Fisher's Geometric Model Of Adaptation Meets The Functional Synthesis: Data On Pairwise Epistasis For Fitness Yields Insights Into The Shape And Size Of Phenotype Space

Evolution

Volumn 67, Issue 10, 2013, Pages 2957-2972

  Weinreich, Daniel M ^a,b   Knies, Jennifer L ^a  

^a BROWN UNIVERSITY   (United States)

^b CHRISTOPHER NEWPORT UNIVERSITY   (United States)

Author keywords

Adaptation; Epistasis; Fitness; Models simulations; Mutations; Pleiotropy

Indexed keywords

BIOCHEMISTRY; DATA SET; EPISTASIS; FITNESS; MUTATION; NUMERICAL MODEL; PHENOTYPE; PLEIOTROPY; PROTEIN;

PROTEIN;

ADAPTATION; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; EPISTASIS; EVOLUTION; FITNESS; GENETICS; MODELS/SIMULATIONS; MUTATION; MUTATIONS; NONPARAMETRIC TEST; PHENOTYPE; PLEIOTROPY; POPULATION GENETICS; REPRODUCTIVE FITNESS;

ADAPTATION; EPISTASIS; FITNESS; MODELS/SIMULATIONS; MUTATIONS; PLEIOTROPY;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; COMPUTER SIMULATION; EPISTASIS, GENETIC; GENETIC FITNESS; GENETICS, POPULATION; MODELS, GENETIC; MUTATION; PHENOTYPE; PROTEINS; STATISTICS, NONPARAMETRIC;

EID: 84885051509     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12156     Document Type: Article

References (80)

1. Ambler, R. P., A. F. W. Coulson, J.-M. Frère, J.-M. Ghuysen, B. Joris, M. Forsman, R. C. Levesque, G. Tiraby, and S. G. Waley 1991. A standard numbering scheme for the Class A β-lactamases. Biochem. J. 276:269-272.
2. Avery, L., and S. Wasserman 1992. Ordering gene function: the interpretation of epistasis in regulatory hierarchies. Trends Genet. 8:312-316.
3. Bateson, W. 1909. Mendel's principles of heredity. Cambridge Univ. Press, Cambridge, U.K.
4. Bloom, J. D., J. J. Silberg, C. O. Wilke, D. A. Drummond, C. Adami, and F. H. Arnold 2005. Thermodynamic prediction of protein neutrality. Proc. Natl. Acad. Sci. USA 102:606-611.
5. Bonhoeffer, S., C. Chappey, N. T. Parkin, J. M. Whitcomb, and C. J. Petropolous 2004. Evidence for positive epistasis in HIV-1. Science 306:1547-1550.
6. Bridgham, J. T., S. M. Carroll, and J. W. Thornton 2007. Evolution of hormone-receptor complexity by molecular exploitation. Science 312:97-100.
7. Brodie, E. D., III. 2000. Why evolutionary genetics does not always add up. Pp. 3-20 in J. B. Wolf, E. D. Brodie, III, and M. J. Wade, eds. Epistasis and the evolutionary process. Oxford Univ. Press, New York.
8. Brown, K. M., M. A. DePristo, D. M. Weinreich, and D. L. Hartl 2009. Temporal constraints on the incorporation of regulatory mutants in evolutionary pathways. Mol. Biol. Evol. 26:2455-2462.
9. Burch, C. L., and L. Chao 1999. Evolution by small steps and rugged landscapes in the RNA virus ø6. Genetics 151:921-927.
10. Camps, M., A. Herman, E. Loh, and L. A. Loeb 2007. Genetic constraints on protein evolution. Crit. Rev. Biochem. Mol. Biol. 42:313-326.
11. Chevin, L.-M., G. Martin, and T. Lenormand 2010. Fisher's model and the genomics of adaptation: restricted pleiotropy, heterogeneous mutation, and parallel evolution. Evolution 64:3213-3231.
12. Costanzo, M., A. Baryshnikova, J. Bellay, Y. Kim, E. D. Spear, C. S. Sevier, H. Ding, J. L. Y. Koh, K. Toufighi, S. Mostafavi, et al. 2010. The genetic landscape of a cell. Science 327:425-431.
13. Darwin, C. 1859. On the origin of species by means of natural selection. John Murray, Lond.
14. de Visser, J. A. G. M., S.-C. Park, and J. Krug 2009. Exploring the effect of sex on empirical fitness landscapes. Am. Nat. 174:S15-S30.
15. Dean, A. M., and J. W. Thornton 2007. Mechanistic approaches to the study of evolution: the functional synthesis. Nat. Rev. Genet. 8:675-688.
16. DePristo, M. A., D. M. Weinreich, and D. L. Hartl 2005. Missense meandering through sequence space: a biophysical perspective on protein evolution. Nat. Rev. Genet. 6:678-687.
17. Elena, S. F., and R. E. Lenski 1997a. Data from: test of synergistic interactions among deleterious mutations in bacteria. doi:10.5061/dryad.rg8mb.
18. Elena, S. F., and R. E. Lenski 1997b. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390:395-397.
19. Fisher, R. A. 1930. The genetical theory of natural selection. Clarendon Press, Oxford, U.K.
20. Griffiths, A. J. F., W. M. Gelbart, R. C. Lewontin, and J. Miller 2002. Modern genetic analysis: integrating genes and chromosomes. W.H. Freeman, New York.
21. Gu, X. 2007. Evolutionary framework for protein sequence evolution and gene pleiotropy. Genetics 175:1813-1822.
22. Hartl, D. L., and C. H. Taubes 1996. Compensatory nearly neutral mutations: selection without adaptation. J. Theor. Biol. 182:303-309.
23. Hartl, D. L., and C. H. Taubes 1998. Toward a theory of evolutionary adaptation. Genetica 102/103:525-533.
24. He, X., W. Qian, Z. Wang, Y. Li, and J. Zhang 2010. Prevalent positive epistasis in Escherichia coli and Saccharomyces cerevisiae metabolic networks. Nature Genet. 42:272-276.
25. Huang, W., and T. Palzkill 1997. A natural polymorphism in β-lactamase is a global suppressor. Proc. Natl. Acad. Sci. USA 94:8801-8806.
26. Kacser, H., and J. Burns 1973. The control of flux. Symp. Soc. Exp. Biol. 27:65-104.
27. Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge Univ. Press, Cambridge, U.K.
28. Kimura, M., and T. Maruyama 1966. The mutational load with epistatic gene interactions in fitness. Genetics 54:1337-1351.
29. Kondrashov, A. S. 1988. Deleterious mutations and the evolution of sex. Nature 336:435-440.
30. Lande, R. 1980. The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94:203-215.
31. Lapedes, A., and R. Farber 2001. The geometric of shape space: application to influenza. J. Theor. Biol. 212:57-69.
32. Le Nagard, H., L. Chao, and O. Tenaillon 2011. The emergence of complexity and restricted pleiotropy in adapting networks. BMC Evol. Biol. 11:326.
33. Lourenço, J., N. Galtier, and S. Glémin 2011. Complexity, pleiotropy, and the fitness effect of mutations. Evolution 65:1559-1571.
34. Lozevsky, E. R., T. Chookajorn, K. M. Brown, M. Imwong, P. J. Shaw, S. Kamchonwongpaisan, D. E. Neafsey, D. M. Weinreich, and D. L. Hartl 2009. Stepwise acquisition of pyrimethamine resistance in the malaria parasite. Proc. Natl. Acad. Sci. 106:12025-12030.
35. Lunzer, M., A. Natarajan, D. E. Dykuisen, and A. M. Dean 2002. Enzyme kinetics, substitutable resources and competition: from biochemistry to frequency-dependent selection in lac. Genetics 162:485-499.
36. Lunzer, M., S. P. Miller, R. Felsheim, and A. M. Dean 2005a. The biochemical architecture of an ancient adaptive landscape. Science 310:499-501.
37. Lunzer, M., S. P. Miller, R. Felsheim, and A. M. Dean 2005b. Data from: the biochemical architecture of an ancient adaptive landscape. doi:10.5061/dryad.7nd70.
38. Mackay, T. F. C. 2001. Quantitative trait loci in Drosophila. Nat. Rev. Genet. 2:11-20.
39. MacLean, R. C., G. G. Perron, and A. Gardner 2010. Diminishing returns from beneficial mutations and pervasive epistasis shape the fitness landscape for Rifampicin resistance in Pseudomonas aeruginosa. Genetics 186:1345-1354.
40. Malcolm, B. A., K. P. Wilson, B. W. Matthews, J. F. Kirsch, and A. C. Wilson 1990. Ancestral lysozymes reconstructed, neutrality tested, and thermostability linked to hydrocarbon packing. Nature 345:86-89.
41. Martin, G., and T. Lenormand 2006. A general multivariate extension of Fisher's geometric model and the distribution of fitness effects across species. Evolution 60:893-907.
42. 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.
43. Orencia, M. C., J. S. Yoon, J. E. Ness, W. P. C. Stemmer, and R. D. Stevens 2001. Predicting the emergence of antibiotic resistance by directed evolution and structural analysis. Nat. Struct. Biol. 8:238-242.
44. Orr, H. A. 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52:935-949.
45. Orr, H. A. 1999. The evolutionary genetics of adaptation: a simulation study. Genet Res 74:207-214.
46. Orr, H. A. 2005a. The genetic theory of adaptation: a brief history. Nature Rev. Genet. 6:119-127.
47. Orr, H. A. 2005b. Theories of adaptation: what they do and don't say. Genetica 123:3-13.
48. 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.
49. Perelson, A. S., and G. F. Oster 1979. Theoretical studies of clonal selection: minimal antibody repertoire size and reliability of self-non-self discrimination. J. Theor. Biol. 81:645-670.
50. Phillips, P. C. 1998. The language of gene interaction. Genetics 149:1167-1171.
51. Phillips, P. C. 2008. Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 9:855-867.
52. Poon, A., and S. P. Otto 2000. Compensating for our load of mutations: freezing the meltdown of small populations. Evolution 54:1467-1479.
53. Raquet, X., J. Lamotte-Brasseur, E. Fonzé, S. Goussard, P. Courvalin, and J.-M. Frère 1994. TEM β-lactamase mutants hydrolysing third-generation cephalosporins. J. Mol. Biol. 2444:625-639.
54. Raquet, X., M. Vanhove, J. Lamotte-Brasseur, S. Goussard, P. Courvalin, and J.-M. Frère 1995. Stability of TEM β-lactamase mutants hydrolyzing third generation cephalosporins. Proteins 23:63-72.
55. Rice, S. H. 2000. The evolution of developmental interactions. Pp. 82-98 in J. B. Wolf, E. D. I. Brodie and M. J. Wade, eds. Epistasis and the evolutionary process. Oxford Univ. Press, Oxford, U.K.
56. Rokyta, D. R., P. Joyce, S. B. Caudle, C. Miller, C. J. Beisel, and H. A. Wichman 2011. Epistasis between beneficial mutations and the phenotype-to-fitness map for a ssdna virus. PLoS Genet. 7:e1002075.
57. Roth, F. P., H. D. Lipshitz, and B. J. Andrews 2009. Q&A: epistasis. J. Biol. 8:35.
58. Salverda, M. M., E. Dellus, F. A. Gorter, A. J. M. debets, J. van der Oost, R. F. Hoekstra, D. S. Tawfik, and J. A. G. M. de Visser 2011. Initial mutations direct alternative pathways of protein evolution. PLoS Genet. 7:e1001321.
59. Sanjuán, R., A. Moya, and S. F. Elena 2004. The contribution of epistasis to the architecture of fitness in an RNA virus. Proc. Natl. Acad. Sci. 101:15376-15379.
60. Segrè, D., A. DeLuna, G. M. Church, and R. Kishony 2005. Modular epistasis in yeast metabolism. Nat. Genet. 37:77-83.
61. Sella, G. 2009. An exact steady state solution of Fisher's geometric model and other models. Theor. Popul. Biol. 75:30-34.
62. Sellis, D., B. J. Callahan, D. A. Petrov, and P. W. Messer 2011. Heterozygote advantage as a natural consequence of adaptation in diploids. Proc.Natl. Acad. Sci. 108:20666-20671.
63. Sideraki, V., W. Huang, T. Palzkill, and H. F. Gilbert 2001. A secondary drug resistance mutation of TEM-1 β-lactamase that suppresses misfolding and aggregation. Proc. Natl. Acad. Sci. USA 98:283-288.
64. Sokal, R. R., and F. J. Rohlf 1995. Biometry. W.H. Freeman and Company, New York.
65. Szathmáry, E. 1993. Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics 133:127-132.
66. Tenaillon, O., O. K. Silander, J.-P. Uzan, and L. Chao 2007. Quantifying organismal complexity using a population genetic approach. PLoS One 2:e217.
67. Tokuriki, N., F. Stricher, L. Serrano, and D. S. Tawfik 2008. How protein stability and new functions trade off. PLoS Comp. Biol. 4:e1000002.
68. Tomatis, P. E., R. M. Rasia, L. Segovia, and A. J. Vila 2005. Mimicking natural selection in metallo-β-lactamases through second-shell ligand mutations. Proc. Natl. Acad. Sci. USA 102:13761-13766.
69. Trindade, S., A. Sousa, K. B. Xavier, F. Dionisio, M. G. Ferreira, and I. Gordo 2009a. Data from: positive epistasis drives the acquisition of multidrug resistance. doi:10.5061/dryad.20k7j.
70. Trindade, S., A. Sousa, K. B. Xavier, F. Dionisio, M. G. Ferreira, and I. Gordo 2009b. Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet. 5:e1000578.
71. Wang, Z., G. Minasov, and B. K. Shoichet 2002. Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J. Mol. Biol. 320:85-95.
72. Waxman, D. 2006. Fisher's geometric model of evolutionary adaptation-beyond spherical geometry. J. Theor. Biol. 241:887-895.
73. Waxman, D., and J. J. Welch 2005. Fisher's microscope and Haldane's ellipse. Am. Nat. 166:447-457.
74. Weinreich, D. M. 2010. Predicting molecular evolutionary trajectories in principle and in practice. Encyclopedia of life sciences (ELS). John Wiley & Sons, Chichester, U.K.
75. Weinreich, D. M., N. F. Delaney, M. A. DePristo, and D. L. Hartl 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111-114.
76. Weinreich, D. M., R. A. Watson, and L. Chao 2005. Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165-1174.
77. Welch, J. J., and D. Waxman 2003. Modularity and the cost of complexity. Evolution 57:1723-1734.
78. Yokoyama, S., H. Yang, and W. T. Starmer 2008. Molecular basis of spectral tuning in the red- and green-sensitive (M/LWS) pigments in vertebrates. Genetics 179:2037-2043.
79. Zeldovich, K. B., P. Q. Chen, and E. I. Shakhnovich 2007. Protein stability imposes limits on organism complexity and speed of molecular evolution. Proc. Natl. Acad. Sci. 104:16152-16157.
80. Zhou, H.-Z., S. T. Wlodek, and J. A. McCammon 1998. Conformational gating as a mechanism for enzyme specificity. Proc. Natl. Acad. Sci. USA 95:9280-9283.