Experimental evolution, loss-of-function mutations, and "the first rule of adaptive evolution"

Quarterly Review of Biology

Volumn 85, Issue 4, 2010, Pages 419-445

  Behe, Michael J ^a  

^a LEHIGH UNIVERSITY   (United States)

Author keywords

Adaptation; Experimental evolution; Loss of function; Malaria; Mutation; Yersinia pestis

Indexed keywords

ADAPTATION; ARTICLE; BACTERIUM; DIRECTED MOLECULAR EVOLUTION; EVOLUTION; GENETICS; METABOLISM; MUTATION; VIRUS;

ADAPTATION, PHYSIOLOGICAL; BACTERIA; BIOLOGICAL EVOLUTION; DIRECTED MOLECULAR EVOLUTION; MUTATION; VIRUSES;

YERSINIA PESTIS;

EID: 78650155718     PISSN: 00335770     EISSN: None     Source Type: Journal    
DOI: 10.1086/656902     Document Type: Article

References (86)

1. Agudelo-Romero P., Carbonell P., Perez-Amador M. A., Elena S. F. 2008. Virus adaptation by manipulation of host's gene expression. PLoS ONE 3:e2397.
2. Axe D. D., Foster N. W., Fersht A. R. 1996. Active barnase variants with completely random hydrophobic cores. Proceedings of the National Academy of Sciences USA 93:5590-5594.
3. Behe M. J., Englander S. W. 1979. Mixed gelation theory. Kinetics, equilibrium and gel incorporation in sickle hemoglobin mixtures. Journal of Molecular Biology 133:137-160.
4. Blount Z. D., Borland C. Z., Lenski R. E. 2008. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proceedings of the National Academy of Sciences USA 105:7899-7906.
5. Bowie J. U., Sauer R. T. 1989. Identifying determinants of folding and activity for a protein of unknown structure. Proceedings of the National Academy of Sciences USA 86:2152-2156.
6. Bowie J. U., Reidhaar-Olson J. F., Lim W. A., Sauer R. T. 1990. Deciphering the message in protein sequences: tolerance to amino acid substitutions. Science 247:1306-1310.
7. Bull J. J., Badgett M. R., Rokyta D., Molineux I. J. 2003. Experimental evolution yields hundreds of mutations in a functional viral genome. Journal of Molecular Evolution 57:241-248.
8. Bull J. J., Badgett M. R., Wichman H. A., Huelsenbeck J. P., Hillis D. M., Gulati A., Ho C., Molineux I. J. 1997. Exceptional convergent evolution in a virus. Genetics 147:1497-1507.
9. Bull J. J., Molineux I. J. 2008. Predicting evolution from genomics: experimental evolution of bacteriophage T7. Heredity 100:453-463.
10. Bull J. J., Springman R., Molineux I. J. 2007. Compensatory evolution in response to a novel RNA polymerase: orthologous replacement of a central network gene. Molecular Biology and Evolution 24:900-908.
11. Burch C. L., Chao L. 1999. Evolution by small steps and rugged landscapes in the RNA virus ψ 6. Genetics 151:921-927.
12. Carniel E. 2003. Evolution of pathogenic Yersinia: some lights in the dark. Pages 3-12 in The Genus Yersinia: Entering the Functional Genomic Era, edited by M. Skurnik et al. New York: Kluwer Academic/ Plenum.
13. Cavalli-Sforza L. L., Menozzi P., Piazza A. 1994. The History and Geography of Human Genes. Princeton (NJ): Princeton University Press.
14. Chain P. S., Hu P., Malfatti S. A., Radnedge L., Larimer F., Vergez L. M., Worsham P., Chu M. C., Andersen G. L. 2006. Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. Journal of Bacteriology 188:4453-4463.
15. Clarke P. H. 1984. Amidases of Pseudomonas aeruginosa. Pages 187-232 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
16. Cooper T. F., Rozen D. E., Lenski R. E. 2003. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proceedings of the National Academy of Sciences USA 100:1072-1077.
17. Cooper V. S., Schneider D., Blot M., Lenski R. E. 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. Journal of Bacteriology 183:2834-2841.
18. Couñago R., Chen S., Shamoo Y. 2006. In vivo molecular evolution reveals biophysical origins of organismal fitness. Molecular Cell 22:441-449.
19. Crill W. D., Wichman H. A., Bull J. J. 2000. Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154:27-37.
20. Crozat E., Philippe N., Lenski R. E., Geiselmann J., Schneider D. 2005. Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169:523-532.
21. Cuevas J. M., Elena S. F., Moya A. 2002. Molecular basis of adaptive convergence in experimental populations of RNA viruses. Genetics 162:533-542.
22. Darwin C. 1859. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London (UK): John Murray.
23. Drake J. W., Charlesworth B., Charlesworth D., Crow J. F. 1998. Rates of spontaneous mutation. Genetics 148:1667-1686.
24. Duffy S., Burch C. L., Turner P. E. 2007. Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution 61:2614-2622.
25. Duffy S., Turner P. E., Burch C. L. 2006. Pleiotropic costs of niche expansion in the RNA bacteriophage ψ 6. Genetics 172:751-757.
26. Elena S. F., Agudelo-Romero P., Carrasco P., Codoner F. M., Martin S., Torres-Barcelo C., Sanjuan R. 2008. Experimental evolution of plant RNA viruses. Heredity 100:478-483.
27. Elena S. F., Lenski R. E. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Reviews Genetics 4:457-469.
28. Elena S. F., Sanjuan R. 2007. Virus evolution: Insights from an experimental approach. Annual Review of Ecology, Evolution, and Systematics 38:27-52.
29. Ferenci T. 2008. The spread of a beneficial mutation in experimental bacterial populations: the influence of the environment and genotype on the fixation of rpoS mutations. Heredity 100:446-452.
30. Flint J., Hill A. V., Bowden D. K., Oppenheimer S. J., Sill P. R., Serjeantson S. W., Bana-Koiri J., Bhatia K., Alpers M. P., Boyce A. J. 1986. High frequencies of α -thalassaemia are the result of natural selection by malaria. Nature 321:744-750.
31. Forget B. G. 1998. Molecular basis of hereditary persistence of fetal hemoglobin. Annals of the New York Academy of Sciences 850:38-44.
32. Friedman M. J. 1978. Erythrocytic mechanism of sickle cell resistance to malaria. Proceedings of the National Academy of Sciences USA 75:1994-1997.
33. Hall B. G. 1982. Chromosomal mutation for citrate utilization by Escherichia coli K-12. Journal of Bacteriology 151:269-273.
34. Hall B. G. 1983. Evolution of new metabolic functions in laboratory organisms. Pages 234-257 in Evolution of Genes and Proteins, edited by M. Nei and R. K. Koehn. Sunderland (MA): Sinauer Associates.
35. Hall B. G. 1984. The evolved β-galactosidase system of Escherichia coli. Pages 165-186 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
36. Hall B. G. 1995. Evolutionary potential of the ebgA gene. Molecular Biology and Evolution 12:514-517.
37. Hall B. G. 2003. The EBG system of E. coli: origin and evolution of a novel β -galactosidase for the metabolism of lactose. Genetica 118:143-156.
38. Hartley B. S. 1984. Experimental evolution of ribitol dehydrogenase. Pages 23-54 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
39. Huang W., Petrosino J., Hirsch M., Shenkin P. S., Palzkill T. 1996. Amino acid sequence determinants of β -lactamase structure and activity. Journal of Molecular Biology 258:688-703.
40. Kemper J. 1984. Gene recruitment for a subunit of isopropylmalate isomerase. Pages 255-284 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
41. Kennedy J. R. 2002. Modulation of sickle cell crisis by naturally occurring band 3 specific antibodies-a malaria link. Medical Science Monitor 8:HY10-HY13.
42. Lang G. I., Murray A. W., Botstein D. 2009. The cost of gene expression underlies a fitness trade-off in yeast. Proceedings of the National Academy of Sciences USA 106:5755-5760.
43. Lenski R. E. 2004. Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant Breeding Reviews 24:225-265.
44. Lenski R. E., Simpson S. C., Nguyen T. T. 1994. Genetic analysis of a plasmid-encoded, host genotype-specific enhancement of bacterial fitness. Journal of Bacteriology 176:3140-3147.
45. Lenski R. E., Travisano M. 1994. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proceedings of the National Academy of Sciences USA 91:6808-6814.
46. Lenski R. E., Winkworth C. L., Riley M. A. 2003. Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. Journal of Molecular Evolution 56:498-508.
47. Licis N., Balklava Z., van Duin J. 2000. Forced retroevolution of an RNA bacteriophage. Virology 271: 298-306.
48. Licis N., van Duin J. 2006. Structural constraints and mutational bias in the evolutionary restoration of a severe deletion in RNA phage MS2. Journal of Molecular Evolution 63:314-329.
49. Lim W. A., Sauer R. T. 1989. Alternative packing arrangements in the hydrophobic core of lambda repressor. Nature 339:31-36.
50. Lin E. C. C., Wu T. T. 1984. Functional divergence of the l-fucose system in mutants of Escherichia coli. Pages 135-164 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
51. McKenna R., Ilag L. L., Rossmann M. G. 1994. Analysis of the single-stranded DNA bacteriophage X174, refined at a resolution of 3.0 Å. Journal of Molecular Biology 237:517-543.
52. Modiano D., Luoni G., Sirima B. S., Simpore J., Verra F., Konate A., Rastrelli E., Olivieri A., Calissano C., Paganotti G. M., D'Urbano L., Sanou I., Sawadogo A., Modiano G., Coluzzi M. 2001. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature 414:305-308.
53. Mortlock R. P. 1984a. Microorganisms as Model Systems for Studying Evolution. New York: Plenum Press.
54. Mortlock R. P. 1984b. The development of catabolic pathways for the uncommon aldopentoses. Pages 109-134 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
55. Mortlock R. P. 1984c. The utilization of pentitols in studies of the evolution of enzyme pathways. Pages 1-21 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
56. Olsthoorn R. C., van Duin J. 1996. Evolutionary reconstruction of a hairpin deleted from the genome of an RNA virus. Proceedings of the National Academy of Sciences USA 93:12256-12261.
57. Patrick W. M., Quandt E. M., Swartzlander D. B., Matsumura I. 2007. Multicopy suppression underpins metabolic evolvability. Molecular Biology and Evolution 24:2716-2722.
58. Pelosi L., Kuhn L., Guetta D., Garin J., Geiselmann J., Lenski R. E., Schneider D. 2006. Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173: 1851-1869.
59. Pepin K. M., Domsic J., McKenna R. 2008. Genomic evolution in a virus under specific selection for host recognition. Infection, Genetics and Evolution 8:825-834.
60. Perfeito L., Fernandes L., Mota C., Gordo I. 2007. Adaptive mutations in bacteria: high rate and small effects. Science 317:813-815.
61. Pogo A. O., Chaudhuri A. 2000. The Duffy protein: a malarial and chemokine receptor. Seminars in Hematology 37:122-129.
62. Pos K. M., Dimroth P., Bott M. 1998. The Escherichia coli citrate carrier CitT: A member of a novel eubacterial transporter family related to the 2-oxoglutaratemalate translocator from spinach chloroplasts. Journal of Bacteriology 180:4160-4165.
63. Reidhaar-Olson J. F., Sauer R. T. 1988. Combinatorial cassette mutagenesis as a probe of the informational content of protein sequences. Science 241: 53-57.
64. Reidhaar-Olson J. F., Sauer R. T. 1990. Functionally acceptable substitutions in two α -helical regions of lambda repressor. Proteins 7:306-316.
65. Rokyta D., Badgett M. R., Molineux I. J., Bull J. J. 2002. Experimental genomic evolution: extensive compensation for loss of DNA ligase activity in a virus. Molecular Biology and Evolution 19:230-238.
66. Rozen D. E., Lenski R. E. 2000. Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. American Naturalist 155:24-35.
67. Ruwende C., Khoo S. C., Snow R. W., Yates S. N., Kwiatkowski D., Gupta S., Warn P., Allsopp C. E., Gilbert S. C., Peschu N. 1995. Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 376:246-249.
68. Sachs J. L., Bull J. J. 2005. Experimental evolution of conflict mediation between genomes. Proceedings of the National Academy of Sciences USA 102: 390-395.
69. Sauer R. T., Milla M. E., Waldburger C. D., Brown B. M., Schildbach J. F. 1996. Sequence determinants of folding and stability for the P22 Arc repressor dimer. FASEB Journal 10:42-48.
70. Schneider D., Duperchy E., Coursange E., Lenski R. E., Blot M. 2000. Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. Genetics 156:477-488.
71. Sniegowski P. D., Gerrish P. J., Lenski R. E. 1997. Evolution of high mutation rates in experimental populations of E. coli. Nature 387:703-705.
72. Springman R., Badgett M. R., Molineux I. J., Bull J. J. 2005. Gene order constrains adaptation in bacteriophage T7. Virology 341:141-152.
73. Stone J. R., Wray G. A. 2001. Rapid evolution of cis-regulatory sequences via local point mutations. Molecular Biology and Evolution 18:1764-1770.
74. Stott R. 2003. Darwin and the Barnacle. New York: W. W. Norton.
75. Stover C. K., Kemper J., Marsh R. C. 1988. Molecular cloning and characterization of supQ/newD, a gene substitution system for the leuD gene of Salmonella typhimurium. Journal of Bacteriology 170:3115-3124.
76. Subbarao E. K., London W., Murphy B. R. 1993. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. Journal of Virology 67:1761-1764.
77. Suckow J., Markiewicz P., Kleina L. G., Miller J., Kisters-Woike B., Muller-Hill B. 1996. Genetic studies of the Lac repressor. XV: 4000 single amino acid substitutions and analysis of the resulting phenotypes on the basis of the protein structure. Journal of Molecular Biology 261:509-523.
78. Verra F., Simpore J., Warimwe G. M., Tetteh K. K., Howard T., Osier F. H., Bancone G., Avellino P., Blot I., Fegan G., Bull P. C., Williams T. N., Conway D. J., Marsh K., and Modiano D. 2007. Haemoglobin C and S role in acquired immunity against Plasmodium falciparum malaria. PLoS ONE 2:e978.
79. Weatherall D. J., Miller L. H., Baruch D. I., Marsh K., Doumbo O. K., Casals-Pascual C., Roberts D. J. 2002. Malaria and the red cell. Hematology: American Society of Hematology Education Program 2002:35-57.
80. Wichman H. A., Badgett M. R., Scott L. A., Boulianne C. M., Bull J. J. 1999. Different trajectories of parallel evolution during viral adaptation. Science 285:422-424.
81. Wichman H. A., Millstein J., Bull J. J. 2005. Adaptive molecular evolution for 13,000 phage generations: a possible arms race. Genetics 170:19-31.
82. Wills C. 1984. Structural evolution of yeast alcohol dehydrogenase in the laboratory. Pages 233-254 in Microorganisms as Model Systems for Studying Evolution, edited by R. P. Mortlock. New York: Plenum Press.
83. Woods R., Schneider D., Winkworth C. L., Riley M. A., Lenski R. E. 2006. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proceedings of the National Academy of Sciences USA 103:9107-9112. (Pubitemid 43902541)
84. Wren B. W. 2003. The Yersiniae -a model genus to study the rapid evolution of bacterial pathogens. Nature Reviews Microbiology 1:55-64.
85. Yin F. H., Lomax N. B. 1983. Host range mutants of human rhinovirus in which nonstructural proteins are altered. Journal of Virology 48:410-418.
86. Zinser E. R., Schneider D., Blot M., Kolter R. 2003. Bacterial evolution through the selective loss of beneficial genes. Trade-offs in expression involving two loci. Genetics 164:1271-1277.