New insights into bacterial adaptation through in vivo and in silico experimental evolution

Nature Reviews Microbiology

Volumn 10, Issue 5, 2012, Pages 352-365

  Hindré, Thomas ^a,b   Knibbe, Carole ^c,d   Beslon, Guillaume ^c,e   Schneider, Dominique ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITÉ LYON 1   (France)

^e UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE; FACTOR FOR INVERSION STIMULATION; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RNA DIRECTED RNA POLYMERASE;

BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM; BIOCHEMISTRY; BURKHOLDERIA; CELL SIZE; CELL STRUCTURE; COMMENSALISM; COMPUTER MODEL; DNA MODIFICATION; DNA REPAIR; DROSOPHILA MELANOGASTER; ECOLOGY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; GENE REGULATORY NETWORK; GENE SEQUENCE; GENE TARGETING; IN VIVO STUDY; MOLECULAR BIOLOGY; MYXOCOCCUS XANTHUS; NONHUMAN; OPERON; PARASITISM; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; PROTEOMICS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; RALSTONIA SOLANACEARUM; REVIEW; SACCHAROMYCES CEREVISIAE; SALMONELLA ENTERICA; SYMBIOSIS;

ADAPTATION, BIOLOGICAL; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOLOGICAL EVOLUTION; COMPUTATIONAL BIOLOGY; MICROBIOLOGICAL TECHNIQUES;

BACTERIA (MICROORGANISMS);

EID: 84859899271     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro2750     Document Type: Review

References (158)

1. Gould, S. J. The evolution of life on the earth. Sci. Am. 271, 84-91 (1994).
2. Elena, S. F. & Lenski, R. E. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Rev. Genet. 4, 457-469 (2003).
3. Adami, C. Digital genetics: unravelling the genetic basis of evolution. Nature Rev. Genet. 7, 109-118 (2006). An introduction to the general principles of digital genetics and to the Avida framework, and a presentation of the main experiments that have been conducted using this framework.
4. Buckling, A., MacLean, R. C., Brockhurst, M. A. & Colegrave, N. The Beagle in a bottle. Nature 457, 824-829 (2009).
5. Philippe, N., Crozat, E., Lenski, R. E. & Schneider, D. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. BioEssays 29, 846-860 (2007).
6. Brockhurst, M. A., Colegrave, N. & Rozen, D. E. Next-generation sequencing as a tool to study microbial evolution. Mol. Ecol. 20, 972-980 (2011).
7. Conrad, T. M., Lewis, N. E. & Palsson, B. O. Microbial laboratory evolution in the era of genome-scale science. Mol. Syst. Biol. 7, 509 (2011).
8. Bull, J. J. & Molineux, I. J. Predicting evolution from genomics: experimental evolution of bacteriophage T7. Heredity 100, 453-463 (2008).
9. Elena, S. F. et al. Experimental evolution of plant RNA viruses. Heredity 100, 478-483 (2008).
10. Burke, M. K. et al. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467, 587-590 (2010).
11. Darwin, C. On the Origin of Species by Means of Natural Selection (Murray, London, 1859).
12. Lenski, R. E. Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant. Breed. Rev. 24, 225-265 (2004).
13. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315-1341 (1991).
14. Helling, R. B., Vargas, C. N. & Adams, J. Evolution of Escherichia coli during growth in a constant environment. Genetics 116, 349-358 (1987).
15. Ferenci, T. Bacterial physiology, regulation and mutational adaptation in a chemostat environment. Adv. Microb. Physiol. 53, 169-229 (2008).
16. Gresham, D. et al. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4, e1000303 (2008).
17. Ferea, T. L., Botstein, D., Brown, P. O. & Rosenzweig, R. F. Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc. Natl Acad. Sci. USA 96, 9721-9726 (1999).
18. Cooper, T. F. & Lenski, R. E. Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evol. Biol. 10, 11 (2010).
19. Velicer, G. J. & Vos, M. Sociobiology of the myxobacteria. Annu. Rev. Microbiol. 63, 599-623 (2009). A review describing the ease of the evolution (back and forth) of social behavioural traits.
20. Velicer, G. J., Kroos, L. & Lenski, R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376-12380 (1998).
21. Velicer, G. J. & Yu, Y-T. N. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425, 75-78 (2003).
22. Fiegna, F., Yu, Y. T. N., Kadam, S. V. & Velicer, G. J. Evolution of an obligate social cheater to a superior cooperator. Nature 441, 310-314 (2006).
23. Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69-72 (1998). An evolution experiment showing fast radiation involving phenotypic innovation to colonize a new ecological niche.
24. McDonald, M. J., Gehrig, S. M., Meintjes, P. L., Zhang, X.-X. & Rainey, P. B. Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183, 1041-1053 (2009).
25. Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024-1027 (2004).
26. Marchetti, M. et al. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8, e1000280 (2010).
27. Zeyl, C. Experimental evolution with yeast. FEMS Yeast Res. 6, 685-691 (2006).
28. Nilsson, A. I. et al. Bacterial genome size reduction by experimental evolution. Proc. Natl Acad. Sci. USA 102, 12112-12116 (2005).
29. Lind, P. A. & Andersson, D. I. Whole-genome mutational biases in bacteria. Proc. Natl Acad. Sci. USA 105, 17878-17883 (2008).
30. De Visser, J. A. G. M. et al. Perspective: evolution and detection of genetic robustness. Evolution 57, 1959-1972 (2003).
31. Fong, S. S., Nanchen, A., Palsson, B. O. & Sauer, U. Latent pathway activation and increased pathway capacity enable Escherichia coli adaptation to loss of key metabolic enzymes. J. Biol. Chem. 281, 8024-8033 (2006).
32. Stoebel, D. M., Hokamp, K., Last, M. S. & Dorman, C. J. Compensatory evolution of gene regulation in response to stress by Escherichia coli lacking RpoS. PLoS Genet. 5, e1000671 (2009).
33. Charusanti, P. et al. Genetic basis of growth adaptation of Escherichia coli after deletion of pgi, a major metabolic gene. PLoS Genet. 6, e1001186 (2010).
34. Auriol, C., Bestel-Corre, G., Claude, J.-B., Soucaille, P. & Meynial-Salles, I. Stress-induced evolution of Escherichia coli points to original concepts in respiratory factor selectivity. Proc. Natl Acad. Sci. USA 108, 1278-1283 (2011).
35. Stern, S., Dror, T., Stolovicki, E., Brenner, N. & Braun, E. Genome-wide transcriptional plasticity underlies cellular adaptation to novel challenge. Mol. Syst. Biol. 3, 1-9 (2007).
36. Floreano, D. & Mattiussi, C. Bio-Inspired Artificial Intelligence Theories, Methods, and Technologies (Massachusetts Institute of Technology Press, Cambridge, Massachusetts, 2008).
37. Smith, J. M. Byte-sized evolution. Nature 355, 772-773 (1992).
38. Ray, T. S. in Artificial Life II. Santa Fe Institute Studies in the Sciences of Complexity Vol. X (eds Langton, C. G., Taylor, C., Farmer, J. D. & Rasmussen, S.) 371-408 (Addison Wesley, Redwood City, California,1991). The seminal work that initiated the field of in silico evolution, describing the Tierra framework, in which complex host-parasite interactions emerge spontaneously.
39. Clarke, P. H. Experiments in microbial evolution: new enzymes, new metabolic activities. Proc. R. Soc. Lond. B 207, 385-404 (1980).
40. Mortlock, R. P. Microorganisms as Model Systems for Studying Evolution (Springer, New York, 1984).
41. Clarke, P. H. & Drew, R. An experiment in enzyme evolution. Studies with Pseudomonas aeruginosa amidase. Biosci. Rep. 8, 103-120 (1988).
42. Dykhuizen, D. E. Experimental studies of natural selection in bacteria. Annu. Rev. Ecol. Syst. 21, 373-398 (1990).
43. Dykhuizen, D. E. & Dean, A. M. Enzyme activity and fitness: evolution in solution. Trends Ecol. Evol. 5, 257-262 (1990).
44. Philippe, N., Pelosi, L., Lenski, R. E. & Schneider, D. Evolution of penicillin-binding protein 2 concentration and cell shape during a long-term experiment with Escherichia coli. J. Bacteriol. 191, 909-921 (2009).
45. Fong, S. S., Joyce, A. R. & Palsson, B. O. Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Genome Res. 15, 1365-1372 (2005).
46. Cooper, T. F., Remold, S. K., Lenski, R. E. & Schneider, D. Expression profiles reveal parallel evolution of epistatic interactions involving the CRP regulon in Escherichia coli. PLoS Genet. 4, e35 (2008). An example of evolution through changes in epistatic interactions inside regulatory networks.
47. Conrad, T. M. et al. RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media. Proc. Natl Acad. Sci. USA 107, 20500-20505 (2010). An example of evolution towards new kinetic properties of the transcriptional machinery to confer higher fitness in minimal media.
48. Finkel, S. E. & Kolter, R. Evolution of microbial diversity during prolonged starvation. Proc. Natl Acad. Sci. USA 96, 4023-4027 (1999).
49. Hugues, B. S., Cullum, A. J. & Bennett, A. F. Evolutionary adaptation to environmental pH in experimental lineages of Escherichia coli. Evolution 61, 1725-1734 (2007).
50. Harris, D. R. et al. Directed evolution of ionizing radiation resistance in Escherichia coli. J. Bacteriol. 191, 5240-5252 (2009).
51. Ferenci, T. Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol. Microbiol. 57, 1-8 (2005).
52. Toprak, E. et al. Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nature Genet. 44, 101-106 (2012).
53. Zhang, Q. et al. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333, 1764-1767 (2011).
54. Spiers, A. J., Kahn, S. G., Bohannon, J., Travisano, M. & Rainey, P. B. Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161, 33-46 (2002).
55. MacLean, R. C. & Bell, G. Experimental adaptive radiation in Pseudomonas. Am. Nat. 160, 569-581 (2002).
56. Lee, D. H. & Palsson, B. Ø. Adaptive evolution of Escherichia coli K-12 MG1655 during growth on a nonnative carbon source, L-1,2-propanediol. Appl. Environ. Microbiol. 76, 4158-4168 (2010).
57. Lenski, R. E. & Bennett, A. F. Evolutionary response of Escherichia coli to thermal stress. Am. Nat. 142, S47-S64 (1993).
58. Leroi, A. M., Bennett, A. F. & Lenski, R. E. Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc. Natl Acad. Sci. USA 91, 1917-1921 (1994).
59. Blount, Z. D., Borland, C. Z. & Lenski, R. E. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl Acad. Sci. USA 105, 7899-7906 (2008). A seminal evolution replay experiment demonstrating the emergence of a phenotypic innovation that transcends the species boundaries through historical contingency.
60. Meyer, J. R. et al. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335, 428-432 (2012).
61. Futuyama, D. J. Evolutionary Biology 2nd edn (Sinauer, Sunderland, Massachusetts,1986).
62. Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 335, 457-461 (2012).
63. Riehle, M. M., Bennett, A. F. & Long, A. D. Changes in gene expression following high-temperature adaptation in experimentally evolved populations of Escherichia coli. Physiol. Biochem. Zool. 78, 299-315 (2005).
64. Crozat, E. et al. Parallel genetic and phenotypic evolution of DNA superhelicity in experimental populations of Escherichia coli. Mol. Biol. Evol. 27, 2113-2128 (2010).
65. Treves, D. S., Manning, S. & Adams, J. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol. Biol. Evol. 15, 789-797 (1998).
66. Almahmoud, I., Kay, E., Schneider, D. & Maurin, M. Mutational paths towards increased fluoroquinolone resistance in Legionella pneumophila. J. Antimicrob. Chemother. 64, 284-293 (2009).
67. Huitric, E. et al. Rates and mechanisms of resistance development in Mycobacterium tuberculosis to a novel diarylquinoline ATP synthase inhibitor. Antimicrob. Agents Chemother. 54, 1022-1028 (2010).
68. Bantinaki, E. et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 176, 441-453 (2007).
69. Maharjan, R., Seeto, S., Notley-McRobb, L. & Ferenci, T. Clonal adaptive radiation in a constant environment. Science 313, 514-517 (2006).
70. Papadopoulos, D. et al. Genomic evolution during a 10,000-generation experiment with bacteria. Proc. Natl Acad. Sci. USA 96, 3807-3812 (1999).
71. Beaumont, H. J., Gallie, J., Kost, C., Ferguson, G. C. & Rainey, P. B. Experimental evolution of bet hedging. Nature 462, 90-93 (2009).
72. Le Gac, M. et al. Metabolic changes associated with adaptive diversification in Escherichia coli. Genetics 178, 1049-1060 (2008).
73. Spencer, C. C., Bertrand, M., Travisano, M. & Doebeli,M. Adaptive diversification in genes that regulate resource use in Escherichia coli. PLoS Genet. 3, e15 (2007).
74. Bohannan, B. J. M., Kerr, B., Jessup, C. M., Hughes, J. B. & Sandvik, G. Trade-offs and coexistence in microbial microcosms. Antonie Van Leeuwenhoek 81, 107-115 (2002).
75. Rozen, D. E., Philippe, N., de Visser, J. A., Lenski, R. E. & Schneider, D. Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol. Lett. 12, 34-44 (2009).
76. Laland, K. N., Odling-Smee, F. J. & Feldman, M. W. Evolutionary consequences of niche construction and their implications for ecology. Proc. Natl Acad. Sci. USA 96, 10242-10247 (1999).
77. Rosenzweig, F. R., Sharp, R. R., Treves, D. S. & Adams, J. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137, 903-917 (1994).
78. West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffin, A. S. The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38, 53-77 (2007).
79. De Vos, D. et al. Study of pyroverdine type and production by Pseudomonas aeruginosa isolated from cystic fibrosis patients: prevalence of type II pyoverdine isolates and accumulation of pyoverdine-negative mutants. Arch. Microbiol. 175, 384-388 (2001).
80. West, S. A. & Buckling, A. Cooperation, virulence and siderophore production in bacterial parasites. Proc. R. Soc. Lond. B 270, 37-44 (2003).
81. Rainey, P. B. & Rainey, K. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425, 72-74 (2003).
82. Velicer, G. J., Kroos, L. & Lenski, R. E. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598-601 (2000).
83. Manhes, P. & Velicer, G. J. Experimental evolution of selfish policing in social bacteria. Proc. Natl Acad. Sci. USA 108, 8357-8362 (2011).
84. Chow, S. S., Wilke, C. O., Ofria, C., Lenski, R. E. & Adami, C. Adaptive radiation from resource competition in digital organisms. Science 305, 84-86 (2004).
85. Crombach, A. & Hogeweg, P. Evolution of resource cycling in ecosystems and individuals. BMC Evol. Biol. 9, 122 (2009).
86. Hanage, W. P., Spratt, B. G., Turner, K. M. E. & Fraser, C. Modelling bacterial speciation. Phil. Trans. R. Soc. B 361, 2039-2044 (2006).
87. Lenski, R. E., Ofria, C., Pennock, R. T. & Adami, C. The evolutionary origin of complex features. Nature 423, 139-144 (2003).
88. Clune, J., Goldsby, H. J., Ofria, C. & Pennock, R. T. Selective pressures for accurate altruism targeting: evidence from digital evolution for difficult-to-test aspects of inclusive fitness theory. Proc. Biol. Sci. 278, 666-674 (2011).
89. Waibel, M., Floreano, D. & Keller, L. A. Quantitative test of Hamilton's rule for the evolution of altruism. PLoS Biol. 9, e1000615 (2011).
90. Pigliucci, M. Is evolvability evolvable? Nature Rev. Genet. 9, 75-82 (2008).
91. Cooper, V. S., Schneider, D., Blot, M. & Lenski, R. E. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J. Bacteriol. 183, 2834-2841 (2001).
92. Herring, C. D. et al. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nature Genet. 38, 1406-1412 (2006).
93. Pelosi, L. et al. Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173, 1851-1869 (2006).
94. Barrick, J. E. et al. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243-1247 (2009).
95. Andersson, D. I. & Hughes, D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nature Rev. Microbiol. 8, 260-271 (2010).
96. Andersson, D. I. The biological cost of mutational antibiotic resistance: any practical conclusions? Curr. Opin. Microbiol. 9, 461-465 (2006).
97. Macvanin, M., Ballagi, A. & Hughes, D. Fusidic acid-resistant mutants of Salmonella enterica serovar Typhimurium have low levels of heme and a reduced rate of respiration and are sensitive to oxidative stress. Antimicrob. Agents Chemother. 48, 3877-3883 (2004).
98. Marcusson, L. L., Frimodt-Moller, N. & Hughes, D. Interplay in the selection of fluoroquinolones resistance and bacterial fitness. PLoS Pathog. 5, e1000541 (2009).
99. Macvanin, M. et al. Fusidic acid-resistant mutants of Salmonella enterica serovar Typhimurium with low fitness in vivo are defective in RpoS induction. Antimicrob. Agents Chemother. 47, 3743-3749 (2003).
100. S). Genetics 183, 539-546 (2009).
101. Kohanski, M. A., Dwyer, D. J. & Collins, J. J. How antibiotics kill bacteria: from targets to networks. Nature Rev. Microbiol. 8, 423-435 (2010).
102. Cooper, T. F., Rozen, D. E. & Lenski, R. E. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc. Natl Acad. Sci. USA 100, 1072-1077 (2003).
103. Knight, C. G. et al. Unraveling adaptive evolution: how a single point mutation affects the protein coregulation network. Nature Genet. 38, 1015-1022 (2006).
104. Kadam, S. V., Wegener-Feldbrugge, S., Sogaard-Andersen, L. & Velicer, G. J. Novel transcriptome patterns accompany evolutionary restoration of defective social development in the bacterium Myxococcus xanthus. Mol. Biol. Evol. 25, 1274-1281 (2008).
105. Velicer, G. J. et al. Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc. Natl Acad. Sci. USA 103, 8107-8112 (2006).
106. Notley-McRobb, L., King, T. & Ferenci, T. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J. Bacteriol. 184, 806-811 (2002).
107. Wang, L. et al. Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol. Evol. 2, 478-487 (2010).
108. Applebee, M. K., Herrgård, M. J. & Palsson, B. O. Impact of individual mutations on increased fitness in adaptively evolved strains of Escherichia coli. J. Bacteriol. 190, 5087-5094 (2008).
109. Yu, Y. T., Yuan, X. & Velicer, G. J. Adaptive evolution of an sRNA that controls Myxococcus development. Science 328, 993 (2010).
110. Jacob, F. Evolution and tinkering. Science 196, 1161-1166 (1977).
111. McLean, R. C., Bell, G. & Rainey, P. B. The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proc. Natl Acad. Sci. USA 101, 8072-8077 (2004).
112. Khan, A. I., Dinh, D. M., Schneider, D., Lenski, R. E. & Cooper, T. F. Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332, 1193-1196 (2011).
113. Woods, R. J. et al. Second-order selection for evolvability in a large Escherichia coli population. Science 331, 1433-1436 (2011). The demonstration that beneficial alleles can be selected because of their future evolvability.
114. Le Gac, M. & Doebeli, M. Epistasis and frequency dependence influence the fitness of an adaptive mutation in a diversifying lineage. Mol. Ecol. 19, 2430-2438 (2010).
115. Bhagwat, A. A. et al. Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl. Environ. Microbiol. 72, 4978-4986 (2006).
116. Ferenci, T., Galbiati, H. F., Betteridge, T., Phan, K. & Spira, B. The constancy of global regulation across a species: the concentrations of ppGpp and RpoS are strain-specific in Escherichia coli. BMC Microbiol. 11, 62 (2011).
117. Levert, M. et al. Molecular and evolutionary bases of within-patient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. PLoS Pathog. 6, e1001125 (2010).
118. Yang, L. et al. Evolutionary dynamics of bacteria in a human host environment. Proc. Natl Acad. Sci. USA 108, 7481-7486 (2011).
119. Lieberman, T. D. et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nature Genet. 43, 1275-1281 (2011).
120. Rainey, P. B. & Cooper, T. F. Evolution of bacterial diversity and the origins of modularity. Res. Microbiol. 155, 370-375 (2004).
121. Wagner, G. P., Pavlicev, M. & Cheverud, J. M. The road to modularity. Nature Rev. Genet. 12, 921-931 (2007).
122. Kashtan, N. & Alon, U. Spontaneous evolution of modularity and network motifs. Proc. Natl Acad. Sci. USA 102, 13773-13778 (2005).
123. Espinosa-Soto, C. & Wagner, A. Specialization can drive the evolution of modularity. PLoS Comp. Biol. 6, e1000719 (2010).
124. François, P. & Hakim, V. Design of genetic networks with specified functions by evolution in silico. Proc. Natl Acad. Sci. USA 101, 580-585 (2004).
125. Veening, J. W., Smits, W. K. & Kuipers, O. P. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62, 193-210 (2008).
126. Kuo, P. D., Banzhaf, W. & Leier, A. Network topology and the evolution of dynamics in an artificial genetic regulatory network model created by whole genome duplication and divergence. BioSystems 85, 177-200 (2006).
127. Beslon, G., Parsons, D. P., Sanchez-Dehesa, Y., Peña, J. M. & Knibbe, C. Scaling laws in bacterial genomes: a side-effect of selection of mutational robustness? BioSystems 102, 32-40 (2010).
128. Wielgoss, S. et al. Mutation rate inferred from synonymous substitutions in a long-term evolution experiment with Escherichia coli. G3 (Bethesda) 1, 183-186 (2011).
129. Sniegowski, P. D., Gerrish, P. J. & Lenski, R. E. Evolution of high mutation rates in experimental populations of E. coli. Nature 387, 703-705 (1997).
130. Gaffé, J. et al. Insertion sequence-driven evolution of Escherichia coli in chemostats. J. Mol. Evol. 72, 398-412 (2011).
131. Oliver, A., Cantón, R., Campo, P., Baquero, F. & Blázquez, J. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288, 1251-1254 (2000).
132. Cox, E. C. & Gibson, T. C. Selection for high mutation rates in chemostats. Genetics 77, 169-184 (1974).
133. Chao, L. & Cox, E. C. Competition between high and low mutating strains of Escherichia coli. Evolution 37, 125-134 (1983).
134. Racey, D., Inglis, R. F., Harrison, F., Oliver, A. & Buckling, A. The effect of elevated mutation rates on the evolution of cooperation and virulence of Pseudomonas aeruginosa. Evolution 64, 515-521 (2010).
135. Taddei, F. et al. Role of mutator alleles in adaptive evolution. Nature 387, 700-702 (1997).
136. Tenaillon, O., Toupance, B., Le Nagard, H., Taddei, F. & Godelle, B. Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152, 485-493 (1999).
137. Bedau, M. A. & Packard, M. H. Evolution of evolvability via adaptation of mutation rates. BioSystems 69, 143-162 (2003).
138. Clune, J. et al. Natural selection fails to optimize mutation rates for long-term adaptation on rugged fitness landscapes. PLoS Comp. Biol. 4, e1000187 (2008).
139. Wagner, G. P. & Altenberg, L. Complex adaptations and the evolution of evolvability. Evolution 50, 967-976 (1996).
140. Knibbe, C., Coulon, A., Mazet, O., Fayard, J. M. & Beslon, G. A long-term evolutionary pressure on the amount of noncoding DNA. Mol. Biol. Evol. 24, 2344-2353 (2007).
141. Crombach, A. & Hogeweg, P. Chromosome rearrangements and the evolution of genome structuring and adaptability. Mol. Biol. Evol. 24, 1130-1139 (2007).
142. Wilke, C. O., Wang, J. L., Ofria, C., Lenski, R. E. & Adami, C. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 412, 331-333 (2001). An in silico experiment that uses the Avida framework to investigate the complex interactions between fitness and robustness, and shows that selection for robustness can overcome selection for fitness at high mutation rates.
143. Crombach, A. & Hogeweg, P. Evolution of evolvability in gene regulatory networks. PLoS Comp. Biol. 4, e1000112 (2008). In silico experiments with the 'string-of-pearls' formalism, showing that evolvability may be selected in regulation networks.
144. Lenski, R. E., Barrick, J. E. & Ofria, C. Balancing robustness and evolvability. PLoS Biol. 4, e428 (2006).
145. Wagner, A. Neutralism and selectionism: a network-based reconciliation. Nature Rev. Genet. 9, 965-974 (2008).
146. McBride, R. C., Ogbunugafor, C. B. & Turner, P. E. Robustness promotes evolvability of thermotolerance in an RNA virus. BMC Evol. Biol. 8, 231 (2008).
147. Elena, S. F. & Sanjuán, R. The effect of genetic robustness on evolvability in digital organisms. BMC Evol. Biol. 8, 284 (2008).
148. Luria, S. E. & Delbrück, M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28, 491-511 (1943).
149. O'Neill, B. Digital evolution. PLoS Biol. 1, e18 (2003).
150. Misevic, D., Ofria, C. & Lenski, R. E. Sexual reproduction reshapes the genetic architecture of digital organisms. Proc. Biol. Sci. 273, 457-464 (2006).
151. de Boer, F. K. & Hogeweg, P. Eco-evolutionary dynamics, coding structure and the information threshold. BMC Evol. Biol. 10, 361 (2010).
152. Kashtan, N., Noor, E. & Alon, U. Varying environments can speed up evolution. Proc. Natl Acad. Sci. USA 104, 13711-13716 (2007).
153. Kashtan, N., Parter, M., Dekel, E., Mayo, A. E. & Alon, U. Extinctions in heterogeneous environments and the evolution of modularity. Evolution 63, 1964-1975 (2009).
154. Kaneko, K. Proportionality between variances in gene expression induced by noise and mutation: consequence of evolutionary robustness. BMC Evol. Biol. 11, 27 (2011).
155. Floreano, D., Mitri, S., Magnenat, S. & Keller, L. Evolutionary conditions for the emergence of communication in robots. Curr. Biol. 17, 514-519 (2007).
156. ten Tusscher, K. H. W. J. & Hogeweg, P. The role of genome and gene regulatory network canalization in the evolution of multi-trait polymorphisms and sympatric speciation. BMC Evol. Biol. 9, 159 (2009).
157. Mattiussi, C. & Floreano, D. Analog genetic encoding for the evolution of circuits and networks. IEEE Trans. Evol. Comput. 11, 596-607 (2007).
158. Marbach, D., Mattiussi, C. & Floreano, D. Replaying the evolutionary tape: biomimetic reverse engineering of gene networks. Ann. NY Acad. Sci. 1158, 234-245 (2009).