Long-term evolution is surprisingly predictable in lattice proteins

Journal of the Royal Society Interface

Volumn 10, Issue 82, 2013, Pages

  Palmer, Michael E ^a   Moudgil, Arnav ^a   Feldman, Marcus W ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Evolvability; Lineage evolution; Long term evolution; Macroevolution; Protein evolution; Survivability

Indexed keywords

HEALTH; PROTEIN FOLDING; PROTEINS;

EVOLVABILITY; LINEAGE EVOLUTION; LONG-TERM EVOLUTION; MACROEVOLUTION; PROTEIN EVOLUTION; SURVIVABILITY;

BIOLOGY;

LATTICE PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGY; CELL LINEAGE; ENTROPY; MOLECULAR EVOLUTION; NATURAL SELECTION; OUTCOME ASSESSMENT; PREDICTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; BIOLOGICAL MODEL; CHEMISTRY; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; PHYSIOLOGY;

EVOLUTION, MOLECULAR; GENETIC VARIATION; MODELS, GENETIC; PROTEIN FOLDING; PROTEINS; SELECTION, GENETIC;

MLCS; MLOWN;

EID: 84881273268     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2013.0026     Document Type: Article

References (32)

1. Kirschner M, Gerhart J. 1998 Evolvability. Proc. Natl Acad. Sci. USA 95, 8420-8427. (doi:10.1073/pnas.95.15.8420)
2. Houle D. 1992 Comparing evolvability and variability of quantitative traits. Genetics 130, 195-204.
3. Wagner GP, Altenberg L. 1996 Perspective: complex adaptations and the evolution of evolvability. Evolution 50, 967-976. (doi:10.2307/2410639)
4. Jones AG, Arnold SJ, Bürger R. 2007 The mutation matrix and the evolution of evolvability. Evolution 61, 727-745. (doi:10.1111/j.1558-5646.2007. 00071.x)
5. Altenberg L. 1994 The evolution of evolvability in genetic programming. In Advances in genetic programming (ed K Kinnear), pp. 47-74. Cambridge, MA: MIT Press.
6. Draghi J, Wagner GP. 2009 The evolutionary dynamics of evolvability in a gene network model. J. Evol. Biol. 22, 599-611. (doi:10.1111/j.1420-9101.2008. 01663.x)
7. Draghi J, Wagner GP. 2008 Evolution of evolvability in a developmental model. Evolution 62, 301-315. (doi:10.1111/j.1558-5646.2007.00303.x)
8. Griswold CK. 2006 Pleiotropic mutation, modularity and evolvability. Evol. Dev. 8, 81-93. (doi:10.1111/j.1525-142X.2006.05077.x)
9. Palmer ME, Feldman MW. 2011 Spatial environmental variation can select for evolvability. Evolution 65, 2345-2356. (doi:10.1111/j.1558-5646.2011.01283. x)
10. Palmer ME, Feldman MW. 2012 Survivability is more fundamental than evolvability. PLoS ONE 7, e38025. (doi:10.1371/journal.pone.0038025)
11. Woods RJ, Barrick JE, Cooper TF, Shrestha U, Kauth MR, Lenski RE. 2011 Second-order selection for evolvability in a large Escherichia coli population. Science 331, 1433-1436. (doi:10.1126/science.1198914)
12. Lu R, Neff NF, Quake SR, Weissman IL. 2011 Tracking single hematopoietic stem cells in vivo using high-throughput sequencing in conjunction with viral genetic barcoding. Nat. Biotechnol. 29, 928-933. (doi:10.1038/nbt.1977)
13. Lauring AS, Andino R. 2011 Exploring the fitness landscape of an RNA virus by using a universal barcode microarray. J. Virol. 85, 3780-3791. (doi:10.1128/JVI.02217-10)
14. Gerrits A, Dykstra B, Kalmykowa OJ, Klauke K, Verovskaya E, Broekhuis MJC, de Haan G, Bystrykh LV. 2010 Cellular barcoding tool for clonal analysis in the hematopoietic system. Blood 115, 2610-2618. (doi:10.1182/blood-2009-06- 229757)
15. Bloom JD, Wilke CO, Arnold FH, Adami C. 2004 Stability and the evolvability of function in a model protein. Biophys. J. 86, 2758-2764. (doi:10.1016/S0006-3495(04)74329-5)
16. Dill KA, Bromberg S, Yue K, Fiebig KM, Yee DP, Thomas PD. 1995 Principles of protein folding: a perspective from simple exact models. Protein Sci. 4, 561-602. (doi:10.1002/pro.5560040401)
17. Miyazawa S, Jernigan RL. 1985 Estimation of effective interresidue contact energies from protein crystal structures: quasi-chemical approximation. Macromolecules 18, 534-552. (doi:10.1021/ma00145a039)
18. Bloom JD, Silberg JJ, Wilke CO, Drummond DA, Adami C, Arnold FH. 2005 Thermodynamic prediction of protein neutrality. Proc. Natl Acad. Sci. USA 102, 606-611. (doi:10.1073/pnas.0406744102)
19. Thompson SK. 1987 Sample size for estimating multinomial proportions. Am. Stat. 41, 42-46.
20. Desai MM, Fisher DS. 2007 Beneficial mutation selection balance and the effect of linkage on positive selection. Genetics 176, 1759-1798. (doi:10.1534/genetics.106.067678)
21. Clune J, Misevic D, Ofria C, Lenski RE, Elena SF, Sanjuán R. 2008 Natural selection fails to optimize mutation rates for long-term adaptation on rugged fitness landscapes. PLoS Comput. Biol. 4, e1000187. (doi:10.1371/journal. pcbi.1000187)
22. Brillouin L. 1953 The negentropy principle of information. J. Appl. Phys. 24, 1152-1163. (doi:10.1063/1.1721463)
23. Gibbs JW. 1873 A method of geometrical representation of the thermodynamic properties of substances by means of surfaces. Trans. Connecticut Acad. Arts Sci. 2, 382-404.
24. Adami C. 2004 Information theory in molecular biology. Phys. Life Rev. 1, 3-22. (doi:10.1016/j.plrev.2004.01.002)
25. Cover TM, Thomas JA. 2006 Elements of information theory. London, UK: Wiley-Interscience.
26. Slatkin M. 1981 Fixation probabilities and fixation times in a subdivided population. Evolution 35, 477-488. (doi:10.2307/2408196)
27. Bloom JD, Labthavikul ST, Otey CR, Arnold FH. 2006 Protein stability promotes evolvability. Proc. Natl Acad. Sci. USA 103, 5869-5874. (doi:10.1073/pnas.0510098103)
28. Costanzo MS, Brown KM, Hartl DL. 2011 Fitness trade-offs in the evolution of dihydrofolate reductase and drug resistance in Plasmodium falciparum. PLoS ONE 6, e19636. (doi:10.1371/journal.pone.0019636)
29. Lozovsky ER et al. 2009 Stepwise acquisition of pyrimethamine resistance in the malaria parasite. Proc. Natl Acad. Sci. USA 106, 12 025-12 030. (doi:10.1073/pnas.0905922106)
30. Weinreich DM, Delaney NF, DePristo MA, Hartl DL. 2006 Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111-114. (doi:10.1126/science.1123539)
31. Blount ZD, Borland CZ, Lenski RE. 2008 Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl Acad. Sci. USA 105, 7899-7906. (doi:10.1073/pnas.0803151105)
32. Bloom JD, Raval A, Wilke CO. 2006 Thermodynamics of neutral protein evolution. Genetics 175, 255-266. (doi:10.1534/genetics.106.061754)