Abstract
Adaptive evolution navigates a balance between chance and determinism. The stochastic processes of mutation and drift generate phenotypic variation; however, once mutations reach an appreciable frequency in the population, their fate is governed by the deterministic action of selection, enriching for favorable genotypes and purging the less-favorable ones. The net result is that replicate populations will traverse similar—but not identical—pathways to higher fitness. This parallelism in evolutionary outcomes can be leveraged to identify the genes and pathways under selection. However, distinguishing between beneficial and neutral mutations is challenging because many beneficial mutations will be lost due to drift and clonal interference, and many neutral (and even deleterious) mutations will fix by hitchhiking. Here, we review the best practices that our laboratory uses to identify genetic targets of selection from next-generation sequencing data of evolved yeast populations. The general principles for identifying the mutations driving adaptation will apply more broadly.
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References
Aggeli D, Marad DA, Liu X, Buskirk SW, Levy SF, Lang GI (2022) Overdominant and partially dominant mutations drive clonal adaptation in diploid Saccharomyces cerevisiae. Genetics 221(2):iyac061
Arjan GJ, Visser Md, Zeyl CW, Gerrish PJ, Blanchard JL, Lenski RE (1999) Diminishing returns from mutation supply rate in asexual populations. Science 283(5400):404–406
Atwood KC, Schneider LK, Ryan FJ (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci 37(3):146–155
Bailey SF, Bataillon T (2016) Can the experimental evolution programme help us elucidate the genetic basis of adaptation in nature? Mol Ecol 25(1):203–218
Bailey SF, Rodrigue N, Kassen R (2015) The effect of selection environment on the probability of parallel evolution. Mol Biol Evol 32(6):1436–1448
Bailey SF, Blanquart F, Bataillon T, Kassen R (2017) What drives parallel evolution? How population size and mutational variation contribute to repeated evolution. BioEssays 39(1):1–9
Bailey SF, Alonso Morales LA, Kassen R (2021) Effects of synonymous mutations beyond codon bias: the evidence for adaptive synonymous substitutions from microbial evolution experiments. Genome Biol Evol 13(9):evab141
Bajić D, Vila JC, Blount ZD, Sánchez A (2018) On the deformability of an empirical fitness landscape by microbial evolution. Proc Natl Acad Sci 115(44):11286–11291
Barrett RD, MacLean RC, Bell G (2005) Experimental evolution of Pseudomonas fluorescens in simple and complex environments. Am Nat 166(4):470–480
Barrick JE, Lenski RE (2013) Genome dynamics during experimental evolution. Nat Rev Genet 14(12):827–839
Barrick JE, Kauth MR, Strelioff CC, Lenski RE (2010) Escherichia coli rpoB mutants have increased evolvability in proportion to their fitness defects. Mol Biol Evol 27(6):1338–1347
Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM, Kishony R (2015) Inexpensive multiplexed library preparation for megabase-sized genomes. PLoS ONE 10(5):e0128036
Behringer MG, Choi BI, Miller SF, Doak TG, Karty JA, Guo W, Lynch M (2018) Escherichia coli cultures maintain stable subpopulation structure during long-term evolution. Proc Natl Acad Sci 115(20):E4642–E4650
Blount ZD, Barrick JE, Davidson CJ, Lenski RE (2012) Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489(7417):513–518
Blundell JR, Schwartz K, Francois D, Fisher DS, Sherlock G, Levy SF (2019) The dynamics of adaptive genetic diversity during the early stages of clonal evolution. Nat Ecol Evol 3(2):293–301
Boeva V, Popova T, Bleakley K, Chiche P, Cappo J, Schleiermacher G, Janoueix-Lerosey I, Delattre O, Barillot E (2012) Control-FREEC: a tool for assessing copy number and allelic content using next-generation sequencing data. Bioinformatics 28(3):423–425
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
Bull J, Badgett M, Wichman HA, Huelsenbeck JP, Hillis DM, Gulati A, Ho C, Molineux I (1997) Exceptional convergent evolution in a virus. Genetics 147(4):1497–1507
Burke MK, Dunham JP, Shahrestani P, Thornton KR, Rose MR, Long AD (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467(7315):587–590
Buskirk SW, Peace RE, Lang GI (2017) Hitchhiking and epistasis give rise to cohort dynamics in adapting populations. Proc Natl Acad Sci 114(31):8330–8335
Chou H-H, Chiu H-C, Delaney NF, Segrè D, Marx CJ (2011) Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332(6034):1190–1192
Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6(2):80–92
Cisneros-Mayoral S, Graña-Miraglia L, Pérez-Morales D, Peña-Miller R, Fuentes-Hernández A (2022) Evolutionary history and strength of selection determine the rate of antibiotic resistance adaptation. Mol Biol Evol 39(9):msac185
Cooper VS (2018) Experimental evolution as a high-throughput screen for genetic adaptations. mSphere 3(3):e00121-00118
Cooper VS, Schneider D, Blot M, Lenski RE (2001) Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol 183(9):2834–2841
Cowen LE, Sanglard D, Calabrese D, Sirjusingh C, Anderson JB, Kohn LM (2000) Evolution of drug resistance in experimental populations of Candida albicans. J Bacteriol 182(6):1515–1522
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158
Deatherage DE, Barrick JE (2021) High-throughput characterization of mutations in genes that drive clonal evolution using multiplex adaptome capture sequencing. Cell Syst 12(12):1187–1200
Deatherage DE, Kepner JL, Bennett AF, Lenski RE, Barrick JE (2017) Specificity of genome evolution in experimental populations of Escherichia coli evolved at different temperatures. Proc Natl Acad Sci 114(10):E1904–E1912
DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM (2013) Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41(7):4336–4343
Dutta A, Dutreux F, Schacherer J (2021) Loss of heterozygosity results in rapid but variable genome homogenization across yeast genetic backgrounds. Elife 10:e70339
Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4(6):457–469
Elena SF, Cooper VS, Lenski RE (1996) Punctuated evolution caused by selection of rare beneficial mutations. Science 272(5269):1802–1804
Eyre-Walker A, Keightley PD (2007) The distribution of fitness effects of new mutations. Nat Rev Genet 8(8):610–618
Ferea TL, Botstein D, Brown PO, Rosenzweig RF (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci 96(17):9721–9726
Fisher KJ, Buskirk SW, Vignogna RC, Marad DA, Lang GI (2018) Adaptive genome duplication affects patterns of molecular evolution in Saccharomyces cerevisiae. PLoS Genet 14(5):e1007396
Fisher KJ, Kryazhimskiy S, Lang GI (2019) Detecting genetic interactions using parallel evolution in experimental populations. Philos Trans R Soc B 374(1777):20180237
Fisher KJ, Vignogna RC, Lang GI (2021) Overdominant mutations restrict adaptive loss of heterozygosity at linked loci. Genome Biol Evol 13(8):evab181
Foster PL, Lee H, Popodi E, Townes JP, Tang H (2015) Determinants of spontaneous mutation in the bacterium <i>Escherichia coli</i> as revealed by whole-genome sequencing. Proc Natl Acad Sci 112(44):E5990–E5999
Foster PL, Niccum BA, Popodi E, Townes JP, Lee H, MohammedIsmail W, Tang H (2018) Determinants of base-pair substitution patterns revealed by whole-genome sequencing of dna mismatch repair defective Escherichia coli. Genetics 209(4):1029–1042
Frenkel EM, McDonald MJ, Van Dyken JD, Kosheleva K, Lang GI, Desai MM (2015) Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations. Proc Natl Acad Sci 112(36):11306–11311
Garrison E, Marth G (2012) Haplotype-based variant detection from short-read sequencing. arXiv preprint arXiv:1207.3907
Gerrish PJ, Lenski RE (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102–103(1–6):127–144
Gerstein A, Cleathero L, Mandegar M, Otto S (2011) Haploids adapt faster than diploids across a range of environments. J Evol Biol 24(3):531–540
Gerstein A, Kuzmin A, Otto S (2014) Loss-of-heterozygosity facilitates passage through Haldane’s sieve for Saccharomyces cerevisiae undergoing adaptation. Nat Commun 5(1):1–9
Giaever G, Chu AM, Ni L, et al (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391. https://doi.org/10.1038/nature00935
Good BH, McDonald MJ, Barrick JE, Lenski RE, Desai MM (2017) The dynamics of molecular evolution over 60,000 generations. Nature 551(7678):45–50
Gorkovskiy A, Verstrepen KJ (2021) The role of structural variation in adaptation and evolution of yeast and other fungi. Genes 12(5):699
Grant PR, Grant BR, Markert JA, Keller LF, Petren K (2004) Convergent evolution of Darwin’s finches caused by introgressive hybridization and selection. Evolution 58(7):1588–1599
Hallsworth JE (2018) Stress-free microbes lack vitality. Fungal Biol 122(6):379–385
Harcombe W, Springman R, Bull J (2009) Compensatory evolution for a gene deletion is not limited to its immediate functional network. BMC Evol Biol 9(1):1–11
Harris KB, Flynn KM, Cooper VS (2021) Polygenic adaptation and clonal interference enable sustained diversity in experimental Pseudomonas aeruginosa populations. Mol Biol Evol 38(12):5359–5375
Hegreness M, Shoresh N, Hartl D, Kishony R (2006) An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 311(5767):1615–1617
Helsen J, Voordeckers K, Vanderwaeren L, Santermans T, Tsontaki M, Verstrepen KJ, Jelier R (2020) Gene loss predictably drives evolutionary adaptation. Mol Biol Evol 37(10):2989–3002
Hershberg R, Petrov DA (2008) Selection on codon bias. Annu Rev Genet 42:287–299
Jagdish T, Ba ANN (2022) Microbial experimental evolution in a massively multiplexed and high-throughput era. Curr Opin Genet Dev 75:101943
James TY, Michelotti LA, Glasco AD, Clemons RA, Powers RA, James ES, Simmons DR, Bai F, Ge S (2019) Adaptation by loss of heterozygosity in Saccharomyces cerevisiae clones under divergent selection. Genetics 213(2):665–683
Jerison ER, Kryazhimskiy S, Mitchell JK, Bloom JS, Kruglyak L, Desai MM (2017) Genetic variation in adaptability and pleiotropy in budding yeast. Elife 6:e27167
Johnson MS, Gopalakrishnan S, Goyal J, Dillingham ME, Bakerlee CW, Humphrey PT, Jagdish T, Jerison ER, Kosheleva K, Lawrence KR (2021) Phenotypic and molecular evolution across 10,000 generations in laboratory budding yeast populations. Elife 10:e63910
Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484(7392):55–61
Joseph SB, Hall DW (2004) Spontaneous mutations in diploid Saccharomyces cerevisiae: more beneficial than expected. Genetics 168(4):1817–1825
Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC (2012) Experimental evolution. Trends Ecol Evol 27(10):547–560
Kerr B, Neuhauser C, Bohannan BJ, Dean AM (2006) Local migration promotes competitive restraint in a host–pathogen’tragedy of the commons’. Nature 442(7098):75–78
Khan AI, Dinh DM, Schneider D, Lenski RE, Cooper TF (2011) Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332(6034):1193–1196
Kinsler G, Schmidlin K, Newell D, Eder R, Apodaca S, Petrov D, Geiler-Samerotte K (2023) Extreme sensitivity of fitness to environmental conditions; lessons from #1BigBatch. J Mol Evol. https://doi.org/10.1101/2022.08.25.505320
Kryazhimskiy S, Rice DP, Jerison ER, Desai MM (2014) Global epistasis makes adaptation predictable despite sequence-level stochasticity. Science 344(6191):1519–1522
Laan L, Koschwanez JH, Murray AW (2015) Evolutionary adaptation after crippling cell polarization follows reproducible trajectories. Elife 4:e09638
LaBar T, Hsieh Y-YP, Fumasoni M, Murray AW (2020) Evolutionary repair experiments as a window to the molecular diversity of life. Curr Biol 30(10):R565–R574
Lang GI, Murray AW (2011) Mutation rates across budding yeast chromosome VI are correlated with replication timing. Genome Biol Evol 3:799–811
Lang GI, Murray AW, Botstein D (2009) The cost of gene expression underlies a fitness trade-off in yeast. Proc Natl Acad Sci 106(14):5755–5760
Lang GI, Botstein D, Desai MM (2011) Genetic variation and the fate of beneficial mutations in asexual populations. Genetics 188(3):647–661
Lang GI, Parsons L, Gammie AE (2013) Mutation rates, spectra, and genome-wide distribution of spontaneous mutations in mismatch repair deficient yeast. G3 (Bethesda) 3(9):1453–1465
Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, Botstein D, Desai MM (2013b) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500(7464):571–574
Lenski RE, Rose MR, Simpson SC, Tadler SC (1991) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138(6):1315–1341
Lenski RE (2023) Revisiting the design of the long-term evolution experiment with Escherichia coli. J Mol Evol. https://doi.org/10.1007/s00239-023-10095-3
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754–1760
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP (2009) The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25(16):2078–2079
Maddamsetti R, Hatcher PJ, Green AG, Williams BL, Marks DS, Lenski RE (2017) Core genes evolve rapidly in the long-term evolution experiment with Escherichia coli. Genome Biol Evol 9(4):1072–1083
Marad DA, Buskirk SW, Lang GI (2018) Altered access to beneficial mutations slows adaptation and biases fixed mutations in diploids. Nat Ecol Evol 2(5):882–889
Martínez AA, Conboy A, Buskirk SW, Marad DA, Lang GI (2022) Long-term adaptation to galactose as a sole carbon source selects for mutations in nutrient signaling pathways. biorxiv. https://doi.org/10.1101/2022.05.17.492354
McDonald MJ (2019) Microbial experimental evolution–a proving ground for evolutionary theory and a tool for discovery. EMBO Rep 20(8):e46992
McDonald MJ, Gehrig SM, Meintjes PL, Zhang X-X, Rainey PB (2009) Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183(3):1041–1053
McDonald MJ, Hsieh Y-Y, Yu Y-H, Chang S-L, Leu J-Y (2012) The evolution of low mutation rates in experimental mutator populations of Saccharomyces cerevisiae. Curr Biol 22(13):1235–1240
Miller AW, Befort C, Kerr EO, Dunham MJ (2013) Design and use of multiplexed chemostat arrays. JoVE 72:e50262
Paquin C, Adams J (1983) Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302(5908):495–500
Payen C, Dunham MJ (2016) Experimental evolution and resequencing analysis of yeast. Yeast functional genomics. Springer, Berlin, pp 361–374
Perfeito L, Fernandes L, Mota C, Gordo I (2007) Adaptive mutations in bacteria: high rate and small effects. Science 317(5839):813–815
Philippe N, Pelosi L, Lenski RE, Schneider D (2009) Evolution of penicillin-binding protein 2 concentration and cell shape during a long-term experiment with Escherichia coli. J Bacteriol 191(3):909–921
Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38(1):107–111
Quandt EM, Deatherage DE, Ellington AD, Georgiou G, Barrick JE (2014) Recursive genomewide recombination and sequencing reveals a key refinement step in the evolution of a metabolic innovation in Escherichia coli. Proc Natl Acad Sci 111(6):2217–2222
Quandt EM, Gollihar J, Blount ZD, Ellington AD, Georgiou G, Barrick JE (2015) Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment. Elife 4:e09696
Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394(6688):69–72
Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29(1):24–26
Rojas Echenique JI, Kryazhimskiy S, Nguyen Ba AN, Desai MM (2019) Modular epistasis and the compensatory evolution of gene deletion mutants. PLoS Genet 15(2):e1007958
Rose MR, Vu LN, Park SU, Graves JL Jr (1992) Selection on stress resistance increases longevity in Drosophila melanogaster. Exp Gerontol 27(2):241–250
Sadhu MJ, Bloom JS, Day L, Siegel JJ, Kosuri S, Kruglyak L (2018) Highly parallel genome variant engineering with CRISPR-Cas9. Nat Genet 50(4):510–514
Sane M, Diwan GD, Bhat BA, Wahl LM, Agashe D (2022) Shifts in mutation spectra enhance access to beneficial mutations. biorxiv. https://doi.org/10.1101/2020.09.05.284158
Sharon E, Chen SA, Khosla NM, Smith JD, Pritchard JK, Fraser HB (2018) Functional genetic variants revealed by massively parallel precise genome editing. Cell 175(2):544–557
Sharp NP, Sandell L, James CG, Otto SP (2018) The genome-wide rate and spectrum of spontaneous mutations differ between haploid and diploid yeast. Proc Natl Acad Sci 115(22):E5046–E5055
Shen JP, Zhao D, Sasik R, Luebeck J, Birmingham A, Bojorquez-Gomez A, Licon K, Klepper K, Pekin D, Beckett AN, Sanchez KS, Thomas A, Kuo CC, Du D, Roguev A, Lewis NE, Chang AN, Kreisberg JF, Krogan N, Qi L, Ideker T, Mali P (2017) Combinatorial CRISPR-Cas9 screens for de novo mapping of genetic interactions. Nat Methods 14(6):573–576
Shoemaker WR, Lennon JT (2022) Predicting parallelism and quantifying divergence in microbial evolution experiments. Msphere 7(1):e00672-e621
Smukowski Heil CS, DeSevo CG, Pai DA, Tucker CM, Hoang ML, Dunham MJ (2017) Loss of heterozygosity drives adaptation in hybrid yeast. Mol Biol Evol 34(7):1596–1612
Smukowski Heil CS (2023) Loss of heterozygosity and its importance in genome evolution. J Mol Evol. https://doi.org/10.1007/s00239-022-10088-8
Spealman P, De T, Chuong J, Gresham D (2023) Best practices in microbial experimental evolution: using reporters and long read sequencing to identify copy number variation in experimental evolution. J Mol Evol (in press)
Szamecz B, Boross G, Kalapis D, Kovács K, Fekete G, Farkas Z, Lázár V, Hrtyan M, Kemmeren P, Groot Koerkamp MJ (2014) The genomic landscape of compensatory evolution. PLoS Biol 12(8):e1001935
Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon P-H, Godelle B (1997) Role of mutator alleles in adaptive evolution. Nature 387(6634):700–702
Tenaillon O, Rodríguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, Gaut BS (2012) The molecular diversity of adaptive convergence. Science 335(6067):457–461
Tenaillon O, Barrick JE, Ribeck N, Deatherage DE, Blanchard JL, Dasgupta A, Wu GC, Wielgoss S, Cruveiller S, Médigue C (2016) Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 536(7615):165–170
Thompson DA, Desai MM, Murray AW (2006) Ploidy controls the success of mutators and nature of mutations during budding yeast evolution. Curr Biol 16(16):1581–1590
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14(2):178–192
Tuffaha M, Varakunan S, Castellano D, Gutenkunst RN, Wahl LM (2022) Shifts in mutation bias promote mutators by altering the distribution of fitness effects. biorxiv. https://doi.org/10.1101/2022.09.27.509708
Tung S, Bakerlee CW, Phillips AM, Nguyen Ba AN, Desai MM (2021) The genetic basis of differential autodiploidization in evolving yeast populations. G3 11(8):jkab192
Turner CB, Marshall CW, Cooper VS (2018) Parallel genetic adaptation across environments differing in mode of growth or resource availability. Evol Lett 2(4):355–367
Van den Bergh B, Swings T, Fauvart M, Michiels J (2018) Experimental design, population dynamics, and diversity in microbial experimental evolution. Microbiol Mol Biol Rev 82(3):e00008-00018
Velicer GJ, Kroos L, Lenski RE (1998) Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc Natl Acad Sci 95(21):12376–12380
Venkataram S, Dunn B, Li Y, Agarwala A, Chang J, Ebel ER, Geiler-Samerotte K, Herissant L, Blundell JR, Levy SF, Fisher DS, Sherlock G, Petrov DA (2016) Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast. Cell 166(6):1585–1596
Vignogna RC, Allocca M, Monticelli M, Norris JW, Steet R, Perlstein EO, Andreotti G, Lang GI (2022) Evolutionary rescue of phosphomannomutase deficiency in yeast models of human disease. eLife 11:e79346
Wichman H, Badgett M, Scott L, Boulianne C, Bull J (1999) Different trajectories of parallel evolution during viral adaptation. Science 285(5426):422–424
Wiser MJ, Lenski RE (2015) A comparison of methods to measure fitness in Escherichia coli. PLoS ONE 10(5):e0126210
Wiser MJ, Ribeck N, Lenski RE (2013) Long-term dynamics of adaptation in asexual populations. Science 342(6164):1364–1367
Worthan SB, McCarthy RDP, Behringer MG (2023) Case studies in the assessment of microbial fitness: seemingly subtle changes can have major effects on phenotypic outcomes. J Mol Evol. https://doi.org/10.1007/s00239-022-10087-9
Zhang H, Zeidler AF, Song W, Puccia CM, Malc E, Greenwell PW, Mieczkowski PA, Petes TD, Argueso JL (2013) Gene copy-number variation in haploid and diploid strains of the yeast Saccharomyces cerevisiae. Genetics 193(3):785–801
Zhu YO, Siegal ML, Hall DW, Petrov DA (2014) Precise estimates of mutation rate and spectrum in yeast. Proc Natl Acad Sci 111(22):E2310–E2318
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We thank Dimitra Aggeli for comments on the manuscript. This study was supported by the National Institutes of Health: R01GM127420.
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The National Institute of General Medical Sciences, R01GM127420, Gregory Lang.
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Martínez, A.A., Lang, G.I. Identifying Targets of Selection in Laboratory Evolution Experiments. J Mol Evol 91, 345–355 (2023). https://doi.org/10.1007/s00239-023-10096-2
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DOI: https://doi.org/10.1007/s00239-023-10096-2