Long-term adaptation of epistatic genetic networks

Evolution

Volumn 62, Issue 9, 2008, Pages 2215-2235

  Yukilevich, Roman ^a   Lachance, Joseph ^a   Aoki, Fumio ^a   True, John R ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Adaptive walks; Antagonistic epistasis; Constraint; Evolutionary theory; Individual based simulation; Mutation; Sign epistasis; Synergistic epistasis

Indexed keywords

EPISTASIS; EVOLUTIONARY BIOLOGY; EVOLUTIONARY THEORY; FITNESS; GENETIC VARIATION; INDIVIDUAL-BASED MODEL; MUTATION; SYNERGISM;

ADAPTATION; ALLELE; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENE REGULATORY NETWORK; GENETIC EPISTASIS; GENETIC SELECTION; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MUTATION; TIME;

ADAPTATION, BIOLOGICAL; ALLELES; COMPUTER SIMULATION; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; GENE REGULATORY NETWORKS; MODELS, GENETIC; MUTATION; SELECTION (GENETICS); TIME FACTORS; VARIATION (GENETICS);

EID: 51249107149     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00445.x     Document Type: Article

References (96)

1. Azevedo, B. R., R. Lohaus, S. Srinivasan, K. K. Dang, and C. L. Burch. 2006. Sexual reproduction selects for robustness and negative epistasis in artificial gene networks. Nature 440 : 87 90.
2. Bohannan, B. J. M., M. Travisano, and R. E. Lenski. 1999. Epistatic interactions can lower the cost of resistance to multiple consumers. Evolution 53 : 292 295.
3. Barton, N. 1995. Linkage and the limits to natural selection. Genetics 140 : 821 841.
4. Beerenwinkel, N., L. Pachter, B. Sturmfels, S. F. Elena, and R. E. Lenski. 2007. Analysis of epistatic interactions and fitness landscapes using a new geometric approach. BMC Evol. Biol. 7 : 60.
5. Brodie, E. D. I. 2000. Why evolutionary genetics does not always add up. Pp. 3 19 in J. B. Wolf, E. D. B., and Wade, M. J., eds. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford.
6. Carlborg, O., and C. S. Haley. 2004. Epistasis: too often neglected in complex trait studies? Nat. Rev. Genet. 5 : 618 625.
7. Carter, A. J., J. Hermisson, and T. F. Hansen. 2005. The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theor. Popul. Biol. 68 : 179 196.
8. Chambers, D. M., J. Peters, and C. M. Abbott. 1998. The lethal mutation of the mouse wasted (wst) is a deletion that abolishes expression of a tissue-specific isoform of translation elongation factor 1alpha, encoded by the Eef1a2 gene. Proc. Natl. Acad. Sci. USA 95 : 4463 4468.
9. Cheverud, J. M., and E. J. Routman. 1995. Epistasis and its contribution to genetic variance components. Genetics 139 : 1455 1461.
10. Desai, M. M., Weissman, D., and Feldman, M. W. 2007. Evolution can favor antagonistic epistasis. Genetics 177 : 1001 1010.
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. Elena, S. F., and R. E. Lenski. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4 : 457 469.
13. Ewens, W. J. 1979. Mathematical population genetics. Springer, New York.
14. Eyre-Walker, A., and P. D. Keightley. 2007. The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8 : 610 618.
15. Eyre-Walker, A., M. Woolfit, and T. Phelps. 2006. The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173 : 891 900.
16. Falconer, D. S. and T. Mackay. 1996. Introduction to quantitative genetics. Longman Group Ltd, Harlow, UK.
17. Featherstone, D. E., and K. Broadie. 2002. Wrestling with pleiotropy: genomic and topological analysis of the yeast gene expression network. Bioessays 24 : 267 274.
18. Fedorowicz, G. M., J. D. Fry, R. R. Anholt, and T. F. Mackay. 1998. Epistatic interactions between smell-impaired loci in Drosophila melanogaster. Genetics 148 : 1885 1891.
19. Felsenstein, J. 1965. The effect of linkage on directional selection. Genetics 52 : 349 363.
20. Fisher, R. A. 1930. The genetical theory of natural selection. Oxford Univ. Press, Oxford.
21. Fontana, W., P. F. Stadler, E. G. Bornberg-Bauer, T. Griesmacher, I. L. Hofacker, M. Tacker, P. Tarazona, E. D. Weinberger, and P. Schuster. 1993. RdA folding and combinatory landscapes. Phys. Rev.:E. 47 : 2083 2099.
22. Franklin, I., and R. C. Lewontin. 1970. Is the gene the unit of selection? Genetics 65 : 707 734.
23. Fraser, H. B., A. E. Hirsh, L. M. Steinmetz, C. Scharfe, and M. W. Feldman. 2002. Evolutionary rate in the protein interaction network. Science 296 : 750 752.
24. Gavrilets, S. 2004. Fitness landscapes and the origin of species. Princeton Univ. Press, Princeton NJ.
25. Gavrilets, S., and G. de Jong. 1993. Pleiotropic models of polygenic variation, stabilizing selection, and epistasis. Genetics 134 : 609 625.
26. Gillespie, J. H. 1974. Natural selection for within-generation variance in offspring number. Genetics. 76 : 601 606.
27. Gillespie, J. H. 1983. A simple stochastic gene substitution model. Theor. Popul. Biol. 23 : 202 215.
28. Gillespie, J. H. 1984. Molecular evolution over the mutational landscape. Evolution 38 : 1116 1139.
29. Gillespie, J. H. 1991. The causes of molecular evolution. Oxford Univ. Press, Oxford.
30. Gillespie, J. H. 1994. Substitution processes in molecular evolution. III. Deleterious alleles. Genetics 138 : 943 952.
31. Gimelfarb, A. 1989. Genotypic variation for a quantitative character maintained understabilizing selection without mutations: epistasis. Genetics 123 : 217 227.
32. Goodnight, C. J. 1995. Epistasis and the increase in additive genetic variance: implications for phase 1 of Wright's shifting balance process. Evolution 49 : 502 511.
33. Goodnight, C. J. 2000. Modeling gene interactions in structured populations. Pp. 129 145 in J. B. Wolf, E.D., B. and Wade, M. J., eds. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford.
34. Hahn, M. W., G. C. Conant, and A. Wagner. 2004. Molecular evolution in large genetic networks: does connectivity equal constraint? J. Mol. Evol. 58 : 203 211.
35. Haldane, J. B. S. 1927. A mathematical theory of natural and artificial selection. Proc. Camp. Philos. Soc. 23 : 838 844.
36. Hansen, T. F., and G. P. Wagner. 2001. Modeling genetic architecture: a multilinear theory of gene interaction. Theor. Popul. Biol. 59 : 61 86.
37. Hansen, T. F. and D. Houle. 2004. Evolvability, stabilizing selection, and the problem of stasis. Pp. 130 150 in M. Pigliucci, Pigliucci, K., ed. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford Univ. Press, Oxford, UK.
38. Hansen, T. F., J. M. Alvarez-Castro, A. J. Carter, J. Hermisson, and G. P. Wagner. 2006. Evolution of genetic architecture under directional selection. Evolution 60 : 1523 1536.
39. Hartl, D. L., D. D. Dykhuizen, and K. M. Dean. 1985. Limits of adaptation. The evolution of selective neutrality. Genetics 111 : 655 674.
40. Hermisson, J., T. F. Hansen, and G. P. Wagner. 2003. Epistasis in polygenic traits and the evolution of genetic architecture under stabilizing selection. Am. Nat. 161 : 708 734.
41. Jeong, H., S. P. Mason, A. L. Barabasi, and Z. N. Oltvai. 2001. Lethality and centrality in protein networks. Nature 411 : 41 42.
42. Johnson, N. A. 2000. Gene interactions and the origin of species. Pp. 197 212 in J. B. Wolf, E. D., B and Wade, M. J., eds. Epistasis and the evolutionary process. Oxford Press, Oxford UK.
43. Johnson, N. A., and Porter, A. H. 2000. Rapid speciation via parallel, directional selection on regulatory genetic pathways. J. Theor. Biol. 205 : 527 542
44. Kassen, R., and T. Bataillon. 2006. Distribution of fitness effects among beneficial mutations before selection in experimental populations of bacteria. Nat. Genet. 38 : 484 488.
45. Kauffman, S. A. 1993. The origins of order: self-organization and selection in evolution. Oxford Univ. Press, Oxford, UK.
46. Kauffman, S. A., and S. Levin. 1987. Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol. 128 : 11 45.
47. Kauffman, S. A., and Weinberger. 1989. The NK model of rugged fitness landscapes and its application to the maturation of the immune response. J. Theor. Biol. 141 : 211 245.
48. Kimura, M. 1954. Process leading to quasi-fixation of genes in natural populations due to random fluctuation of selection intensities. Genetics 39 : 280 295.
49. Kimura, M. 1962. On the probability of fixation of mutant genes in a population. Genetics 47 : 713 719.
50. Kingman, J. F. C., 1978. A simple model for the balance between selection and mutation. J. Appl. Prob. 15 : 1 12.
51. Lenski, R. E., and Travisano M. 1994. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl. Acad. Sci. USA 91 : 6808 6814.
52. Lewontin, R. C. 1974. The genetic basis of evolutionary change. Columbia Univ. Press, NY.
53. Lewontin, R. C. 1978. Adaptation. Sci. Am. 239 : 212 218, 220, 222 passim.
54. Lynch, M, and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer Assoc., Inc. Sunderland, MA.
55. Mackay, T. F. 2001. Quantitative trait loci in Drosophila. Nat. Rev. Genet. 2 : 11 20.
56. Malmberg, R. L. 1977. Evolution of epistasis and advantage of recombination in populations of bacteriophage T4. Genetics 86 : 607 621.
57. Malmberg, R. L., and R. Mauricio. 2005. QTL-based evidence for the role of epistasis in evolution. Genet. Res. 86 : 89 95.
58. Martin, G., S. F. Elena, and T. Lenormand. 2007. Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nat. Genet. 39 : 555 560
59. Maynard Smith, J. 1970. Natural selection and the concept of a protein space. Nature 225 : 563 564.
60. Mayr, E. 1959. Where are we? Cold Spring Harbor Symp. Quant. Biol. 24 : 1 14.
61. Mayr, E. 1963. Animal species and evolution. Belknap Press, Cambridge, MA.
62. Misevic, D., Ofria, C., and Lenski, R. E. 2006. Sexual reproduction reshapes the genetic architecture of digital organisms. Proc. R. Soc. Lond. B. 273 : 457 464.
63. Nielsen, R., and Z. Yang. 2003. Estimating the distribution of selection coefficients from phylogenetic data with applications to mitochondrial and viral DNA. Mol. Biol. Evol. 20 : 1231 1239.
64. Ohta, T. 1977. Extension of the neutral mutation drift hypothesis. Pp. 148 167 in M. Kimura ed., Molecular evolution and polymorphism. National Institute of Genetics, Mishima.
65. Ohta, T. 1997. Role of random genetic drift in the evolution of interactive systems. J. Mol. Evol. 44 : S9 S14.
66. Ohta, T. 1998. Evolution by nearly-neutral mutations. Genetica 102/103 : 83 90.
67. Orr, A. H. 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52 : 935 949.
68. Orr, A. H. 2002. The population genetics of adaptation: the adaptation of DNA sequences. Evolution 56 : 1317 1330.
69. Orr, A. H. 2006. The population genetics of adaptation on correlated fitness landscapes: the block model. Evolution 60 : 1113 1124.
70. Phillips, P. C. 1996. Waiting for a compensatory mutation: phase zero of the shifting balance process. Genetical Research 67 : 271 283.
71. Phillips, P. C. 1998. The language of gene interaction. Genetics 149 : 1167 1171.
72. Phillips, P. C., Otto, S. P. and Whitlock, M. C. 2000. Beyond the average, the evolutionary importance of gene interactions and variability of epistatic effects. Pp. 20 38 in J. B. Wolf, E. D. Brodie III. and Wade, M. J., ed. Epistasis and the evolutionary process. Oxford Univ, Oxford UK.
73. Porter, A. H., and Johnson, N. A. 2002. Speciation despite gene flow when developmental pathways evolve. Evolution 56 : 2103 2111
74. Sambandan, D., A. Yamamoto, J. J. Fanara, T. F. Mackay, and R. R. Anholt. 2006. Dynamic genetic interactions determine odor-guided behavior in Drosophila melanogaster. Genetics 174 : 1349 1363.
75. Sanjuan, R., and S. F. Elena. 2006. Epistasis correlates to genomic complexity. Proc. Natl. Acad. Sci. USA 103 : 14402 14405.
76. Sanjuan, R., A. Moya, and S. F. Elena. 2004. The contribution of epistasis to the architecture of fitness in an RdA virus. PdAS 101 : 15,376 15379.
77. Siegal, M. L., D. E. Promislow, and A. Bergman. 2007. Functional and evolutionary inference in gene networks: does topology matter? Genetica 129 : 83 103.
78. Sokal, R. R., and J. F. Rohlf. 1995. Biometry. W. H. Freeman and Company, New York.
79. Threadgill, D. W., A. A. Dlugosz, L. A. Hansen, T. Tennenbaum, U. Lichti, D. Yee, C. LaMantia, T. Mourton, K. Herrup, R. C. Harris, et al. 1995. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269 : 230 234.
80. van Swinderen, B., and R. J. Greenspan. 2005. Flexibility in a gene network affecting a simple behavior in Drosophila melanogaster. Genetics 169 : 2151 2163.
81. Wade, M. J. 1992. Sewall Wright: gene interaction and the shifting balance theory. Pp. 35 62 in D. J. Futuyma and J. Antonovics, ed. Oxford surveys in evolutionary biology. Oxford Univ. Press, Oxford.
82. Wade, M. J. 2000. Epistasis as a genetic constraint within populations and an accelerant of adaptive divergence among them. Pp. 20 38 in J. B. Wolf, E. D. Brodie III. and Wade, M. J., ed. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford, UK.
83. Wade, M. J. 2002. A gene's eye view of epistasis, selection and speciation. J. Evol. Biol. 15 : 337 346.
84. Wagner, G. 2002. To epistasis - and beyond. Evolution 56 : 852 855.
85. Weinberger, E. D. 1990. Correlated and uncorrelated fitness landscapes and how to tell the difference. Biol. Cybern. 63 : 325 336.
86. Weinreich, D. M. 2005. The rank ordering of genotypic fitness values predicts genetic constraint on natural selection on landscapes lacking sign epistasis. Genetics 171 : 1397 1405.
87. Weinreich, D. M., and L. Chao. 2005. Rapid evolutionary escape by large populations from local fitness peaks is likely in nature. Evolution 59 : 1175 1182.
88. Weinreich, D. M., R. A. Watson, and L. Chao. 2005. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59 : 1165 1174.
89. Welch, J. J. and Waxman, D. 2005. The NK model and population genetics. J. Theor. Biol. 234 : 329 340.
90. Wilke, C. O. and C. Adami. 2001. Interaction between directional epistasis and average mutational effects. Proc. R. Soc. Lond. B 268 : 1469 1474.
91. Whitlock, M. C., P. C. Phillips, F. B.-G. Moore, and S. J. Tonsor. 1995. Multiple fitness peaks and epistasis. Annu. Rev. Ecol. Syst. 26 : 601 629.
92. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16 : 97 159.
93. Wright, S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc. Sixth Inter. Congr. Genet. 1 : 356 366.
94. Wright, S. 1949. Adaptation and selection. Pp. 365 389 in G. G. S. G. L. Jepsen, and E. Mayr. ed. Genetics, paleontology and evolution. Princeton Univ. Press, Princeton, NJ.
95. Wright, S. 1969. Evolution and the genetics of populations. Univ. Chicago Press, Chicago.
96. Zhivotovsky, L. A. and Gavrilets, S. 1992. Quantitative variability and multilocus polymorphism under stabilizing selection. Theor. Popul. Biol. 42 : 254 283.