Neutralism and selectionism: A network-based reconciliation

Nature Reviews Genetics

Volumn 9, Issue 12, 2008, Pages 965-974

  Wagner, Andreas ^a,b,c,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c SANTA FE INSTITUTE   (United States)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN;

CANDIDA ALBICANS; EPISTASIS; EVOLUTIONARY ADAPTATION; GENE DUPLICATION; GENETIC DRIFT; HUMAN IMMUNODEFICIENCY VIRUS; MAXIMUM LIKELIHOOD METHOD; MOLECULAR EVOLUTION; MUTATION; NATURAL SELECTION; NONHUMAN; PHENOTYPE; POPULATION SIZE; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; ZINC FINGER MOTIF;

ANIMALS; EVOLUTION; EVOLUTION, MOLECULAR; GENETICS, POPULATION; GENOTYPE; HUMANS; MODELS, GENETIC; MUTATION; SELECTION (GENETICS);

EID: 56549087988     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg2473     Document Type: Review

References (111)

1. Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).
2. Kimura, M. & Ohta, T. On some principles governing molecular evolution. Proc. Natl Acad. Sci. USA 71, 2848-2852 (1974).
3. Mayr, E. Animal Species and Evolution (Belknap, Cambridge, Massachusetts, 1963).
4. Kreitman, M. The neutral theory is dead: long live the neutral theory. Bioessays 18, 678-683 (1996).
5. Ohta, T. The current significance and standing of neutral and nearly neutral theories. Bioessays 18, 673-684 (1996).
6. Nei, M. Selectionism and neutralism in molecular evolution. Mol. Biol. Evol. 22, 2318-2342 (2005).
7. Lynch, M. The Origins of Genome Architecture (Sinauer, Sunderland, Massachusetts, 2007).
8. McDonald, J. H. & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652-654 (1991).
9. Gillespie, J. H. The Causes of Molecular Evolution (Oxford Univ. Press, New York, 1991).
10. Akashi, H. Inferring weak selection from patterns of polymorphism and divergence at silent sites in Drosophila DNA. Genetics 139, 1067-1076 (1995).
11. Fay, J. C., Wyckoff, G. J. & Wu, C. I. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415, 1024-1026 (2002).
12. Smith, N. G. C. & Eyre-Walker, A. Adaptive protein evolution in Drosophila. Nature 415, 1022-1024 (2002).
13. Bierne, N. & Eyre-Walker, A. The genomic rate of adaptive amino acid substitution in Drosophila. Mol. Biol. Evol. 21, 1350-1360 (2004).
14. Sawyer, S. A., Kulathinal, R. J., Bustamante, C. D. & Hartl, D. L. Bayesian analysis suggests that most amino acid replacements in Drosophila are driven by positive selection. J. Mol. Evol. 57, S154-S164 (2003).
15. Shapiro, J. A. et al. Adaptive genic evolution in the Drosophila genomes. Proc. Natl Acad. Sci. USA 104, 2271-2276 (2007).
16. Andolfatto, P. Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Res. 17, 1755-1762 (2007).
17. Begun, D. J. et al. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PloS Biol. 5, 2534-2559 (2007).
18. Andolfatto, P. Adaptive evolution of non-coding DNA in Drosophila. Nature 437, 1149-1152 (2005).
19. Kohn, M. H., Fang, S. & Wu, C. I. Inference of positive and negative selection on the 5′ regulatory regions of Drosophila genes. Mol. Biol. Evol. 21, 374-383 (2004).
20. Charlesworth, J. & Eyre-Walker, A. The rate of adaptive evolution in enteric bacteria. Mol. Biol. Evol. 23, 1348-1356 (2006).
21. Akashi, H. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics 151, 221-238 (1999).
22. Hahn, M. W. Toward a selection theory of molecular evolution. Evolution 62, 255-265 (2008).
23. Gillespie, J. H. Is the population size of a species relevant to its evolution? Evolution 55, 2161-2169 (2001).
24. Maynard Smith, J. & Haigh, J. The hitch-hiking effect of a favorable gene. Genet. Res. 23, 23-35 (1974).
25. Schultes, E. & Bartel, D. One sequence, two ribozymes: implications for the emergence of new ribozyme folds. Science 289, 448-452 (2000).
26. Smith, D. J. et al. Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371-376 (2004).
27. Koelle, K., Cobey, S., Grenfell, B. & Pascual, M. Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science 314, 1898-1903 (2006).
28. Bloom, J. D., Labthavikul, S. T., Otey, C. R. & Arnold, F. H. Protein stability promotes evolvability. Proc. Natl Acad. Sci. USA 103, 5869-5874 (2006).
29. Aharoni, A. et al. The 'evolvability' of promiscuous protein functions. Nature Genet. 37, 73-76 (2005).
30. Bloom, J., Romero, P., Lu, Z. & Arnold, F. Neutral genetic drift can alter promiscuous protein functions, potentially aiding functional evolution. Biol. Direct 2, 17 (2007).
31. Amitai, G., Gupta, R. & Tawfik, D. Latent evolutionary potentials under the neutral mutational drift of an enzyme HFSP J. 1, 67-78 (2007).
32. Bloom, J. D. et al. Thermodynamic prediction of protein neutrality. Proc. Natl Acad. Sci. USA 102, 606-611 (2005).
33. England, J. L. & Shakhnovich, E. I. Structural determinant of protein designability. Phys. Rev. Lett. 90, 218101 (2003).
34. Ferrada, E. & Wagner, A. Protein robustness promotes evolutionary innovations on large evolutionary time scales. Proc. Roy. Soc. Lond. B. 275,1595-1602 (2008).
35. Shakhnovich, B. E., Deeds, E., Delisi, C. & Shakhnovich, E. Protein structure and evolutionary history determine sequence space topology. Genome Res. 15, 385-392 (2005).
36. Ginsberg, A. M., King, B. O. & Roeder, R. G. Xenopus 5S gene transcription factor, TFIIIA: characterization of a cDNA clone and measurement of RNA levels throughout development. Cell 39, 479-489 (1984).
37. Michael, S. F., Kilfoil, V. J., Schmidt, M. H., Amann, B. T. & Berg, J. M. Metal binding and folding properties of a minimalist Cys2His2 Zinc finger peptide. Proc. Natl Acad. Sci. USA 89, 4796-4800 (1992).
38. Durai, S. et al. Zinc finger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res. 33, 5978-5990 (2005).
39. Venter, J. C. et al. The sequence of the human genome. Science 291, 1304-1351 (2001).
40. Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155 (2000).
41. Gu, Z. L., Cavalcanti, A., Chen, F. C., Bouman, P. & Li, W. H. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol. Biol. Evol. 19, 256-262 (2002).
42. Irish, V. F. & Litt, A. Flower development and evolution: gene duplication, diversification and redeployment. Curr. Opin. Genet. Dev. 15, 454-460 (2005).
43. Lemons, D. & McGinnis, W. Genomic evolution of Hox gene clusters. Science 313, 1918-1922 (2006).
44. Olson, E. Gene regulatory networks in the evolution and development of the heart. Science 313, 1922-1927 (2006).
45. Wagner, A. Gene duplications, robustness, and evolutionary innovations. Bioessays 30, 367-373 (2008).
46. Ohno, S. Evolution by Gene Duplication (Springer, New York, 1970).
47. Ciliberti, S., Martin, O. C. & Wagner, A. Circuit topology and the evolution of robustness in complex regulatory gene networks. PloS Comput. Biol. 3, e15 (2007).
48. Isalan, M. et al. Evolvability and hierarchy in rewired bacterial gene networks. Nature 452, 840-845 (2008).
49. Tsong, A. E., Tuch, B. B., Li, H. & Johnson, A. D. Evolution of alternative transcriptional circuits with identical logic. Nature 443, 415-420 (2006).
50. Wagner, A. Robustness and evolvability: a paradox resolved. Proc. Roy. Soc. Lond. B 275, 91-100 (2008).
51. Sumedha, Martin, O. C. & Wagner, A. New structural variation in evolutionary searches of RNA neutral networks. Biosystems. 90, 475-485. (2007).
52. Huynen, M. Exploring phenotype space through neutral evolution. J. Mol. Evol. 43, 165-169 (1996).
53. Ciliberti, S., Martin, O. C. & Wagner, A. Innovation and robustness in complex regulatory gene networks Proc. Natl Acad. Sci. USA 104, 13591-13596 (2007).
54. Fontana, W. & Schuster, P. Continuity in evolution: on the nature of transitions. Science 280, 1451-1455 (1998).
55. Elena, S. F., Cooper, V. S. & Lenski, R. E. Punctuated evolution caused by selection of rare beneficial mutations. Science 272, 1802-1804 (1996).
56. Cordell, H. J. Epistasis: what it means, what it doesn't mean, and statistical methods to detect it in humans. Hum. Mol. Genet. 11, 2463-2468 (2002).
57. Carlborg, O. & Haley, C. S. Epistasis: too often neglected in complex trait studies? Nature Rev. Genet. 5, 618-625 (2004).
58. Kulathinal, R. J., Bettencourt, B. R. & Hartl, D. L. Compensated deleterious mutations in insect genomes. Science 306, 1553-1554 (2004).
59. Kern, A. D. & Kondrashov, F. A. Mechanisms and convergence of compensatory evolution in mammalian mitochondrial tRNAs. Nature Genet. 36, 1207-1212 (2004).
60. Kondrashov, A. S., Sunyaev, S. & Kondrashov, F. A. Dobzhansky-Muller incompatibilities in protein evolution. Proc. Natl Acad. Sci. USA 99, 14878-14883 (2002).
61. Weinreich, D. M., Delaney, N. F., DePristo, M. A. & Hartl, D. L. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111-114 (2006).
62. Weinreich, D. M. & Chao, L. Rapid evolutionary escape by large populations from local fitness peaks is likely in nature. Evolution 59, 1175-1182 (2005).
63. DePristo, M. A., Hartl, D. L. & Weinreich, D. M. Mutational reversions during adaptive protein evolution. Mol. Biol. Evol. 24, 1608-1610 (2007).
64. Stephan, W. The rate of compensatory evolution. Genetics 144, 419-426 (1996).
65. Takahasi, K. R. & Tajima, F. Evolution of coadaptation in a two-locus epistatic system. Evolution 59, 2324-2332 (2005).
66. Cowperthwaite, M. C., Bull, J. J. & Meyers, L. A. From bad to good: fitness reversals and the ascent of deleterious mutations. PloS Comput. Biol. 2, 1292-1300 (2006).
67. Wilke, C. O., Lenski, R. E. & Adami, C. Compensatory mutations cause excess of antagonistic epistasis in RNA secondary structure folding. BMC Evol. Biol. 3, 3 (2003).
68. Weinreich, D. M., Watson, R. A. & Chao, L. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59, 1165-1174 (2005).
69. DePristo, M. A., Weinreich, D. M. & Hartl, D. L. Missense meanderings in sequence space: a biophysical view of protein evolution. Nature Rev. Genet. 6, 678-687 (2005).
70. Tokuriki, N., Stricher, F., Schymkowitz, J., Serrano, L. & Tawfik, D. S. The stability effects of protein mutations appear to be universally distributed. J. Mol. Biol. 369, 1318-1332 (2007).
71. Bershtein, S., Goldin, K. & Tawfik, D. Intense neutral drifts yield robust and evolvable consensus proteins. J. Mol. Biol. 379, 1029-1044 (2008).
72. Bridgham, J. T., Carroll, S. M. & Thornton, J. W. Evolution of hormone-receptor complexity by molecular exploitation. Science 312, 97-101 (2006).
73. Ortlund, E. A., Bridgham, J. T., Redinbo, M. R. & Thornton, J. W. Crystal structure of an ancient protein: evolution by conformational epistasis. Science 317, 1544-1548 (2007).
74. Dean, A. M. & Thornton, J. W. Mechanistic approaches to the study of evolution: the functional synthesis. Nature Rev. Genet. 8, 675-688 (2007).
75. Bershtein, S., Segal, M., Bekerman, R., Tokuriki, N. & Tawfik, D. S. Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444, 929-932 (2006).
76. Schilling, C. H. & Palsson, B. O. Assessment of the metabolic capabilities of Haemophilus influenzae Rd through a genome-scale pathway analysis. J. Theor. Biol. 203, 249-283 (2000).
77. Forster, J., Famili, I., Fu, P., Palsson, B. & Nielsen, J. Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Res. 13, 244-253 (2003).
78. Edwards, J. S. & Palsson, B. O. Robustness analysis of the Escherichia coli metabolic network. Biotechnol. Prog. 16, 927-939 (2000).
79. Segre, D., Vitkup, D. & Church, G. Analysis of optimality in natural and perturbed metabolic networks. Proc. Natl Acad. Sci. USA 99, 15112-15117 (2002).
80. Motter, A. E., Gulbahce, N., Almaas, E. & Barabasi, A. L. Predicting synthetic rescues in metabolic networks. Mol. Syst. Biol. 4, 168 (2008).
81. Goldman, N. & Yang, Z. H. Codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 11, 725-736 (1994).
82. Yang, Z. H. & Nielsen, R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17, 32-43 (2000).
83. Yang, Z. H. & Nielsen, R. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19, 908-917 (2002).
84. Zhang, J. Z., Nielsen, R. & Yang, Z. H. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22, 2472-2479 (2005).
85. Guindon, S., Rodrigo, A. G., Dyer, K. A. & Huelsenbeck, J. P. Modeling the site-specific variation of selection patterns along lineages. Proc. Natl Acad. Sci. USA 101, 12957-12962 (2004).
86. Shankarappa, R. et al. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73, 10489-10502 (1999).
87. Philippe, H., Casane, D., Gribaldo, S., Lopez, P. & Meunier, J. Heterotachy and functional shift in protein evolution. IUBMB Life 55, 257-265 (2003).
88. Lopez, P., Casane, D. & Philippe, H. Heterotachy, an important process of protein evolution. Mol. Biol. Evol. 19, 1-7 (2002).
89. Thatcher, J. W., Shaw, J. M. & Dickinson, W. J. Marginal fitness contributions of nonessential genes in yeast. Proc. Natl Acad. Sci. USA 95, 253-257 (1998).
90. Carter, A. J. R. & Wagner, G. P. Evolution of functionally conserved enhancers can be accelerated in large populations: a population-genetic model. Proc. Roy. Soc. Lond. B 269, 953-960 (2002).
91. Gavrilets, S. Fitness Landscapes and the Origin of Species (Princeton Univ. Press, Princeton, New Jersey, 2004).
92. Gavrilets, S. Evolution and speciation on holey adaptive landscapes. Trends Ecol. Evol. 12, 307-312 (1997).
93. Gould, S. & Vrba, E. Exaptation - a missing term in the science of form. Paleobiology 8, 4-15 (1982).
94. Provine, W. B. Sewall Wright and Evolutionary Biology (Univ. of Chicago Press, Chicago, Illinois, 1986).
95. Hartl, D. & Clark, A. Principles of Population Genetics (Sinauer Associates Sunderland, Massachusetts, 2007).
96. Charlesworth, B., Morgan, M. T. & Charlesworth, D. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289-1303 (1993).
97. Lynch, M. & Conery, J. The origins of genome complexity. Science 302, 1401-1404 (2003).
98. Schuster, P., Fontana, W., Stadler, P. & Hofacker, I. From sequences to shapes and back - a case-study in RNA secondary structures. Proc. Roy. Soc. Lond. B 255, 279-284 (1994).
99. Maynard Smith, J. Natural selection and the concept of a protein space. Nature 222, 563-564 (1970).
100. Babajide, A., Hofacker, I., Sippl, M. & Stadler, P. Neutral networks in protein space: a computational study based on knowledge-based potentials of mean force. Fold. Des. 2, 261-269 (1997).
101. Li, H., Helling, R., Tang, C. & Wingreen, N. Emergence of preferred structures in a simple model of protein folding. Science 273, 666-669 (1996).
102. Chan, H. & Bornberg-Bauer, E. Perspectives on protein evolution from simple exact models. Appl. Bioinformatics 1, 121-144 (2003).
103. Xia, Y. & Levitt, M. Roles of mutation and recombination in the evolution of protein thermodynamics. Proc. Natl Acad. Sci. USA 99, 10382-10387 (2002).
104. Hofacker, I., Schuster, P. & Stadler, P. Combinatorics of RNA secondary structures. Discrete Appl. Math. 88, 207-237 (1998).
105. Schuster, P. in Evolutionary Dynamics: Exploring the Interplay of Selection, Accident, Neutrality, and Function (eds Crutchfield, J. P. & Schuster, P.) 163-215 (Oxford Univ. Press, New York, 2003).
106. Reidys, C., Stadler, P. & Schuster, P. Generic properties of combinatory maps: neutral networks of RNA secondary structures. Bull. Math. Biol. 59, 339-397 (1997).
107. Eigen, M. & Schuster, P. The Hypercycle: a Principle of Natural Self-Organization (Springer, Berlin, 1979).
108. Pegg, S. C. H. et al. Leveraging enzyme structure-function relationships for functional inference and experimental design: the structure-function linkage database. Biochemistry 45, 2545-2555 (2006).
109. Wagner, A. Robustness and evolvability: a paradox resolved. Proc. Roy. Soc. Lond. B 275, 91-100 (2008).
110. Hofacker, I. et al. Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 125, 167-188 (1994).
111. Kwong, P. D. et al. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659 (1998).