Neutral networks of genotypes: evolution behind the curtain
DOI:
https://doi.org/10.3989/arbor.2010.746n1253Keywords:
Neutral network, genotype-phenotype map, redundancy, adaptation, fitness landscapeAbstract
Our understanding of the evolutionary process has gone a long way since the publication, 150 years ago, of “On the origin of species” by Charles R. Darwin. The XXth Century witnessed great efforts to embrace replication, mutation, and selection within the framework of a formal theory, able eventually to predict the dynamics and fate of evolving populations. However, a large body of empirical evidence collected over the last decades strongly suggests that some of the assumptions of those classical models necessitate a deep revision. The viability of organisms is not dependent on a unique and optimal genotype. The discovery of huge sets of genotypes (or neutral networks) yielding the same phenotype –in the last term the same organism–, reveals that, most likely, very different functional solutions can be found, accessed and fixed in a population through low-cost exploration of the space of genomes. The “evolution behind the curtain’ may be the answer to some of the current puzzles that evolutionary theory faces, like the fast speciation process that is observed in the fossil record after very long stasis periods.
Downloads
References
Aguirre, J., Buldú, J. M., and Manrubia, S. C. (2009): “Evolutionary dynamics on networks of selectively neutral genotypes: Effects of topology and sequence stability”, Phys. Rev. E, 80:066112. doi:10.1103/PhysRevE.80.066112
Ancel, L. W. and Fontana, W. (2000): “Plasticity, evolvability and modularity in RNA”, J. Exp. Zool. (Mol. Dev. Evol.), 288: 242.
Anderson, P. C. and Mecozzi, S. (2005): “Unusually short RNA sequences: Design of 13-mer. RNA that selectively binds and recognizes theophylline”, J. Am. Chem. Soc., 127: 5290. doi:10.1021/ja0432463 PMid:15826145
Barton, N. H. and Coe, J. B. (2009): “On the application of statistical physics to evolutionary biology”, J. Theor. Biol., 259:317-324. doi:10.1016/j.jtbi.2009.03.019 PMid:19348811
Blythe, R. A. and McKane, A. J. (2007): “Stochastic models of evolution in genetics, ecology and linguistics”, J. Stat. Mech., july: P07018.
Darwin, C. R. (1859): On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, John Murray, London, 1st ed.
Domingo, E., Sabo, D., Taniguchi, T., and Weissmann, C. (1978): “Nucleotidesequence heterogeneity of an RNAphage population”, Cell, 13: 735. doi:10.1016/0092-8674(78)90223-4
Duarte, E. A.; Novella, I. S.; Ledesma, S.; Clarke, D. K.; Moya, A.; Elena, S. F.; Domingo, E. and Holland, J. J. (1994): “Subclonal components of consensus fitness in an RNA virus clone”, J. Virology, 6: 4295.
Eigen, M. (1971): “Selforganization of matter and evolution of biological macromolecules”, Naturwissenschaften, 58: 465. doi:10.1007/BF00623322 PMid:4942363
Eldredge, N. and Gould, S. J. (1972): “Punctuated equilibria: an alternative to phyletic gradualism”, in Schopf, T. J. M., editor, Models in Paleobiology, pages 82-115. Freeman Cooper, San Francisco.
Ewens, W. J. (2004): Mathematical Population Genetic. I. Theoretical introduction, Springer, 2nd edition.
Fontana, W. (2002): “Modelling ’evo-devo’ with RNA”, BioEssays, 24: 1164. doi:10.1002/bies.10190 PMid:12447981
Fontana, W. and Schuster, P. (1998): “Continuity in evolution: On the nature of transitions”, Science, 280: 1451-1455. doi:10.1126/science.280.5368.1451 PMid:9603737
Galton, F. (1886): “Regression towards mediocrity in hereditary stature”, J. Anthrop. Inst., 15: 246-263.
Gould, S. J. (2002): The structure of evolutionary theory, Belknap Press of Harvard University Press.
Gru.ner, W.; Giegerich, R.; Strothmann, D.; Reidys, C.; Weber, J.; Hofacker, I. L.; Stadler, P. F. and Schuster, P. (1996): “Analysis of RNA sequence structure maps by exhaustive enumeration. II. Structures of neutral networks and shape space covering”, Monatshefte Chem., 127: 375-389.
Huxley, J. S. (1942): Evolution: The Modern Synthesis, Allen and Unwin.
Kimura, M. (1968): “Evolutionary rate at the molecular level”, Nature, 217.
Koelle, K.; Cobey, S.; Grenfell, B. and Pascual, M. (2006): “Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans”, Science, 314: 1898-1903. doi:10.1126/science.1132745 PMid:17185596
Mayr, E. (1985): The growth of biological thought, Belknap Press of Harvard University Press.
Mendel, G. (1866): “Versuche über Pflanzen-Hybriden”, Verh. Naturforsh. Ver. Brünn, 4: 3-47.
Muller, H. J. (1932): “Some genetic aspects of sex”, Amer. Nat., 66: 118-138. doi:10.1086/280418
Reidys, C. M. and Stadler, P. F. (2002): “Combinatorial landscapes”, SIAM Rev., 44: 3-54. doi:10.1137/S0036144501395952
Schultes, E. A. and Bartel, D. P. (2000): “One sequence, two ribozymes: Implications for the emergence of new ribozyme folds”, Science, 289: 448-452. doi:10.1126/science.289.5478.448 PMid:10903205
Schuster, P. (2006): “Prediction of RNA secondary structures: from theory to models and real molecules”, Rep. Prog. Phys., 69: 1419. doi:10.1088/0034-4885/69/5/R04
Schuster, P.; Fontana, W.; Stadler, P. F. and Hofacker, I. L. (1994): “From sequences to shapes and back: A case study in RNA secondary structures”, Proc. Roy. Soc. London B, 255: 279. doi:10.1098/rspb.1994.0040 PMid:7517565
Sella, G. and Hirsh, A. E. (2005): “The application of statistical physics to evolutionary biology”, Proc. Nat. Acad. Sci. USA, 102: 9541-9546. doi:10.1073/pnas.0501865102 PMid:15980155 PMCid:1172247
Stich, M., Briones, C., and Manrubia, S. C. (2008): “On the structural repertoire of pools of short, random RNA sequences”, J. Theor. Biol., 252: 750-763. doi:10.1016/j.jtbi.2008.02.018 PMid:18374951
van Nimwegen, E.; Crutchfield, J. P. and Huynen, M. (1999): “Neutral evolution of mutational robustness”, Proc. Natl. Acad. Sci. USA, 96: 9716-9720. doi:10.1073/pnas.96.17.9716
Waterman, M. S. and Smith, T. F. (1978): “RNA secondary structure - Complete mathematical analysis”, Math. Biosci., 42: 257. doi:10.1016/0025-5564(78)90099-8
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2010 Consejo Superior de Investigaciones Científicas (CSIC)

This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.