Properties of selected mutations and genotypic landscapes under Fisher's geometric model

Evolution

Volumn 68, Issue 12, 2014, Pages 3537-3554

  Blanquart, François ^a   Achaz, Guillaume ^b   Bataillon, Thomas ^a   Tenaillon, Olivier ^c  

^a AARHUS UNIVERSITY   (Denmark)

^b CNRS   (France)

^c INSERM   (France)

Author keywords

Adaptation; Epistasis; Experimental evolution; NK model; Rough Mount Fuji; Selection

Indexed keywords

ADAPTATION; BACTERIUM; BIOLOGICAL MODEL; EPISTASIS; GENETIC SELECTION; GENETICS; GENOTYPE; MUTATION; REPRODUCTIVE FITNESS;

ADAPTATION, PHYSIOLOGICAL; BACTERIA; EPISTASIS, GENETIC; GENETIC FITNESS; GENOTYPE; MODELS, GENETIC; MUTATION; SELECTION, GENETIC;

EID: 84914701200     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12545     Document Type: Article

References (66)

1. Achaz, G., A. Rodriguez-Verdugo, B. S. Gaut, and O. Tenaillon . 2014. The reproducibility of adaptation in the light of experimental evolution with whole genome sequencing. Ecol. Genomics 781:211-231.
2. Bataillon, T., and S. F. Bailey . 2014. Effects of new mutations on fitness: insights from models and data. Ann. NY Acad. Sci. 1320:76-92.
3. Carneiro, M., and D. L. Hartl . 2010. Adaptive landscapes and protein evolution. Proc. Natl. Acad. Sci. 107(Suppl. 1):1747-1751.
4. Chevin, L., 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.
5. Chevin, L.-M., G. Decorzent, and T. Lenormand . 2014. Niche dimensionality and the genetics of ecological speciation. Evolution 68:1244-1256.
6. Chou, H.-H., H.-C. Chiu, N. F. Delaney, D. Segrè, and C. J. Marx . 2011. Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332:1190-1192.
7. Chou, H.-H., N. F. Delaney, J. A. Draghi, and C. J. Marx . 2014. Mapping the fitness landscape of gene expression uncovers the cause of antagonism and sign epistasis between adaptive mutations. PLoS Genet. 10: e1004149.
8. Colegrave, N., and A. Buckling . 2005. Microbial experiments on adaptive landscapes. Bioessays 27:1167-1173.
9. Costanzo, M., A. Baryshnikova, J. Bellay, Y. Kim, E. D. Spear, C. S. Sevier, H. Ding, J. L. Koh, K. Toufighi, S. Mostafavi, et al. 2010. The genetic landscape of a cell. Science 327:425-431.
10. da Silva, J., M. Coetzer, R. Nedellec, C. Pastore, and D. E. Mosier . 2010. Fitness epistasis and constraints on adaptation in a human immunodeficiency virus type 1 protein region. Genetics 185:293-303.
11. 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.
12. de Visser, J. A. G., S.-C. Park, and J. Krug . 2009. Exploring the effect of sex on empirical fitness landscapes. Am. Nat. 174:S15-S30.
13. Draghi, J. A., and J. B. Plotkin . 2013. Selection biases the prevalence and type of epistasis along adaptive trajectories. Evolution 67:3120-3131.
14. Firnberg, E., J. W. Labonte, J. J. Gray, and M. Ostermeier. 2014. A comprehensive, high-resolution map of a gene's fitness landscape. Mol. Biol. Evol. 31:1581-1592.
15. Fisher, R. 1930. The genetical theory of natural selection. Oxford Univ. Press, Oxford, U.K.
16. 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. RNA folding and combinatory landscapes. Phys. Rev. E 47:2083-2099.
17. Franke, J., A. Klözer, J. A. G. de Visser, and J. Krug . 2011. Evolutionary accessibility of mutational pathways. PLoS Comput. Biol. 7:e1002134.
18. Gavrilets, S. 2004. Fitness landscapes and the origin of species. Princeton Univ. Press. Princeton, NJ.
19. Gifford, D. R., S. E. Schoustra, and R. Kassen . 2011. The length of adaptive walks is insensitive to starting fitness in Aspergillus nidulans. Evolution 65:3070-3078.
20. Gillespie, J. H. 1991. The causes of molecular evolution. Oxford Univ. Press, Oxford, U.K.
21. Greene, D., and K. Crona . 2014. The changing geometry of a fitness landscape along an adaptive walk. PLoS Comput. Biol. 10:e1003520.
22. Gros, P.-A., and O. Tenaillon . 2009. Selection for chaperone-like mediated genetic robustness at low mutation rate: impact of drift, epistasis and complexity. Genetics 182:555-564.
23. Gros, P.-A., H. Le Nagard, and O. Tenaillon . 2009. The evolution of epistasis and its links with genetic robustness, complexity and drift in a phenotypic model of adaptation. Genetics 182:277-293.
24. Hartl, D. L., and C. H. Taubes . 1996. Compensatory nearly neutral mutations: selection without adaptation. J. Theor. Biol. 182:303-309.
25. Hietpas, R. T., J. D. Jensen, and D. N. Bolon. 2011. Experimental illumination of a fitness landscape. Proc. Natl. Sci. 108:7896-7901.
26. Kauffman, S. A. 1993. The origins of order: self-organization and selection in evolution. Oxford Univ. Press, Oxford, U.K.
27. Kauffman, S., and S. Levin . 1987. Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol. 128:11-45.
28. Khan, A. I., D. M. Dinh, D. Schneider, R. E. Lenski, and T. F. Cooper . 2011. Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332:1193-1196.
29. Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge Univ. Press, Cambridge, U.K.
30. Kingman, J. 1978. A simple model for the balance between selection and mutation. J. Appl. Probab. 15:1-12.
31. Kondrashov, F. A., and A. S. Kondrashov . 2001. Multidimensional epistasis and the disadvantage of sex. Proc. Natl. Acad. Sci. 98:12089-12092.
32. Lee, Y.-H., L. M. DSouza, and G. E. Fox . 1997. Equally parsimonious pathways through an RNA sequence space are not equally likely. J. Mol. Evol. 45:278-284.
33. Lourenço, J., N. Galtier, and S. Glémin . 2011. Complexity, pleiotropy, and the fitness effect of mutations. Evolution 65:1559-1571.
34. Lozovsky, 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., S. P. Miller, R. Felsheim, and A. M. Dean . 2005. The biochemical architecture of an ancient adaptive landscape. Science 310:499-501.
36. MacLean, R., 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.
37. Manna, F., G. Martin, and T. Lenormand . 2011. Fitness landscapes: an alternative theory for the dominance of mutation. Genetics 189:923-937.
38. Martin, G. 2014. Fisher's geometrical model emerges as a property of complex integrated phenotypic networks. Genetics 197:237-255.
39. 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.
40. Martin, G., and T. Lenormand . 2008. The distribution of beneficial and fixed mutation fitness effects close to an optimum. Genetics 179:907-916.
41. 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.
42. O'Maille, P. E., A. Malone, N. Dellas, B. A. Hess, L. Smentek, I. Sheehan, B. T. Greenhagen, J. Chappell, G. Manning, and J. P. Noel . 2008. Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nat. Chem. Biol. 4:617-623.
43. Orr, H. A. 2005. The genetic theory of adaptation: a brief history. Nat. Rev. Genet. 6:119-127.
44. Otto, S. P. 2009. The evolutionary enigma of sex. Am. Nat. 174:S1-S14.
45. Patwa, Z., and L. Wahl . 2008. The fixation probability of beneficial mutations. J. R. Soc. Interface 5:1279-1289.
46. Perfeito, L., A. Sousa, T. Bataillon, and I. Gordo . 2014. Rates of fitness decline and rebound suggest pervasive epistasis. Evolution 68:50-162.
47. Poelwijk, F. J., S. Tănase-Nicola, D. J. Kiviet, and S. J. Tans . 2011. Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J. Theor. Biol. 272:141-144.
48. Poon, A., and S. P. Otto . 2000. Compensating for our load of mutations: freezing the meltdown of small populations. Evolution 54:1467-1479.
49. 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.
50. Rowe, W., M. Platt, D. C. Wedge, P. J. Day, D. B. Kell, and J. Knowles . 2009. Analysis of a complete DNA-protein affinity landscape. J. R. Soc. Interface 7:397-408.
51. Rozen, D. E., J. De Visser, and P. J. Gerrish . 2002. Fitness effects of fixed beneficial mutations in microbial populations. Curr. Biol. 12:1040-1045.
52. Salverda, M. L., E. Dellus, F. A. Gorter, A. J. Debets, J. van der Oost, R. F. Hoekstra, D. S. Tawfik, and J. A. G. de Visser . 2011. Initial mutations direct alternative pathways of protein evolution. PLoS Genet. 7:e1001321.
53. 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. USA 101:15376-15379.
54. Schenk, M. F., I. G. Szendro, M. L. Salverda, J. Krug, and J. A. G. de Visser . 2013. Patterns of epistasis between beneficial mutations in an antibiotic resistance gene. Mol. Biol. Evol. 30:1779-1787.
55. Szendro, I. G., M. F. Schenk, J. Franke, J. Krug, and J. A. G. de Visser . 2013. Quantitative analyses of empirical fitness landscapes. J. Stat. Mech. Theory Exp. 2013:P01005.
56. Tenaillon, O., O. K. Silander, J.-P. Uzan, and L. Chao . 2007. Quantifying organismal complexity using a population genetic approach. PLoS One 2:e217.
57. Tenaillon, O., A. Rodrguez-Verdugo, R. L. Gaut, P. McDonald, A. F. Bennett, A. D. Long, and B. S. Gaut . 2012. The molecular diversity of adaptive convergence. Science 335:457-461.
58. Velenich, A., and J. Gore . 2013. The strength of genetic interactions scales weakly with mutational effects. Genome Biol. 14:R76.
59. Watson, R. A., D. M. Weinreich, and J. Wakeley . 2011. Genome structure and the benefit of sex. Evolution 65:523-536.
60. Waxman, D., and Peck, J. R. 1998. Pleiotropy and the preservation of perfection. Science 279:1210-1213.
61. Waxman, D., and J. Welch . 2005. Fisher's microscope and Haldane's ellipse. Am. Nat. 166:447-457.
62. Weinreich, D. M., R. A. Watson, and L. Chao . 2005. Perspective: sign epistasis and genetic costraint on evolutionary trajectories. Evolution 59:1165-1174.
63. 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.
64. Weinreich, D. M., Y. Lan, C. S. Wylie, and R. B. Heckendorn . 2013. Should evolutionary geneticists worry about higher-order epistasis?. Curr. Opin. Genet. Dev. 23:700-707.
65. 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.
66. Wright, S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc. Sixth Int. Congr. Genetics 1:356-366.