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The Role of Randomness in Darwinian Evolution

Published online by Cambridge University Press:  01 January 2022

Andreas Wagner
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Abstract

Historically, one of the most controversial aspects of Darwinian evolution has been the prominent role that randomness and random change play in it. Most biologists agree that mutations in DNA have random effects on fitness. However, fitness is a highly simplified scalar representation of an enormously complex phenotype. Challenges to Darwinian thinking have focused on such complex phenotypes. Whether mutations affect such complex phenotypes randomly is ill understood. Here I discuss three very different classes of well-studied molecular phenotypes in which mutations cause nonrandom changes, based on our current knowledge. What is more, this nonrandomness facilitates evolutionary adaptation. Thus, living beings may translate DNA change into nonrandom phenotypic change that facilitates Darwinian evolution.

Type
Research Article
Information
Philosophy of Science , Volume 79 , Issue 1 , January 2012 , pp. 95 - 119
Copyright
Copyright © The Philosophy of Science Association

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Footnotes

‡

I acknowledge support through Swiss National Science Foundation grants 315200-116814, 315200-119697, and 315230-129708, as well as through the YeastX project of SystemsX.ch.

References

Beatty, J. 1984. “Chance and Natural Selection.” Philosophy of Science 51:183–211.CrossRefGoogle Scholar
Bharathan, G., Goliber, T. E., Moore, C., Kessler, S., Pham, T., and Sinha, N. R.. 2002. “Homologies in Leaf Form Inferred from Knoxi Gene Expression during Development.” Science 296:1858–60.CrossRefGoogle ScholarPubMed
Bollobas, B., Kohayakawa, Y., and Luczak, T.. 1992. “The Evolution of Random Subgraphs of the Cube.” Random Structures and Algorithms 3:55–90.CrossRefGoogle Scholar
Brakefield, P. M. 2006. “Evo-Devo and Constraints on Selection.” Trends in Ecology and Evolution 21:362–68.CrossRefGoogle ScholarPubMed
Cairns, J., Overbaugh, J., and Miller, S.. 1988. “The Origin of Mutants.” Nature 335:142–45.CrossRefGoogle ScholarPubMed
Carroll, S. B., Grenier, J. K., and Weatherbee, S. D.. 2001. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. Malden, MA: Blackwell.Google Scholar
Causier, B., Castillo, R., Zhou, J. L., Ingram, R., Xue, Y. B., Schwarz-Sommer, Z., and Davies, B.. 2005. “Evolution in Action: Following Function in Duplicated Floral Homeotic Genes.” Current Biology 15:1508–12.CrossRefGoogle ScholarPubMed
Chaitin, G. J. 1975. “Randomness and Mathematical Proof.” Scientific American 5:47–52.CrossRefGoogle Scholar
Chaitin, G. J.. 2001. Exploring Randomness. London: Springer.CrossRefGoogle Scholar
Chen, L. B., DeVries, A. L., and Cheng, C. H. C.. 1997. “Convergent Evolution of Antifreeze Glycoproteins in Antarctic Notothenioid Fish and Arctic Cod.” Proceedings of the National Academy of Sciences of the United States of America 94:3817–22.Google ScholarPubMed
Cheng, C. C.-H. 1998. “Evolution of the Diverse Antifreeze Proteins.” Current Opinion in Genetics and Development 8:715–20.CrossRefGoogle ScholarPubMed
Cheverud, J. M. 1984. “Quantitative Genetics and Developmental Constraints on Evolution by Selection.” Journal of Theoretical Biology 110:155–71.CrossRefGoogle ScholarPubMed
Ciliberti, S., Martin, O. C., and Wagner, A.. 2007a. “Circuit Topology and the Evolution of Robustness in Complex Regulatory Gene Networks.” PLoS Computational Biology 3 (2): e15.CrossRefGoogle Scholar
Ciliberti, S., Martin, O. C., and Wagner, A.. 2007b. “Innovation and Robustness in Complex Regulatory Gene Networks.” Proceedings of the National Academy of Sciences of the United States of America 104:13591–96.Google Scholar
Cline, R. E., Hill, R. H., Phillips, D. L., and Needham, L. L.. 1989. “Pentachlorophenol Measurements in Body-Fluids of People in Log Homes and Workplaces.” Archives of Environmental Contamination and Toxicology 18:475–81.CrossRefGoogle ScholarPubMed
Copley, S. D. 2000. “Evolution of a Metabolic Pathway for Degradation of a Toxic Xenobiotic: The Patchwork Approach.” Trends in Biochemical Sciences 25:261–65.CrossRefGoogle ScholarPubMed
Dawkins, R. 1996. Climbing Mount Improbable. New York: Norton.Google Scholar
Denver, D. R., et al. 2009. “A Genome-Wide View of Caenorhabditis Elegans Base-Substitution Mutation Processes.” Proceedings of the National Academy of Sciences of the United States of America 106:16310–14.Google ScholarPubMed
Drake, J. W., Charlesworth, B., Charlesworth, D., and Crow, J. F.. 1998. “Rates of Spontaneous Mutation.” Genetics 148:1667–86.CrossRefGoogle ScholarPubMed
Earman, J. 1986. A Primer on Determinism. Dordrecht: Reidel.CrossRefGoogle Scholar
Eble, G. J. 1999. “On the Dual Nature of Chance in Evolutionary Biology and Paleobiology.” Paleobiology 25:75–87.Google Scholar
Elbert, T., Ray, W. J., Kowalik, Z. J., Skinner, J. E., Graf, K. E., and Birbaumer, N.. 1994. “Chaos and Physiology—Deterministic Chaos in Excitable Cell Assemblies.” Physiological Reviews 74:1–47.CrossRefGoogle ScholarPubMed
Erdös, P., and Renyi, A.. 1960. “On the Evolution of Random Graphs.” Evolution 5:17–61.Google Scholar
Feller, W. 1968. An Introduction to Probability Theory and Its Applications. New York: Wiley.Google Scholar
Ferrada, E., and Wagner, A.. 2008. “Protein Robustness Promotes Evolutionary Innovations on Large Evolutionary Time Scales.” Proceedings of the Royal Society of London B 275:1595–1602.Google Scholar
Ferrada, E., and Wagner, A.. 2010. “Evolutionary Innovation and the Organization of Protein Functions in Sequence Space.” PLoS ONE 5 (11): e14172.CrossRefGoogle Scholar
Fontana, W., and Schuster, P.. 1998. “Continuity in Evolution: On the Nature of Transitions.” Science 280:1451–55.CrossRefGoogle ScholarPubMed
Futuyma, D. J. 1998. Evolutionary Biology. 3rd ed. Sunderland, MA: Sinauer.Google Scholar
Gavrilets, S. 1997. “Evolution and Speciation on Holey Adaptive Landscapes.” Trends in Ecology and Evolution 12:307–12.CrossRefGoogle ScholarPubMed
Gilbert, S. F. 1997. Developmental Biology. 5th ed. Sunderland, MA: Sinauer.Google Scholar
Glass, L. 2001. “Synchronization and Rhythmic Processes in Physiology.” Nature 410:277–84.CrossRefGoogle ScholarPubMed
Golding, G. B., and Dean, A. M.. 1998. “The Structural Basis of Molecular Adaptation.” Molecular Biology and Evolution 15:355–69.CrossRefGoogle ScholarPubMed
Gould, S. J. 1991. “The Disparity of the Burgess Shale Arthropod Fauna and the Limits of Cladistic-Analysis—Why We Must Strive to Quantify Morphospace.” Paleobiology 17:411–23.CrossRefGoogle Scholar
Gould, S. J.. 1993. Eight Little Piggies: Reflections in Natural History. New York: Norton.Google Scholar
Griffiths, P. E., and Neumann-Held, E. M.. 1999. “The Many Faces of the Gene.” BioScience 49:656–62.CrossRefGoogle Scholar
Griffiths, P. E., and Stotz, K.. 2007. “Gene.” In Cambridge Companion to the Philosophy of Biology, ed. Hull, D. and Ruse, M., 85–102. New York: Cambridge University Press.CrossRefGoogle Scholar
Gruner, 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.” Pt. 2, “Structures of Neutral Networks and Shape Space Covering.” Monatshefte fur Chemie 127:375–89.Google Scholar
Hartl, D. L., and Clark, A. G.. 2007. Principles of Population Genetics. 4th ed. Sunderland, MA: Sinauer.Google Scholar
Hastings, A., Hom, C. L., Ellner, S., Turchin, P., and Godfray, H. C. J.. 1993. “Chaos in Ecology—Is Mother Nature a Strange Attractor?” Annual Review of Ecology and Systematics 24:1–33.CrossRefGoogle Scholar
Hendrickson, H., Slechta, E. S., Bergthorsson, U., Andersson, D. I., and Roth, J. R.. 2002. “Amplification-Mutagenesis: Evidence That ‘Directed’ Adaptive Mutation and General Hypermutability Result from Growth with a Selected Gene Amplification.” Proceedings of the National Academy of Sciences of the United States of America 99:2164–69.Google ScholarPubMed
Hodin, J. 2000. “Plasticity and Constraints in Development and Evolution.” Paper presented at the Modularity of Animal Form Workshop, Friday Harbor, WA.3.0.CO;2-7>CrossRefGoogle Scholar
Hueber, S. D., and Lohmann, I.. 2008. “Shaping Segments: Hox Gene Function in the Genomic Age.” Bioessays 30:965–79.CrossRefGoogle ScholarPubMed
Hughes, C. L., and Kaufman, T. C.. 2002. “Hox Genes and the Evolution of the Arthropod Body Plan.” Evolution and Development 4:459–99.CrossRefGoogle ScholarPubMed
Hull, D. L. 1972. “Reduction in Genetics—Biology or Philosophy.” Philosophy of Science 39:491–99.CrossRefGoogle Scholar
Hull, D. L.. 1979. “Reduction in Genetics.” Philosophy of Science 46:316–20.CrossRefGoogle Scholar
Irish, V. F. 2003. “The Evolution of Floral Homeotic Gene Function.” Bioessays 25:637–46.CrossRefGoogle ScholarPubMed
Jia, W. L., and Higgs, P. G.. 2008. “Codon Usage in Mitochondrial Genomes: Distinguishing Context-Dependent Mutation from Translational Selection.” Molecular Biology and Evolution 25:339–51.CrossRefGoogle ScholarPubMed
Jörg, T., Martin, O. C., and Wagner, A.. 2008. “Neutral Network Sizes of Biological RNA Molecules Can Be Computed and Are Not Atypically Small.” BMC Bioinformatics 9:464.CrossRefGoogle Scholar
Karlin, S., and Brendel, V.. 1993. “Patchiness and Correlations in DNA Sequences.” Science 259:677–80.CrossRefGoogle ScholarPubMed
Karlin, S., and Cardon, L. R.. 1994. “Computational DNA Sequence Analysis.” Annual Review of Microbiology 48:619–54.CrossRefGoogle ScholarPubMed
Laubichler, M. D., Muller, G. B., Fontana, W., and Wagner, G. P.. 2005. “Sacrificing Dialogue for Politics.” Science 309:324.CrossRefGoogle ScholarPubMed
Lemons, D., and McGinnis, W.. 2006. “Genomic Evolution of Hox Gene Clusters.” Science 313:1918–22.CrossRefGoogle ScholarPubMed
Levitt, M. 2009. “Nature of the Protein Universe.” Proceedings of the National Academy of Sciences of the United States of America 106:11079–84.Google ScholarPubMed
Li, W.-H. 1997. Molecular Evolution. Sunderland, MA: Sinauer.Google ScholarPubMed
Liang, Y. H., Hua, Z. Q., Liang, X., Xu, Q., and Lu, G. Y.. 2001. “The Crystal Structure of Bar-Headed Goose Hemoglobin in Deoxy Form: The Allosteric Mechanism of a Hemoglobin Species with High Oxygen Affinity.” Journal of Molecular Biology 313:123–37.CrossRefGoogle ScholarPubMed
Lipman, D. J., and Wilbur, W. J.. 1991. “Modeling Neutral and Selective Evolution of Protein Folding.” Proceedings of the Royal Society of London B 245:7–11.Google Scholar
MacCarthy, T., Seymour, R., and Pomiankowski, A.. 2003. “The Evolutionary Potential of the Drosophila Sex Determination Gene Network.” Journal of Theoretical Biology 225:461–68.CrossRefGoogle ScholarPubMed
Mackey, M. C., and Glass, L.. 1977. “Oscillation and Chaos in Physiological Control Systems.” Science 197:287–88.CrossRefGoogle ScholarPubMed
May, R. M. 1976. “Simple Mathematical Models with Very Complicated Dynamics.” Nature 261:459–67.CrossRefGoogle ScholarPubMed
Maynard-Smith, J. 1970. “Natural Selection and the Concept of a Protein Space.” Nature 255:563–64.Google Scholar
Maynard-Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D., and Wolpert, L.. 1985. “Developmental Constraints and Evolution.” Quarterly Review of Biology 60:265–87.Google Scholar
Mayr, E. 1961. “Cause and Effect in Biology.” Science 134:1501–6.CrossRefGoogle ScholarPubMed
Millstein, R. L. 2000. “Chance and Macroevolution.” Philosophy of Science 67:603–24.CrossRefGoogle Scholar
Millstein, R. L.. 2002. “Are Random Drift and Natural Selection Conceptually Distinct?” Biology and Philosophy 17:33–53.CrossRefGoogle Scholar
Morton, B. R. 2003. “The Role of Context-Dependent Mutations in Generating Compositional and Codon Usage Bias in Grass Chloroplast DNA.” Journal of Molecular Evolution 56:616–29.CrossRefGoogle ScholarPubMed
Newman, S. A., and Bhat, R.. 2009. “Dynamical Patterning Modules: A ‘Pattern Language’ for Development and Evolution of Multicellular Form.” International Journal of Developmental Biology 53:693–705.CrossRefGoogle Scholar
Niu, D. K., Lin, K., and Zhang, D. Y.. 2003. “Strand Compositional Asymmetries of Nuclear DNA in Eukaryotes.” Journal of Molecular Evolution 57:325–34.CrossRefGoogle ScholarPubMed
Odell, G. M., Oster, G., Alberch, P., and Burnside, B.. 1981. “The Mechanical Basis of Morphogenesis.” Pt. 1, “Epithelial Folding and Invagination.” Developmental Biology 85:446–62.CrossRefGoogle Scholar
Omilian, A. R., Cristescu, M. E. A., Dudycha, J. L., and Lynch, M.. 2006. “Ameiotic Recombination in Asexual Lineages of Daphnia.” Proceedings of the National Academy of Sciences of the United States of America 103:18638–43.Google ScholarPubMed
Ossowski, S., Schneeberger, K., Lucas-Lledo, J. I., Warthmann, N., Clark, R. M., Shaw, R. G., Weigel, D., and Lynch, M.. 2009. “The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis Thaliana.” Science 327:92–94.CrossRefGoogle Scholar
Oster, G. F., Shubin, N., Murray, J. D., and Alberch, P.. 1988. “Evolution and Morphogenetic Rules—the Shape of the Vertebrate Limb in Ontogeny and Phylogeny.” Evolution 42:862–84.CrossRefGoogle ScholarPubMed
Price, N. D., Papin, J. A., Schilling, C. H., and Palsson, B. O.. 2003. “Genome-Scale Microbial in Silico Models: The Constraints-Based Approach.” Trends in Biotechnology 21:162–69.CrossRefGoogle ScholarPubMed
Rehmann, L., and Daugulis, A. J.. 2008. “Enhancement of PCB Degradation by Burkholderia xenovorans LB400 in Biphasic Systems by Manipulating Culture Conditions.” Biotechnology and Bioengineering 99:521–28.CrossRefGoogle ScholarPubMed
Reidhaar-Olson, J. F., and Sauer, R. T.. 1990. “Functionally Acceptable Substitutions in 2 Alpha-Helical Regions of Lambda Repressor.” Proteins: Structure, Function, and Genetics 7:306–16.Google Scholar
Reidys, C. M., and Stadler, P. F.. 2002. “Combinatorial Landscapes.” SIAM Review 44:3–54.CrossRefGoogle Scholar
Reidys, C. M., Stadler, P. F., and Schuster, P.. 1997. “Generic Properties of Combinatory Maps: Neutral Networks of RNA Secondary Structures.” Bulletin of Mathematical Biology 59:339–97.CrossRefGoogle ScholarPubMed
Rodrigues, J. F., and Wagner, A.. 2009. “Evolutionary Plasticity and Innovations in Complex Metabolic Reaction Networks.” PLoS Computational Biology 5:e1000613.CrossRefGoogle Scholar
Rodrigues, J. F., and Wagner, A.. 2011. “Genotype Networks in Sulfur Metabolism.” BMC Systems Biology 5:39.CrossRefGoogle Scholar
Samal, A., Rodrigues, J. F. M., Jost, J., Martin, O. C., and Wagner, A.. 2010. “Genotype Networks in Metabolic Reaction Spaces.” BMC Systems Biology 4:30.CrossRefGoogle ScholarPubMed
Schonborn, C. 2005. “Finding Design in Nature.” New York Times, July 7.Google Scholar
Schuster, P., Fontana, W., Stadler, P., and Hofacker, I.. 1994. “From Sequences to Shapes and Back—a Case-Study in RNA Secondary Structures.” Proceedings of the Royal Society of London B 255:279–84.Google Scholar
Shubin, N. H., and Alberch, P.. 1986. “A Morphogenetic Approach to the Origin and Basic Organization of the Tetrapod Limb.” Evolutionary Biology 20:319–87.Google Scholar
Simpson, G. G. 1953. The Major Features of Evolution. New York: Columbia University Press.CrossRefGoogle Scholar
Sober, E. 1984. The Nature of Selection. Cambridge, MA: MIT Press.Google Scholar
Sober, E.. 2000. Philosophy of Biology. Boulder, CO: Westview.Google Scholar
Sokal, R. R., and Rohlf, F. J.. 1981. Biometry. New York: Freeman.Google Scholar
Sumedha, O., Martin, C., and Wagner, A.. 2007. “New Structural Variation in Evolutionary Searches of RNA Neutral Networks.” Biosystems 90:475–85.CrossRefGoogle ScholarPubMed
Takiguchi, M., Matsubasa, T., Amaya, Y., and Mori, M.. 1989. “Evolutionary Aspects of Urea Cycle Enzyme Genes.” Bioessays 10:163–66.CrossRefGoogle ScholarPubMed
Todd, A. E., Orengo, C. A., and Thornton, J. M.. 2001. “Evolution of Function in Protein Superfamilies, from a Structural Perspective.” Journal of Molecular Biology 307:1113–43.CrossRefGoogle ScholarPubMed
Touchon, M., and Rocha, E. P. C.. 2008. “From Gc Skews to Wavelets: A Gentle Guide to the Analysis of Compositional Asymmetries in Genomic Data.” Biochimie 90:648–59.CrossRefGoogle Scholar
van der Meer, J. R. 1995. “Evolution of Novel Metabolic Pathways for the Degradation of Chloroaromatic Compounds.” Paper presented at the Beijerinck Centennial Symposium on Microbial Physiology and Gene Regulation—Emerging Principles and Applications, The Hague, December.Google Scholar
van der Meer, J. R., Werlen, C., Nishino, S. F., and Spain, J. C.. 1998. “Evolution of a Pathway for Chlorobenzene Metabolism Leads to Natural Attenuation in Contaminated Groundwater.” Applied and Environmental Microbiology 64:4185–93.CrossRefGoogle ScholarPubMed
Wagner, A. 2005. “Circuit Topology and the Evolution of Robustness in Two-Gene Circadian Oscillators.” Proceedings of the National Academy of Sciences of the United States of America 102:11775–80.Google ScholarPubMed
Wagner, A.. 2011. The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems. Oxford: Oxford University Press.CrossRefGoogle Scholar
Wagner, G. P., Amemiya, C., and Ruddle, F.. 2003. “Hox Cluster Duplications and the Opportunity for Evolutionary Novelties.” Proceedings of the National Academy of Sciences of the United States of America 100:14603–6.Google ScholarPubMed
Wimsatt, W. C. 1980. “Randomness and Perceived Randomness in Evolutionary Biology.” Synthese 43:287–329.CrossRefGoogle Scholar