Empirical fitness landscapes and the predictability of evolution (original) (raw)

• Lehner, B. Genotype to phenotype: lessons from model organisms for human genetics. Nature Rev. Genet. 14, 168–178 (2013).
  Article CAS PubMed Google Scholar
• Wagner, G. P. & Zhang, J. The pleiotropic structure of the genotype–phenotype map: the evolvability of complex organisms. Nature Rev. Genet. 12, 204–213 (2011).
  Article CAS PubMed Google Scholar
• Phillips, P. C. Epistasis — the essential role of gene interactions in the structure and evolution of genetic systems. Nature Rev. Genet. 9, 855–867 (2008).
  Article CAS PubMed Google Scholar
• de Visser, J. A. G. M., Cooper, T. F. & Elena, S. F. The causes of epistasis. Proc. R. Soc. B 278, 3617–3624 (2011).
  Article PubMed PubMed Central Google Scholar
• Gavrilets, S. Fitness Landscapes and the Origin of Species (Princeton Univ. Press, 2004).
  Google Scholar
• Achaz, G., Rodriguez-Verdugo, A., Gaut, B. S. & Tenaillon, O. The reproducibility of adaptation in the light of experimental evolution with whole genome sequencing. Adv. Exp. Med. Biol. 781, 211–231 (2014).
  Article PubMed Google Scholar
• Lobkovsky, A. E. & Koonin, E. V. Replaying the tape of life: quantification of the predictability of evolution. Frontiers Genet. 3, 246 (2012).
  Article Google Scholar
• Wright, S. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc. 6th Int. Congress Genet. 1, 356–366 (1932). This paper introduces the concept of the fitness landscape as a key component of Wright's shifting balance theory.
  Google Scholar
• Colegrave, N. & Buckling, A. Microbial experiments on adaptive landscapes. BioEssays 27, 1167–1173 (2005).
  Article PubMed Google Scholar
• Szendro, I. G., Schenk, M. F., Franke, J., Krug, J. & de Visser, J. A. G. M. Quantitative analyses of empirical fitness landscapes. J. Stat. Mech. P01005 (2013).
• Wright, S. Evolution in Mendelian populations. Genetics 16, 97–159 (1931).
  CAS PubMed PubMed Central Google Scholar
• Haldane, J. B. S. A mathematical theory of natural selection. Part VIII. Metastable populations. Proc. Cambridge Philos. Soc. 27, 137–142 (1931).
  Article Google Scholar
• Maynard Smith, J. Natural selection and the concept of a protein space. Nature 225, 563–564 (1970). This study presents the realization that genotypic space is discrete and that mutational pathways are only accessible when they pass through functional genotypes.
  Article Google Scholar
• Kauffman, S. A. & Levin, S. Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol. 128, 11–45 (1987). This is the first mathematical exploration of random fitness landscapes and their consequences for adaptation.
  Article CAS PubMed Google Scholar
• Kauffman, S. A. & Weinberger, E. D. The NK model of rugged fitness landscapes and its application to the maturation of the immune response. J. Theor. Biol. 141, 211–245 (1989).
  Article CAS PubMed Google Scholar
• Harms, M. J. & Thornton, J. W. Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nature Rev. Genet. 14, 559–571 (2013).
  Article CAS PubMed Google Scholar
• Malcolm, B. A., Wilson, K. P., Matthews, B. W., Kirsch, J. F. & Wilson, A. C. Ancestral lysozymes reconstructed, neutrality tested, and thermostability linked to hydrocarbon packing. Nature 345, 86–89 (1990). This is the first empirical analysis of a three-locus fitness landscape of lysozymes in game birds.
  Article CAS PubMed Google Scholar
• Barrick, J. E. & Lenski, R. E. Genome dynamics during experimental evolution. Nature Rev. Genet. 14, 827–839 (2013).
  Article CAS PubMed Google Scholar
• Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988).
  Article CAS PubMed Google Scholar
• Kouyos, R. D., Silander, O. K. & Bonhoeffer, S. Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol. Evol. 22, 308–315 (2007).
  Article PubMed Google Scholar
• de Visser, J. A. G. M., Hoekstra, R. F. & van den Ende, H. Test of interaction between genetic markers that affect fitness in Aspergillus niger. Evolution 51, 1499–1505 (1997).
  Article CAS PubMed Google Scholar
• Hall, D. W., Agan, M. & Pope, S. C. Fitness epistasis among 6 biosynthetic loci in the budding yeast Saccharomyces cerevisiae. J. Hered. 101, S75–S84 (2010).
  Article PubMed Google Scholar
• Kondrashov, F. A. & Kondrashov, A. S. Multidimensional epistasis and the disadvantage of sex. Proc. Natl Acad. Sci. USA 98, 12089–12092 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Weinreich, D. M., Watson, R. A. & Chao, L. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59, 1165–1174 (2005). This paper formally introduces the concept of sign epistasis and proves its equivalence with limited pathway accessibility.
  CAS PubMed Google Scholar
• Poelwijk, F. J., Tanase-Nicola, S., Kiviet, D. J. & Tans, S. J. Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J. Theor. Biol. 272, 141–144 (2011).
  Article PubMed Google Scholar
• 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). This seminal study shows how sign epistasis limits the number of accessible trajectories on a five-locus fitness landscape of β-lactamase.
  Article CAS PubMed Google Scholar
• Weinreich, D. M., Lan, Y., Wylie, S. C. & Heckendorn, R. B. Should evolutionary geneticists worry about higher-order epistasis? Curr. Opin. Genet. Dev. 23, 700–707 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• O'Maille, P. E. et al. Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nature Chem. Biol. 4, 617–623 (2008).
  Article CAS Google Scholar
• Lee, Y.-H., Dsouza, L. M. & Fox, G. E. Equally parsimonious pathways through an RNA sequence space are not equally likely. J. Mol. Evol. 45, 278–284 (1997).
  Article CAS PubMed Google Scholar
• Aita, T., Iwakura, M. & Husimi, Y. A cross-section of the fitness landscape of dihydrofolate reductase. Protein Engineer. 14, 633–638 (2001).
  Article CAS Google Scholar
• Bridgham, J. T., Carroll, S. M. & Thornton, J. W. Evolution of hormone-receptor complexity by molecular exploitation. Science 312, 97–101 (2006).
  Article CAS PubMed Google Scholar
• Brown, K. M. et al. Compensatory mutations restore fitness during the evolution of dihydrofolate reductase. Mol. Biol. Evol. 27, 2682–2690 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• da Silva, J., Coetzer, M., Nedellec, R., Pastore, C. & Mosier, D. E. Fitness epistasis and constraints on adaptation in a human immunodeficiency virus type 1 protein region. Genetics 185, 293–303 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Goulart, C. P. et al. Designing antibiotic cycling strategies by determining and understanding local adaptive landscapes. PLoS ONE 8, e56040 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Lozovsky, E. R. et al. Stepwise acquisition of pyrimethamine resistance in the malaria parasite. Proc. Natl Acad. Sci. USA 106, 12015–12030 (2009).
  Article Google Scholar
• Lunzer, M., Miller, S. P., Felsheim, R. & Dean, A. M. The biochemical architecture of an ancient adaptive landscape. Science 310, 499–501 (2005). This study reconstructs a fitness landscape by analysing enzyme function as a phenotype that links genotype and fitness.
  Article CAS PubMed Google Scholar
• Novais, A. et al. Evolutionary trajectories of β-lactamase CTX-M-1 cluster enzymes: predicting antibiotic resistance. PLoS Pathog. 6, e1000735 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Tan, L., Serene, S., Chao, H. X. & Gore, J. Hidden randomness between fitness landscapes limits reverse evolution. Phys. Rev. Lett. 106, 198102 (2011).
  Article PubMed CAS Google Scholar
• de Vos, M. G. J., Poelwijk, F. J., Battich, N., Ndika, J. D. T. & Tans, S. J. Environmental dependence of genetic constraint. PLoS Genet. 9, e1003580 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Chou, H.-H., Chiu, H.-C., Delaney, N. F., Segrè, D. & Marx, C. J. Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332, 1190–1192 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Khan, A. I., Dinh, D. M., Schneider, D., Lenski, R. E. & Cooper, T. F. Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332, 1193–1196 (2011).
  Article CAS PubMed Google Scholar
• Franke, J., Klözer, A., de Visser, J. A. G. M. & Krug, J. Evolutionary accessibility of mutational pathways. PLoS Computat. Biol. 7, e1002134 (2011).
  Article CAS Google Scholar
• Whitlock, M. C. & Bourguet, D. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54, 1654–1660 (2000).
  Article CAS PubMed Google Scholar
• Schenk, M. F., Szendro, I. G., Salverda, M. L. M., Krug, J. & de Visser, J. A. G. M. Patterns of epistasis between beneficial mutations in an antibiotic resistance gene. Mol. Biol. Evol. 30, 1779–1787 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Draghi, J. A. & Plotkin, J. B. Selection biases the prevalence and type of epistasis along adaptive trajectories. Evolution 67, 3120–3131 (2013).
  Article PubMed Google Scholar
• Pumir, A. & Shraiman, B. Epistasis in a model of molecular signal transduction. PLoS Comput. Biol. 7, e1001134 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Wilke, C. O. & Adami, C. Interaction between directional epistasis and average mutational effects. Proc. R. Soc. B 268, 1469–1474 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• You, L. & Yin, J. Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics 160, 1273–1281 (2002).
  PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Watson, R. A., Weinreich, D. M. & Wakeley, J. Genome structure and the benefits of sex. Evolution 65, 523–536 (2010).
  Article PubMed Google Scholar
• Conway Morris, S. Life's Solution: Inevitable Humans in a Lonely Universe (Cambridge Univ. Press, 2003).
  Book Google Scholar
• Gould, S. J. Wonderful Life: The Burgess Shale and the Nature of History (W. W. Norton & Company, 1989).
  Google Scholar
• Lang, G. I. et al. Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500, 571–574 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 335, 457–461 (2012).
  Article CAS PubMed Google Scholar
• Woods, R., Schneider, D., Winkworth, C. L., Riley, M. A. & Lenski, R. E. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc. Natl Acad. Sci. USA 103, 9107–9112 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Blount, Z. D., Barrick, J. E., Davidson, C. J. & Lenski, R. E. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489, 513–518 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Salverda, M. L. M. et al. Initial mutations direct alternative pathways of protein evolution. PLoS Genet. 7, e1001321 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Papp, B., Notebaart, R. A. & Pál, C. Systems-biology approaches for predicting genomic evolution. Nature Rev. Genet. 12, 591–602 (2011).
  Article CAS PubMed Google Scholar
• Gerrish, P. J. & Sniegowski, P. D. Real time forecasting of near-future evolution. J. R. Soc. Interface 9, 2268–2278 (2012).
  Article PubMed PubMed Central Google Scholar
• Gillespie, J. H. Some properties of finite populations experiencing strong selection and weak mutation. Am. Naturalist 121, 691–708 (1983).
  Article Google Scholar
• Orr, H. A. The genetic theory of adaptation: a brief history. Nature Rev. Genet. 6, 119–127 (2005).
  Article CAS PubMed Google Scholar
• Crona, K., Greene, D. & Barlow, M. The peaks and geometry of fitness landscapes. J. Theor. Biol. 317, 1–10 (2013).
  Article PubMed Google Scholar
• Whitlock, M. C., Phillips, P. C., Moore, F. B.-G. & Tonsor, S. J. Multiple fitness peaks and epistasis. Annu. Rev. Ecol. Systemat. 26, 601–629 (1995).
  Article Google Scholar
• Hegarty, P. & Martinsson, A. On the existence of accessible paths in various models of fitness landscapes. Ann. Appl. Prob. (in the press).
• Schmiegelt, B. & Krug, J. Evolutionary accessibility of modular fitness landscapes. J. Statist. Phys. 154, 334–355 (2014).
  Article Google Scholar
• Roy, S. W. Probing evolutionary repeatability: neutral and double changes and the predictability of evolutionary adaptation. PLoS ONE 4, e4500 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Gerrish, P. J. & Lenski, R. E. The fate of competing beneficial mutations in an asexual population. Genetica 102–103, 127–144 (1998).
• Jain, K., Krug, J. & Park, S.-C. Evolutionary advantage of small populations on complex fitness landscapes. Evolution 65, 1945–1955 (2011).
  Article PubMed Google Scholar
• Rozen, D. E., Habets, M. G. J. L., Handel, A. & de Visser, J. A. G. M. Heterogeneous adaptive trajectories of small populations on complex fitness landscapes. PLoS ONE 3, e1715 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Weissman, D. B., Desai, M. M., Fisher, D. S. & Feldman, M. W. The rate at which asexual populations cross fitness valleys. Theor. Popul. Biol. 75, 286–300 (2009).
  Article PubMed PubMed Central Google Scholar
• Isawa, Y., Michor, F. & Nowak, M. A. Stochastic tunnels in evolutionary dynamics. Genetics 166, 1571–1579 (2004).
  Article Google Scholar
• Woods, R. J. et al. Second-order selection for evolvability in a large Escherichia coli population. Science 331, 1433–1436 (2011). This study experimentally shows the combined influence of epistasis and population dynamics on the outcome of evolution.
  Article CAS PubMed PubMed Central Google Scholar
• Szendro, I. G., Franke, J., de Visser, J. A. G. M. & Krug, J. Predictability of evolution depends non-monotonically on population size. Proc. Natl Acad. Sci. USA 110, 571–576 (2013).
  Article CAS PubMed Google Scholar
• Rowe, W. et al. Analysis of a complete DNA–protein affinity landscape. J. R. Soc. Interface 7, 397–408 (2010).
  Article CAS PubMed Google Scholar
• Pitt, J. N. & Ferré-D'Amaré, A. R. Rapid construction of empirical RNA fitness landscapes. Science 330, 376–379 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Jiménez, J. I., Xulvi-Brunet, R., Campbell, G. W., Turk-MacLeod, R. & Chen, I. A. Comprehensive experimental fitness landscape and evolutionary network for small RNA. Proc. Natl Acad. Sci. 110, 14984–14989 (2013). This is an empirical analysis of the largest fitness landscape so far and involves >10 14 RNA molecules.
  Article PubMed PubMed Central Google Scholar
• Hinkley, T. et al. A systems analysis of mutational effects in HIV-1 protease and reverse transcriptase. Nature Genet. 43, 487–490 (2011). This paper presents an early empirical fitness landscape of large dimensions for HIV-1 with fitness predictions for the many missing genotypes.
  Article CAS PubMed Google Scholar
• Kouyos, R. D. et al. Exploring the complexity of the HIV-1 fitness landscape. PLoS Genet. 8, e1002551 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Otwinowski, J. & Nemenman, I. Genotype to phenotype mapping and the fitness landscape of the E. coli lac promoter. PLoS ONE 8, e61570 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Kinney, J. B., Murugan, A., Callan, C. G. & Cox, E. C. Using deep sequencing to characterize the biophysical mechanism of a transcriptional regulatory sequence. Proc. Natl Acad. Sci. 107, 9158–9163 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Provine, W. B. Sewall Wright and Evolutionary Biology (Chicago Univ. Press, 1986).
  Google Scholar
• de Visser, J. A. G. M., Park, S.-C. & Krug, J. Exploring the effect of sex on empirical fitness landscapes. Am. Naturalist 174, S15–S30 (2009).
  Article Google Scholar
• Wagner, A. Neutralism and selectionism: a network-based reconciliation. Nature Rev. Genet. 9, 965–974 (2008).
  Article CAS PubMed Google Scholar
• Hietpas, R. T., Jensen, J. D. & Bolona, D. N. Experimental illumination of a fitness landscape. Proc. Natl Acad. Sci. USA 108, 7896–7901 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Heckmann, D. et al. Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape. Cell 153, 1579–1588 (2013).
  Article CAS PubMed Google Scholar
• Perfeito, L., Ghozzi, S., Berg, J., Schnetz, K. & Lässig, M. Nonlinear fitness landscape of a molecular pathway. PLoS Genet. 7, e1002160 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Chan, H. S. & Bornberg-Bauer, E. Perspectives on protein evolution from simple exact models. Appl. Bioinformat. 1, 121–144 (2002).
  CAS Google Scholar
• Schuster, P. Prediction of RNA secondary structures: from theory to models and real molecules. Rep. Progress Phys. 69, 1419–1477 (2006).
  Article CAS Google Scholar
• Mustonen, V., Kinney, J., Callan, C. G. & Lässig, M. Energy-dependent fitness: a quantitative model for the evolution of yeast transcription factor binding sites. Proc. Natl Acad. Sci. 105, 12376–12381 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Heo, M., Kang, L. & Shakhnovich, E. I. Emergence of species in evolutionary “simulated annealing”. Proc. Natl Acad. Sci. USA 106, 1869–1874 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Wylie, S. C. & Shakhnovich, E. I. A biophysical protein folding model accounts for most mutational fitness effects in viruses. Proc. Natl Acad. Sci. USA 108, 9916–9921 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Russell, C. A. et al. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336, 1541–1547 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Gong, L. I., Suchard, M. A. & Bloom, J. D. Stability-mediated epistasis constrains the evolution of an influenza protein. eLife 2, e00631 (2013).
  Article PubMed PubMed Central Google Scholar
• Hall, B. G. Predicting evolution by in vitro evolution requires determining evolutionary pathways. Antimicrob. Agents Chemother. 46, 3035–3038 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Palmer, A. C. & Kishony, R. Understanding, predicting and manipulating the genotypic evolution of antibiotic resistance. Nature Rev. Genet. 14, 243–248 (2013).
  Article CAS PubMed Google Scholar
• Ferguson, Andrew, L. et al. Translating HIV sequences into quantitative fitness landscapes predicts viral vulnerabilities for rational immunogen design. Immunity 38, 606–617 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Hansen, T. F. & Wagner, G. P. Modeling genetic architecture: a multilinear theory of gene interaction. Theor. Popul. Biol. 59, 61–86 (2001).
  Article CAS PubMed Google Scholar
• Neher, R. A. & Shraiman, B. I. Statistical genetics and evolution of quantitative traits. Rev. Modern Phys. 83, 1283–1300 (2011).
  Article Google Scholar
• Stadler, P. F. & Happel, R. Random field models of fitness landscapes. J. Math. Biol. 38, 435–478 (1999).
  Article Google Scholar
• Neidhart, J., Szendro, I. G. & Krug, J. Exact results for amplitude spectra of fitness landscapes. J. Theor. Biol. 332, 218–227 (2013).
  Article PubMed Google Scholar
• Kingman, J. F. C. A simple model for the balance between selection and mutation. J. Appl. Probabil. 15, 1–12 (1978).
  Article Google Scholar
• Lobkovsky, A. E., Wolf, Y. I. & Koonin, E. V. Predictability of evolutionary trajectories in fitness landscapes. PLoS Comput. Biol. 7, e1002302 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Palmer, M. E., Moudgil, A. & Feldman, M. W. Long-term evolution is surprisingly predictable in lattice proteins. J. R. Soc. Interface 10, 20130026 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Ferrada, E. & Wagner, A. A comparison of genotype-phenotype maps for RNA and proteins. Biophys. J. 102, 1916–1925 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Martin, G., Elena, S. F. & Lenormand, T. Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nature Genet. 33, 555–560 (2007).
  Article CAS Google Scholar
• Rokyta, D. R. et al. Epistasis between beneficial mutations and the phenotype-to-fitness map for a ssDNA virus. PLoS Genet. 7, e1002075 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Pearson, V. M., Miller, C. R. & Rokyta, D. R. The consistency of beneficial fitness effects of mutations across diverse genetic backgrounds. PLoS ONE 7, e43864 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Chou, H.-H., Delaney, N. F., Draghi, J. A. & Marx, C. J. Mapping the fitness landscape of gene expression uncovers the cause of antagonism and sign epistasis between adaptive mutations. PLoS Genet. 10, e1004149 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Orr, H. A. The probability of parallel evolution. Evolution 59, 216–220 (2005).
  Article CAS PubMed Google Scholar