Evolution of mutation rates in rapidly adapting asexual populations

Genetics

Volumn 204, Issue 3, 2016, Pages 1249-1266

  Good, Benjamin H ^a,b,c   Desai, Michael M ^a,b,c  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Antimutator; Deleterious load; Hitchhiking; Mutator

Indexed keywords

ALLELE; ARTICLE; ASEXUAL REPRODUCTION; CLONAL EVOLUTION; EPISTASIS; EVOLUTION; EVOLUTIONARY ADAPTATION; MICROBIAL POPULATION DYNAMICS; MUTATION RATE; MUTATIONAL ANALYSIS; NATURAL SELECTION; NONHUMAN; POPULATION SIZE; PRIORITY JOURNAL; ADAPTATION; BIOLOGICAL MODEL; GENETIC SELECTION; GENETICS; HAPLOIDY; MOLECULAR EVOLUTION;

ADAPTATION, PHYSIOLOGICAL; EVOLUTION, MOLECULAR; HAPLOIDY; MODELS, GENETIC; MUTATION RATE; REPRODUCTION, ASEXUAL; SELECTION, GENETIC;

EID: 84994885253     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.193565     Document Type: Article

References (81)

1. Andre, J.-B., and B. Godelle, 2006 The evolution of mutation rate in finite asexual populations. Genetics 172: 611–626.
2. Barroso-Batista, J., A. Sousa, M. Lourenço, M.-L. Bergman, J. Demengeot et al., 2014 The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLoS Genet. 10: e1004182.
3. Bjorkholm, B., M. Sjolund, P. G. Falk, O. G. Berg, L. Engstrand et al., 2001 Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc. Natl. Acad. Sci. USA 98: 14607–14612.
4. Chao, L., and E. C. Cox, 1983 Competition between high and low mutating strains of Escherichia coli. Evolution 37: 125–134.
5. Chao, L., C. Vargas, B. B. Spear, and E. C. Cox, 1983 Transposable elements as mutator genes in evolution. Nature 303: 633–635.
6. Charlesworth, B., 1994 The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63: 213–227.
7. Dawson, K. J., 1998 Evolutionarily stable mutation rates. J. Theor. Biol. 194: 147–157.
8. Dawson, K. J., 1999 The dynamics of infinitesimally rare alleles, applied to the evolution of mutation rates and the expression of deleterious mutations. Theor. Popul. Biol. 55: 1–22.
9. del Campo, R., M. I. Morosini, E. G. G. de la Pedrosa, A. Fenoll, C. Munoz-Almagro et al., 2005 Population structure, antimicrobial resistance, and mutation frequencies of Streptococcus pneumoniae isolates from cystic fibrosis patients. J. Clin. Microbiol. 43: 2207–2214.
10. Denamur, E., S. Bonacorsi, A. Giraud, P. Duriez, F. Hilali et al., 2002 High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J. Bacteriol. 184: 605–609.
11. Desai, M. M., and D. S. Fisher, 2007 Beneficial mutation selection balance and the effect of genetic linkage on positive selection. Genetics 176: 1759–1798.
12. Desai, M. M., and D. S. Fisher, 2011 The balance between mutators and nonmutators in asexual populations. Genetics 188: 997–1014.
13. Desai, M. M., D. S. Fisher, and A. W. Murray, 2007 The speed of evolution and the maintenance of variation in asexual populations. Curr. Biol. 17: 385–394.
14. Desai, M. M., A. M. Walczak, and D. S. Fisher, 2013 Genetic diversity and the structure of genealogies in rapidly adapting populations. Genetics 193: 565–585.
15. Fisher, D. S., 2007 Evolutionary dynamics, pp. 395–446. in Complex Systems, Vol. 85, edited by M. M. Jean-Philippe Bouchaud, and J. Dalibard. Elsevier, Les Houches.
16. Fisher, D. S., 2013 Asexual evolution waves: fluctuations and universality. J. Stat. Mech. 2013: P01011.
17. Gardiner, C., 1985 Handbook of Stochastic Methods. Springer, New York.
18. Gentile, C. F., S.-C. Yu, S. A. Serrano, P. J. Gerrish, and P. D. Sniegowski, 2011 Competition between high- and highermutating strains of Escherichia coli. Biol. Lett. 7: 422–424.
19. Gillespie, J. H., 1981 Mutation modification in a random environment. Evolution 35: 468–476.
20. Giraud, A., I. Matic, O. Tenaillon, A. Clara, M. Radman et al., 2001 Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291: 2606–2608.
21. Giraud, A., I. Matic, M. Radman, M. Fons, and F. Taddei, 2002 Mutator bacteria as a risk factor in treatment of infectious diseases. Antimicrob. Agents Chemother. 46: 863–865.
22. Good, B. H., and M. M. Desai, 2014 Deleterious passengers in adapting populations. Genetics 198: 1183–1208.
23. Good, B. H., and M. M. Desai, 2015 The impact of macroscopic epistasis on long-term evolutionary dynamics. Genetics 199: 177–190.
24. Good, B. H., I. M. Rouzine, D. J. Balick, O. Hallatschek, and M. M. Desai, 2012 Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations. Proc. Natl. Acad. Sci. USA 109: 4950–4955.
25. Good, B. H., A. M. Walczak, R. A. Neher, and M. M. Desai, 2014 Genetic diversity in the interference selection limit. PLoS Genet. 10: e1004222.
26. Hallatschek, O., 2011 The noisy edge of traveling waves. Proc. Natl. Acad. Sci. USA 108: 1783–1787.
27. Ishii, K., H. Matsuda, Y. Iawasa, and A. Sasaki, 1989 Evolutionarily stable mutation rate in a periodically changing environment. Genetics 121: 163–174.
28. James, A., and K. Jain, 2015 Fixation probability of rare nonmutator and evolution of mutation rates. Ecol. Evol. 6: 755–764.
29. Johnson, T., 1999a The approach to mutation-selection balance in an infinite asexual population, and the evolution of mutation rates. Proc. Biol. Sci. 266: 2389–2397.
30. Johnson, T., 1999b Beneficial mutations, hitchhiking and the evolution of mutation rates in sexual populations. Genetics 151: 1621–1631.
31. Kessler, D. A., and H. Levine, 1998 Mutator dynamics on a smooth evolutionary landscape. Phys. Rev. Lett. 80: 2012–2015.
32. Kimura, M., 1967 On the evolutionary adjustment of spontaneous mutation rates. Genet. Res. 9: 23–34.
33. Labat, F., O. Pradillon, L. Garry, M. Peuchmaur, B. Fantin et al., 2005 Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis. FEMS Immunol. Med. Microbiol. 44: 317–321.
34. LeClerc, J. E., B. G. Li, W. L. Payne, and T. A. Cebula, 1996 High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 1208–1211.
35. Lee, H., E. Popodi, H. Tanga, and P. L. Foster, 2012 Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc. Natl. Acad. Sci. USA 109: E2774–E2783.
36. Leigh, E. G., 1970 Natural selection and mutability. Am. Nat. 104: 301.
37. Leigh, E. G., 1973 The evolution of mutation rates. Genetics 73: 1–18.
38. Lenski, R. E., M. R. Rose, S. C. Simpson, and S. C. Tadler, 1991 Long-term experimental evolution in Escherichia coli. i. Adaptation and divergence during 2,000 generations. Am. Nat. 138: 1315–1341.
39. Lenski, R. E., M. J. Wiser, N. Ribeck, Z. D. Blount, J. R. Nahum et al., 2015 Sustained fitness gains and variability in fitness trajectories in the long-term evolution experiment with Escherichia coli. Proc. Biol. Sci. 282: 20152292.
40. Liberman, U., and M. W. Feldman, 1986 Modifiers of mutation rate: a general reduction principle. Theor. Popul. Biol. 30: 125–142.
41. Lynch, M., 2008 The cellular, developmental and populationgenetic determinants of mutation-rate evolution. Genetics 180: 933–943.
42. Lynch, M., 2011 The lower bound to the evolution of mutation rates. Genome Biol. Evol. 3: 1107–1118.
43. Matic, I., M. Radman, F. Taddei, B. Picard, C. Doit et al., 1997 Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277: 1833–1834.
44. McDonald, M. J., Y. Y. Hsieh, Y. H. Yu, S. L. Chang, and J. Y. Leu, 2012 The evolution of low mutation rates in experimental mutator populations of Saccharomyces cerevisiae. Curr. Biol. 22: 1235–1240.
45. McDonald, M. J., D. P. Rice, and M. M. Desai, 2016 Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531: 233–236.
46. Neher, R., and B. I. Shraiman, 2011 Genetic draft and quasineutrality in large facultatively sexual populations. Genetics 188: 975–976.
47. Neher, R., and B. I. Shraiman, 2012 Fluctuations of fitness distributions and the rate of Muller’s ratchet. Genetics 191: 1283–1293.
48. Neher, R., B. I. Shraiman, and D. S. Fisher, 2010 Rate of adaptation in large sexual populations. Genetics 184: 467–481.
49. Neher, R. A., T. A. Kessinger, and B. I. Shraiman, 2013 Coalescence and genetic diversity in sexual populations under selection. Proc. Natl. Acad. Sci. USA 110: 15836–15841.
50. Notley-McRobb, L., S. Seeto, and T. Ferenci, 2002 Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics 162: 1055–1062.
51. Oliver, A., R. Canton, P. Campo, F. Baquero, and J. Blazquez, 2000 High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251–1253.
52. Orr, H. A., 2000 The rate of adaptation in asexuals. Genetics 155: 961–968.
53. Painter, P. R., 1975 Mutator genes and selection for the mutation rate in bacteria. Genetics 79: 649–660.
54. Pal, C., M. D. Macia, A. Oliver, I. Schachar, and A. Buckling, 2007 Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450: 1079–1081.
55. Peck, J. R., 1994 A ruby in the rubbish. Genetics 137: 597–606.
56. Perfeito, L., L. Fernandes, C. Mota, and I. Gordo, 2007 Adaptive mutations in bacteria: high rate and small effects. Science 317: 813.
57. Prunier, A. L., B. Malbruny, M. Laurans, J. Brouard, J. F. Duhamel et al., 2003 High rate of macrolide resistance in Staphylococcus aureus strains from patients with cystic fibrosis reveals high proportions of hypermutable strains. J. Infect. Dis. 187: 1709–1716.
58. Richardson, A. R., Z. Yu, T. Popovic, and I. Stojiljkovic, 2002 Mutator clones of neisseria meningitidis in epidemic serogroup a disease. Proc. Natl. Acad. Sci. USA 99: 6103–6107.
59. Rouzine, I. M., J. Wakeley, and J. M. Coffin, 2003 The solitary wave of asexual evolution. Proc. Natl. Acad. Sci. USA 100: 587–592.
60. Shaver, A. C., P. G. Dombrowski, J. Y. Sweeney, T. Treis, R. M. Zappala et al., 2002 Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 162: 557–566.
61. Sniegowski, P. D., P. J. Gerrish, and R. E. Lenski, 1997 Evolution of high mutation rates in experimental populations of E. coli. Nature 387: 703–705.
62. Soderberg, R. J., and O. G. Berg, 2011 Kick-starting the ratchet: the fate of mutators in asexual populations. Genetics 197: 1129–1137.
63. Taddei, F., M. Radman, J. Maynard-Smith, B. Toupance, P. H. Gouyon et al., 1997 Role of mutator alleles in adaptive evolution. Nature 387: 700–702.
64. Tanaka, M. M., C. T. Bergstrom, and B. R. Levin, 2003 The evolution of mutator genes in bacterial populations: the roles of environmental change and timing. Genetics 164: 843–854.
65. Tenaillon, O., B. Toupance, H. L. Nagard, F. Taddei, and B. Godelle, 1999 Mutators, population size, adaptive landscape, and the adaptation of asexual populations of bacteria. Genetics 152: 485–493.
66. Tenaillon, O., H. L. Nagard, B. Godelle, and F. Taddei, 2000 Mutators and sex in bacteria: conflict between adaptive strategies. Proc. Natl. Acad. Sci. USA 97: 10465–10470.
67. Thompson, D. A., M. M. Desai, and A. W. Murray, 2006 Ploidy controls the success of mutators and nature of mutations during budding yeast evolution. Curr. Biol. 16: 1581–1590.
68. Travis, J., and E. Travis, 2002 Mutator dynamics in fluctuating environments. Proc. Biol. Sci. 269: 591–597.
69. Tröbner, W., and R. Piechocki, 1981 Competition growth between Escherichia coli mutL and mut+ in continuously growing cultures. Z. Allg. Mikrobiol. 21: 347–349.
70. Tröbner, W., and R. Piechocki, 1984 Selection against hypermutability in Escherichia coli during long term evolution. Mol. Gen. Genet. 198: 177–178.
71. Tsimring, L., H. Levine, and D. Kessler, 1996 RNA virus evolution via a fitness-space model. Phys. Rev. Lett. 90: 088103.
72. Turrientes, M.-C., F. Baquero, B. R. Levin, J.-L. Martinez, A. Ripoll et al., 2013 Normal mutation rate variants arise in a mutator (mut s) Escherichia coli population. PLoS One 8: e72963.
73. Voordeckers, K., J. Kominek, A. Das, A. Espinosa-Cantú, D. D. Maeyer et al., 2015 Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet. 11: e1005635.
74. Watson, M. E., J. L. Burns, and A. L. Smith, 2004 Hypermutable haemophilus influenzae with mutations in muts are found in cystic fibrosis sputum. Microbiol. Sgm. 150: 2947–2958.
75. Weissman, D., and O. Hallatschek, 2014 The rate of adaptation in large sexual populations with linear chromosomes. Genetics 196: 1167–1183.
76. Weissman, D. W., M. M. Desai, D. S. Fisher, and M. W. Feldman, 2009 The rate at which asexual populations cross fitness valleys. Theor. Popul. Biol. 75: 286–300.
77. Wielgoss, S., J. E. Barrick, O. Tenaillon, S. Cruveiller, B. ChaneWoon-Ming et al., 2011 Mutation rate inferred from synonymous substitutions in a long-term evolution experiment with Escherichia coli. G3 (Bethesda) 1: 183–186.
78. Wielgoss, S., J. E. Barrick, O. Tenaillon, M. J. Wiser, J. Dittmar et al., 2013 Mutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load. Proc. Natl. Acad. Sci. USA 110: 222–227.
79. Wiser, M. J., N. Ribeck, and R. E. Lenski, 2013 Long-term dynamics of adaptation in asexual populations. Science 342: 1364– 1367.
80. Wloch, D. M., K. Szafraniec, R. H. Borts, and R. Korona, 2001 Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics 159: 441–452.
81. Wylie, C. S., C.-M. Ghim, D. Kessler, and H. Levine, 2009 The fixation probability of rare mutators in finite asexual populations. Genetics 181: 1595–1612.