1159/000084939 · Cited by 62 · see citing works
“Paquin and Adams (1983) have shown that S. cerevisiae cultures evolve genetically when limited for glucose.”
BackgroundPeruzzi, B., Araten, D. J., Notaro, R., & Luzzatto, L. (2009) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2009.12.004 · Cited by 61 · see citing works
“Compared to bacteria and yeasts [10], the study of somatic mutations in animals and in animal cells is more complicated for various reasons, including the fact that animal cells are diploid.”
BackgroundFrenkel, E. M., Good, B. H., & Desai, M. M. (2014) · Genetics · doi:10.1534/genetics.113.160069 · Cited by 60 · see citing works
“…Oeller, 1986; Atwood et al., 1951; Barrett et al., 2006; Barrick et al., 2010; de Visser and Rozen, 2006; Hegreness et al., 2006; Helling et al., 1981; Imhof and Schlötterer, 2001; Kao and Sherlock, 2008; Lang et al., 2011; Novick and Szilard, 1950; Paquin and Adams, 1983; Perfeito et al., 2007).”
BackgroundMutational effects depend on ploidy level: all else is not equal
Gerstein, A. C. (2012) · Biology Letters · doi:10.1098/rsbl.2012.0614 · Cited by 59 · see citing works
Synthetic Gene Recruitment Reveals Adaptive Reprogramming of Gene Regulation in Yeast
Stolovicki, E., Dror, T. W., Brenner, N., & Braun, E. (2006) · Genetics · doi:10.1534/genetics.106.055442 · Cited by 57 · see citing works
“Microorganisms grown in continuous cultures (chemostats) are an ideal prototype system for such studies (Novick and Szilard 1950; Paquin and Adams 1983; Saldanha et al. 2004).”
BackgroundEvolution of haploid selection in predominantly diploid organisms
Otto, S. P., Scott, M. F., & Immler, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512004112 · Cited by 57 · see citing works
“These models have shown that purging of deleterious mutations favors expansion of the haploid phase when recombination is infrequent, but that diploids are favored because they better mask mutations from selection when recombination is common (33, 34).”
BackgroundThe Impact of Yeast Genetics and Recombinant DNA Technology on the Wine Industry - A Review
Pretorius, L., & van der Westhuizen, T. J. (1991) · South African Journal of Enology and Viticulture · doi:10.21548/12-1-2220 · Cited by 56 · see citing works
Experimental microbial evolution: history and conceptual underpinnings
Adams, J., & Rosenzweig, F. (2014) · Genomics · doi:10.1016/j.ygeno.2014.10.004 · Cited by 53 · see citing works
“For example, microbial systems were exploited to address questions addressing the predominance of the diploid phase [27], and the neutral theory of evolutionary change [28,29].”
BackgroundSelf-citationThe Influence of Polyploidy on the Evolution of Yeast Grown in a Sub-Optimal Carbon Source
Scott, A. L., Richmond, P. A., Dowell, R. D., & Selmecki, A. M. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx205 · Cited by 50 · see citing works
“Some of these theories have been confirmed experimentally, yet studies have focused almost exclusively on haploid and diploid yeast (Paquin and Adams 1983; Anderson et al. 2004; Zeyl 2004; Gerstein and Otto 2009).”
BackgroundThe population biology and evolutionary significance of Ty elements in Saccharomyces cerevisiae
Wilke, C. M., Maimer, E., & Adams, J. (1992) · Genetica · doi:10.1007/bf00133718 · Cited by 54 · see citing works
“Paquin & Adams, 1983; Kondrashov & Crow, 1991; Perrot, Richerd & Valrro, 1991).”
Self-citationFunctional genomics and the study of development, variation and evolution
White, K. P. (2001) · Nature Reviews Genetics · doi:10.1038/35080565 · Cited by 53 · see citing works
Using Parthenogenetic Lineages to Identify Advantages of Sex
Neiman, M., & Schwander, T. (2011) · Evolutionary Biology · doi:10.1007/s11692-011-9113-z · Cited by 52 · see citing works
“…of higher ploidy levels among old parthenogenetic lineages could instead be a consequence of harboring more targets ‘‘capable’’ of beneficial mutation (Paquin and Adams 1983; Otto and Whitton 2000) or genetic variance that may be beneficial in the face of environmental change (Bell 1982).”
BackgroundExperimental evolution with yeast
Zeyl, C. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00061.x · Cited by 52 · see citing works
Experimental Studies of Evolutionary Dynamics in Microbes
Cvijović, I., Ba, A. N. N., & Desai, M. M. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.06.004 · Cited by 50 · see citing works
“For example, one can construct yeast strains in which loss-of-function mutations in the gene CAN1 lead to resistance to the drug canavanine; the frequency of these mutations can then be precisely tracked by plating on media containing this drug [31].”
- Authors
- Paquin, C., & Adams, J.
- Affiliations
- University of Michigan (US)
- Venue
- Nature
- Published
- 1983-04
- Volume
- 302
- Issue
- 5908
- Pages
- 495-500
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2057017576
- Cited by
- 239
- References
- 55
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 25 · 2023: 4 · 2022: 5 · 2021: 5 · 2020: 4 · 2019: 4 · 2018: 6 · 2017: 10 · 2016: 6 · 2015: 9 · 2014: 11 · 2013: 9 · 2012: 8
- FWCI
- 2.10
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- Funders
- National Institute of General Medical Sciences (T32GM007544)
- 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
- adaptive mutation, fixation frequency, diploidy, haploid populations, Saccharomyces cerevisiae, yeast evolution, population genetics
- MeSH terms
- Adaptation, Biological, Diploidy, Biological Evolution, Gene Frequency, Haploidy, Mutation, Saccharomyces cerevisiae
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