Robustness promotes evolvability of thermotolerance in an RNA virus

BMC Evolutionary Biology

Volumn 8, Issue 1, 2008, Pages

  McBride, Robert C ^a   Ogbunugafor, C Brandon ^a   Turner, Paul E ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CLONE; GENETIC ANALYSIS; GENETIC SELECTION; HEAT SHOCK; HEAT TOLERANCE; MOLECULAR EVOLUTION; NONHUMAN; POPULATION; RNA VIRUS; ADAPTATION; BACTERIOPHAGE; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; PSEUDOMONAS SYRINGAE; SEQUENCE ANALYSIS; VIROLOGY; VIRUS CULTURE;

RNA VIRUSES;

VIRUS RNA;

ADAPTATION, BIOLOGICAL; BACTERIOPHAGE PHI 6; EVOLUTION, MOLECULAR; HEAT; PLAQUE ASSAY; PSEUDOMONAS SYRINGAE; RNA, VIRAL; SELECTION (GENETICS); SEQUENCE ANALYSIS, RNA; VARIATION (GENETICS);

EID: 50049135016     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-8-231     Document Type: Article

References (55)

1. Perspective: Complex adaptations and the evolution of evolvability. GP Wagner L Altenberg, Evolution 1996 50 3 967 976 10.2307/2410639
2. Evolvability. M Kirschner J Gerhart, Proceedings of the National Academy of Sciences of the United States of America 1998 95 15 8420 8427 9671692 10.1073/pnas.95.15.8420
3. Evolvability of an RNA virus is determined by its mutational neighbourhood. CL Burch L Chao, Nature 2000 406 6796 625 628 10.1038/35020564 10949302
4. Perspective: Evolution and detection of genetic robustness. JAGM de Visser J Hermisson GP Wagner LA Meyers HC Bagheri JL Blanchard L Chao JM Cheverud SF Elena W Fontana G Gibson TF Hansen D Krakauer RC Lewontin C Ofria SH Rice G von Dassow A Wagner MC Whitlock, Evolution 2003 57 9 1959 1972 14575319
5. Robustness and evolvability in living systems. A Wagner, Princeton studies in complexity Princeton, N.J., Princeton University Press 2005 xii, 367 p.
6. Balancing robustness and evolvability. RE Lenski JE Barrick C Ofria, PLoS Biology 2006 4 12 2190 2192 10.1371/journal.pbio.0040428
7. Selection for fitness versus selection for robustness in RNA secondary structure folding. CO Wilke, Evolution 2001 55 12 2412 2420 11831657
8. Smoothness within ruggedness: The role of neutrality in adaptation. MA Huynen PF Stadler W Fontana, Proceedings of the National Academy of Sciences of the United States of America 1996 93 1 397 401 8552647 10.1073/pnas.93.1.397
9. The population genetic theory of hidden variation and genetic robustness. J Hermisson GP Wagner, Genetics 2004 168 4 2271 2284 15611191 10.1534/genetics.104.029173
10. Evolution of mutational robustness in an RNA virus. R Montville R Froissart SK Remold O Tenaillon PE Turner, PLoS Biology 2005 3 11 1939 1945 10.1371/journal.pbio.0030381
11. The fittest versus the flattest: Experimental confirmation of the quasispecies effect with subviral pathogens. FM Codoner JA Daros RV Sole SF Elena, PLoS Pathogens 2006 2 12 1187 1193 10.1371/journal.ppat.0020136
12. Selection for robustness in mutagenized RNA viruses. R Sanjuan JM Cuevas V Furio EC Holmes A Moya, Plos Genetics 2007 3 6 939 946 10.1371/journal.pgen. 0030093
13. Cells, embryos, and evolution : toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability. J Gerhart M Kirschner, Boston, Blackwell Science 1997 xiii, 642 p.
14. One sequence, two ribozymes: Implications for the emergence of new ribozyme folds. EA Schultes DP Bartel, Science 2000 289 5478 448 452 10.1126/science.289.5478.448 10903205
15. Protein stability promotes evolvability. JD Bloom ST Labthavikul CR Otey FH Arnold, Proceedings of the National Academy of Sciences of the United States of America 2006 103 15 5869 5874 16581913 10.1073/pnas.0510098103
16. Why highly expressed proteins evolve slowly. DA Drummond JD Bloom C Adami CO Wilke FH Arnold, Proceedings of the National Academy of Sciences of the United States of America 2005 102 40 14338 14343 16176987 10.1073/pnas. 0504070102
17. Plasticity, evolvability, and modularity in RNA. LW Ancel W Fontana, Journal of Experimental Zoology 2000 288 3 242 283 10.1002/1097-010X(20001015) 288:3<242::AID-JEZ5>3.0.CO;2-O 11069142
18. New structural variation in evolutionary searches of RNA neutral networks. Sumedha OC Martin A Wagner, Biosystems 2007 90 2 475 485 10.1016/j.biosystems.2006.11.007 17276586
19. Sex and the evolution of intrahost competition in RNA virus phi6. PE Turner L Chao, Genetics 1998 150 2 523 532 9755186
20. Hybrid frequencies confirm limit to coinfection in the RNA bacteriophage phi6. PE Turner CL Burch KA Hanley L Chao, Journal of Virology 1999 73 3 2420 2424 9971826
21. Co-infection weakens selection against epistatic mutations in RNA viruses. R Froissart CO Wilke R Montville SK Remold L Chao PE Turner, Genetics 2004 168 1 9 19 15454523 10.1534/genetics.104.030205
22. Fitness of RNA virus decreased by Muller's ratchet. L Chao, Nature 1990 348 6300 454 455 10.1038/348454a0 2247152
23. Evolution by small steps and rugged landscapes in the RNA virus phi6. CL Burch L Chao, Genetics 1999 151 3 921 927 10049911
24. Epistasis and its relationship to canalization in the RNA virus phi 6. CL Burch L Chao, Genetics 2004 167 2 559 567 15238511 10.1534/genetics.103.021196
25. Cell wall lysin as a component of the bacteriophage phi 6 virion. L Mindich J Lehman, Journal of Virology 1979 30 2 489 496 469991
26. Canalization in evolutionary genetics: a stabilizing theory? G Gibson G Wagner, Bioessays 2000 22 4 372 380 10.1002/(SICI)1521-1878(200004)22:4<372:: AID-BIES7>3.0.CO;2-J 10723034
27. Compensatory nearly neutral mutations: Selection without adaptation. DL Hartl CH Taubes, Journal of Theoretical Biology 1996 182 3 303 309 10.1006/jtbi.1996.0168 8944162
28. Role of mutator alleles in adaptive evolution. F Taddei M Radman J Maynard-Smith B Toupance PH Gouyon B Godelle, Nature 1997 387 6634 700 702 10.1038/42696 9192893
29. Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. O Tenaillon B Toupance H Le Nagard F Taddei B Godelle, Genetics 1999 152 2 485 493 10353893
30. The fate of microbial mutators. JAGM de Visser, Microbiology-Sgm 2002 148 1247 1252
31. Pleiotropic costs of niche expansion in the RNA bacteriophage phi 6. S Duffy PE Turner CL Burch, Genetics 2006 172 2 751 757 16299384 10.1534/genetics.105.051136
32. Evolution of host specificity drives reproductive isolation among RNA viruses. S Duffy CL Burch PE Turner, Evolution 2007 61 11 2614 2622 10.1111/j.1558-5646.2007.00226.x 17908251
33. High frequency of mutations that expand the host range of an RNA virus. MT Ferris P Joyce CL Burch, Genetics 2007 176 2 1013 1022 17409090 10.1534/genetics.106.064634
34. Membrane fusion in prokaryotes: bacteriophage phi 6 membrane fuses with the Pseudomonas syringae outer membrane. DH Bamford M Romantschuk PJ Somerharju, Embo J 1987 6 5 1467 1473 3608985
35. Distribution of spontaneous mutants and inferences about the replication mode of the RNA bacteriophage phi 6. L Chao CU Rang LE Wong, Journal of Virology 2002 76 7 3276 3281 11884552 10.1128/JVI.76.7.3276-3281.2002
36. Crystal structure of an ancient protein: Evolution by conformational epistasis. EA Ortlund JT Bridgham MR Redinbo JW Thornton, Science 2007 317 5844 1544 1548 10.1126/science.1142819 17702911
37. Henipavirus susceptibility to environmental variables. R Fogarty K Halpin AD Hyatt P Daszak BA Mungall, Virus Research 2008 132 1-2 140 144 10.1016/j.virusres.2007.11.010 18166242
38. Survival of human immunodeficiency virus type 1 after rinsing injection syringes with different cleaning solutions. N Abdala M Crowe Y Tolstov R Heimer, Substance Use and Misuse 2004 39 4 581 600 10.1081/JA-120030059
39. Survival of HIV-1 in syringes: effects of temperature during storage. N Abdala R Reyes JM Carney R Heimer, Substance Use and Misuse 2000 35 10 1369 1383 10.3109/10826080009148220
40. Viral ecology and the maintenance of novel host use. JJ Dennehy NA Friedenberg RD Holt PE Turner, American Naturalist 2006 167 3 429 439 10.1086/499381 16673350
41. Cost of host radiation in an RNA virus. PE Turner SF Elena, Genetics 2000 156 4 1465 1470 11102349
42. Prisoner's dilemma in an RNA virus. PE Turner L Chao, Nature 1999 398 6726 441 443 10.1038/18913 10201376
43. Escape from Prisoner's Dilemma in RNA phage phi 6. PE Turner L Chao, American Naturalist 2003 161 3 497 505 10.1086/367880 12699226
44. Reduced fecundity is the cost of cheating in RNA virus phi 6. JJ Dennehy PE Turner, Proceedings of the Royal Society of London Series B-Biological Sciences 2004 271 1554 2275 2282 10.1098/rspb.2004.2833
45. Cooperation among animals : an evolutionary perspective. LA Dugatkin, Oxford series in ecology and evolution New York, Oxford University Press 1997 xvii, 221 p.
46. A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. JA Bruenn, Nucleic Acids Research 2003 31 7 1821 1829 12654997 10.1093/nar/gkg277
47. Relationships among the positive strand and double-strand RNA viruses as viewed through their RNA-dependent RNA-polymerases. JA Bruenn, Nucleic Acids Research 1991 19 2 217 226 2014162 10.1093/nar/19.2.217
48. Packaging, replication and recombination of the segmented genomes of bacteriophage phi 6 and its relatives. L Mindich, Virus Research 2004 101 1 83 92 10.1016/j.virusres.2003.12.008 15010219
49. Proteins of Bacteriophage Phi6. JF Sinclair A Tzagoloff D Levine L Mindich, Journal of Virology 1975 16 3 685 695 1159897
50. Nucleotide-sequence of the small double-stranded-RNA segment of bacteriophage-phi-6 - novel mechanism of natural translational control. T Mcgraw L Mindich B Frangione, Journal of Virology 1986 58 1 142 151 3754015
51. Theory of lethal mutagenesis for viruses. JJ Bull R Sanjuan CO Wilke, Journal of Virology 2007 81 6 2930 2939 17202214 10.1128/JVI.01624-06
52. Viral error catastrophe by mutagenic nucleosides. JP Anderson R Daifuku LA Loeb, Annual Review of Microbiology 2004 58 183 205 10.1146/annurev.micro.58. 030603.123649 15487935
53. HIV-1 over time: fitness loss or robustness gain? M Rolland C Brander DC Nickle JT Herbeck GS Gottlieb MS Campbell BS Maust JI Mullins, Nature Reviews Microbiology 2007 5 9 2006 2007 10.1038/nrmicro1594-c1
54. Phages with segmented double-stranded RNA genomes. L Mindich, The Bacteriophages Oxford ; New York, Oxford University Press, Calendar R, 2nd 2006 xiii, 746 p.
55. Isolation of nonsense suppressor mutants in Pseudomonas. L Mindich J Cohen M Weisburd, Journal of Bacteriology 1976 126 1 177 182 816771