Synergistic fitness interactions and a high frequency of beneficial changes among mutations accumulated under relaxed selection in Saccharomyces cerevisiae

Genetics

Volumn 178, Issue 3, 2008, Pages 1571-1578

  Dickinson, W Joseph ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT;

ARTICLE; FITNESS; GENE INTERACTION; GENE LOCUS; GENETIC EPISTASIS; GENETIC SELECTION; GENETIC VARIABILITY; MARKER GENE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SPONTANEOUS MUTATION; BIOLOGICAL MODEL; GENETICS; MUTATION;

SACCHAROMYCES CEREVISIAE;

MODELS, GENETIC; MUTATION; SACCHAROMYCES CEREVISIAE; SELECTION (GENETICS);

EID: 45149106736     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.080853     Document Type: Article

References (64)

1. ANDOLFATTO, P., 2005 Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
2. AVILA, V., D. CHAVARRIAS, E. SANCHEZ, A. MANRIQUE, C. LOPEZ-FANJUL et al., 2006 Increase of the spontaneous mutation rate in a long-term experiment with Drosophila melanogaster. Genetics 173: 267-277.
3. BAILEY, T. J., 1995 Statistical Methods in Biology. Cambridge University Press, Cambridge, UK.
4. CHARLESWORTH, B., and D. CHARLESWORTH, 1998 Some evolutionary consequences of deleterious mutations. Genetica 103: 3-19.
5. DAVIES, E. K., A. D. PETERS and P. D. KEIGHTLEY, 1999 High frequency of cryptic deleterious mutations in Caenorhabditis elegans. Science 285: 1748-1751.
6. DENG, H. W., and Y. X. FU, 1998 On the three methods for estimating deleterious genomic mutation parameters. Genet. Res. 71: 223-236.
7. DE VISSER, J. A., and S. F. ELENA, 2007 The evolution of sex: empirical insights into the roles of epistasis and drift. Nat. Rev. Genet. 8: 139-149.
8. DE VISSER, J. A., R. F. HOEKSTRA and H. VAN DEN ENDE, 1997 An experimental test for synergistic epistasis and its application in Chlamydomonas. Genetics 145: 815-819.
9. DRAKE, J. W., 1991 A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. USA 88: 7160-7164.
10. ELENA, S. F., and R. E. LENSKI, 1997 Test of synergistic interactions among deleterious mutations in bacteria. Nature 390: 395-398.
11. ELENA, S. F., and R. E. LENSKI, 2001 Epistasis between new mutations and genetic background and a test of genetic canalization. Evolution 55: 1746-1752.
12. FENSTER, C. B., L. F. GALLOWAY and L. CHAO, 1997 Epistasis and its consequences for the evolution of natural populations. Trends Ecol. Evol. 12: 282-286.
13. FISHER, R. A., 1930 The Genetical Theory of Natural Selection. Clarendon Press, Oxford.
14. FRY, J. D., 2004 On the rate and linearity of viability declines in Drosophila mutation-accumulation experiments: genomic mutation rates and synergistic epistasis revisited. Genetics 166: 797-806.
15. FRY, J. D., P. D. KEIGHTLEY, S. L. HEINSOHN and S. V. NUZHDIN, 1999 New estimates of the rates and effects of mildly deleterious mutation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 96: 574-579.
16. GARCIA-DORADO, A., C. LOPEZ-FANJUL and A. CABALLERO, 1999 Properties of spontaneous mutations affecting quantitative traits. Genet. Res. 74: 341-350.
17. GAVIN, A. C., P. ALOY, P. GRANDI, R. KRAUSE, M. BOESCHE et al., 2006 Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631-636.
18. HARTL, D. L., and A. G. CLARK, 1997 Principles of Population Genetics. Sinauer Associates, Sunderland, MA.
19. HAWLEY, R. S., and M. WALKER, 2003 Advanced Genetic Analysis: Finding Meaning in a Genome. Blackwell, Oxford.
20. HERSKOWITZ, I., and R. E. JENSEN, 1991 Putting the HO gene to work: practical uses for mating-type switching. Methods Enzymol. 194: 132-146.
21. HO, Y., A. GRUHLER, A. HEILBUT, G. D. BADER, L. MOORE et al., 2002 Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415: 180-183.
22. JOSEPH, S. B., and D. W. HALL, 2004 Spontaneous mutations in diploid Saccharomyces cerevisiae: more beneficial than expected. Genetics 168: 1817-1825.
23. KACSER, H., and J. A. BURNS, 1981 The molecular basis of dominance. Genetics 97: 639-666.
24. KEIGHTLEY, P. D., and A. CABALLERO, 1997 Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 94: 3823-3827.
25. KEIGHTLEY, P. D., and A. EYRE-WALKER, 2000 Deleterious mutations and the evolution of sex. Science 290: 331-333.
26. KEIGHTLEY, P. D., and M. LYNCH, 2003 Toward a realistic model of mutations affecting fitness. Evolution 57: 683-685.
27. KIBOTA, T. T., and M. LYNCH, 1996 Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381: 694-696.
28. KIM, P. M., L. J. LU, Y. XIA and M. B. GERSTEIN, 2006 Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314: 1938-1941.
29. KOMILI, S., and F. P. ROTH, 2007 Genetic interaction screens advance in reverse. Genes Dev. 21: 137-142.
30. KONDRASHOV, A. S., 1988 Deleterious mutations and the evolution of sexual reproduction. Nature 336: 435-440.
31. KONDRASHOV, A. S., 1994 Muller's ratchet under epistatic selection. Genetics 136: 1469-1473.
32. KONDRASHOV, A. S., 1998 Measuring spontaneous deleterious mutation process. Genetica 103: 183-197.
33. KORONA, R., 1999 Unpredictable fitness transitions between haploid and diploid strains of the genetically loaded yeast Saccharomyces cerevisiae. Genetics 151: 77-85.
34. KOUYOS, R. D., O. K. SILANDER and S. BONHOEFFER, 2007 Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol. Evol. 22: 308-315.
35. LENSKI, R. E., 1991 Quantifying fitness and gene stability in microorganisms. Biotechnology 15: 173-192.
36. LYNCH, M., 1994 Neutral models of phenotypic evolution, pp. 86-108 in Ecological Genetics, edited by L. A. REAL. Princeton University Press, Princeton, NJ.
37. MARTIN, G., and T. LENORMAND, 2006 A general multivariate extension of Fisher's geometrical model and the distribution of mutation fitness effects across species. Evolution 60: 893-907.
38. MUKAI, T., 1969 The genetic structure of natural populations of Drosophila melanogaster. VII. Synergistic interactions of spontaneous mutant polygenes controlling viability. Genetics 61: 749-761.
39. ORR, H. A., 1995 The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805-1813.
40. ORR, H. A., 2001 The "sizes" of mutations fixed in phenotypic evolution: a response to Clarke and Arthur. Evol. Dev. 3: 121-123.
41. ORR, H. A., 2006 The distribution of fitness effects among beneficial mutations in Fisher's geometric model of adaptation. J. Theor. Biol. 238: 279-285.
42. PERFEITO, L., L. FERNANDES, C. MOTA and I. GORDO, 2007 Adaptive mutations in bacteria: high rate and small effects. Science 317: 813-815.
43. RICE, W. R., 1998 Requisite mutational load, pathway epistasis and deterministic mutation accumulation in sexual versus asexual populations. Genetica 103: 71-81.
44. SANJUAN, R., and S. F. ELENA, 2006 Epistasis correlates to genomic complexity. Proc. Natl. Acad. Sci. USA 103: 14402-14405.
45. SHABALINA, S. A., L. YAMPOLSKY and A. S. KONDRASHOV, 1997 Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection. Proc. Natl. Acad. Sci. USA 94: 13034-13039.
46. SHAW, R. G., D. L. BYERS and E. DARMO, 2000 Spontaneous mutational effects on reproductive traits of Arabidopsis thaliana. Genetics 155: 369-378.
47. SHAW, R., F. SHAW and C. GEYER, 2003 What fraction of mutations reduces fitness? A reply to Keightley and Lynch. Evolution 57: 686-689.
48. SIEGAL, M. L., and A. BERGMAN, 2002 Waddington's canalization revisited: developmental stability and evolution. Proc. Natl. Acad. Sci. USA 99: 10528-10532.
49. SMITH, N. G., and A. EYRE-WALKER, 2002 Adaptive protein evolution in Drosophila. Nature 415: 1022-1024.
50. STEARNS, T., and D. BOTSTEIN, 1988 Unlinked noncomplementation: isolation of new conditional-lethal mutations in each of the tubulin genes of Saccharomyces cerevisiae. Genetics 119: 249-260.
51. SZAFRANIEC, K., D. M. WLOCH, P. SLIWA, R. H. BORTS and R. KORONA, 2003 Small fitness effects and weak genetic interactions between deleterious mutations in heterozygous loci of the yeast Saccharomyces cerevisiae. Genet. Res. 82: 19-31.
52. SZATHMARY, E., 1993 Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics 133: 127-132.
53. THATCHER, J. W., J. M. SHAW and W. J. DICKINSON, 1998 Marginal fitness contributions of nonessential genes in yeast. Proc. Natl. Acad. Sci. USA 95: 253-257.
54. WAGNER, A., 2000 Robustness against mutations in genetic networks of yeast. Nat. Genet. 24: 355-361.
55. WAGNER, G. P., M. D. LAUBICHLER and H. BAGHERI-CHAICHIAN, 1998 Genetic measurement of theory of epistatic effects. Genetica 102-103: 569-580.
56. WAXMAN, D., and J. J. WELCH, 2005 Fisher's microscope and Haldane's ellipse. Am. Nat. 166: 447-457.
57. WEST, S. A., A. D. PETERS and N. H. BARTON, 1998 Testing for epistasis between deleterious mutations. Genetics 149: 435-444.
58. WHITLOCK, M. C., and D. BOURGUET, 2000 Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54: 1654-1660.
59. WILLETT, C. S., 2006 Deleterious epistatic interactions between electron transport system protein-coding loci in the copepod Tigriopus californicus. Genetics 173: 1465-1477.
60. WLOCH, D., R. BORTS and R. KORONA, 2001a Epistatic interactions of spontaneous mutations in haploid strains of the yeast Saccharomyces cerevisiae. J. Evol. Biol. 14: 310-316.
61. WLOCH, D. M., K. SZAFRANIEC, R. H. BORTS and R. KORONA, 2001b Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics 159: 441-452.
62. WOLF, W. B., E. D. I. BRODIE and M. J. WADE, 2000 Epistasis and the Evolutionary Process. Oxford University Press, Oxford.
63. YOOK, K. J., S. R. PROULX and E. M. JORGENSEN, 2001 Rules of non-allelic noncomplementation at the synapse in Caenorhabditis elegans. Genetics 158: 209-220.
64. ZEYL, C., and J. A. DEVISSER, 2001 Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae. Genetics 157: 53-61.