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Randomness in biology

  • THOMAS HEAMS (a1)
Abstract

Biology has contradictory relationships with randomness. First, it is a complex issue for an empirical science to ensure that apparently random events are truly random, this being further complicated by the loose definitions of unpredictability used in the discipline. Second, biology is made up of many different fields, which have different traditions and procedures for considering random events. Randomness is in many ways an inherent feature of evolutionary biology and genetics. Indeed, chance/Darwinian selection principles, as well as the combinatorial genetic lottery leading to gametes and fertilisation, rely, at least partially, on probabilistic laws that refer to random events. On the other hand, molecular biology has long been based on deterministic premises that have led to a focus on the precision of molecular interactions to explain phenotypes, and, consequently, to the relegation of randomness to the marginal status of ‘noise’. However, recent experimental results, as well as new theoretical frameworks, have challenged this view and may provide unifying explanations by acknowledging the intrinsic stochastic dimension of intracellular pathways as a biological parameter, rather than just as background noise. This should lead to a significant reappraisal of the status of randomness in the life sciences, and have important consequences on research strategies for theoretical and applied biology.

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References
Hide All
Ansel, J.et al. (2008) Cell-to-cell stochastic variation in gene expression is a complex genetic trait. PLoS Genetics 4 e1000049.
Arias, A. M. and Hayward, P. (2006) Filtering transcriptional noise during development: concepts and mechanisms. Nature Reviews Genetics 7 3444.
Arndt, M., Juffmann, T. and Vedral, V. (2009) Quantum physics meets biology. HFSP Journal 3 386400.
Atlan, H. (1972) L'organisation biologique et la théorie de l'information, Seuil, Paris.
Atlan, H. and Koppel, M. (1990) The cellular computer DNA: program or data. Bulletin of Mathematical Biology 52 335348.
Badyaev, A. V. (2005) Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proceedings of the Royal Society B: Biological Sciences 272 877886.
Ball, P. (2011) Physics of life: The dawn of quantum biology. Nature 474 272274.
Bennett, D. C. (1983) Differentiation in mouse melanoma cells: initial reversibility and an on-off stochastic model. Cell 34 445453.
Bjedov, I.et al. (2003) Stress-induced mutagenesis in bacteria. Science 300 14041409.
Brisson, D. (2003) The directed mutation controversy in an evolutionary context. Critical Reviews in Microbiology 29 2535.
Buiatti, M. and Buiatti, M. (2008) Chance vs. necessity in living systems, a false antinomy. Biology Forum 101 2966.
Buiatti, M. and Longo, G. (2011) Randomness and Multi-level Interactions in Biology. arXiv:1104.1110v1.
Burnet, F. M. (1957) A modification of Jerne's theory of antibody production using the concept of clonal selection. Australian Journal of Science 20 6769.
Capp, J. P. (2012) Stochastic gene expression stabilization as a new therapeutic strategy for cancer. Bioessays 34 (3)170–3.
Chang, H. H., Hemberg, M., Barahona, M., Ingber, D. E. and Huang, S. (2008) Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453 544547.
Changeux, J. P. and Danchin, A. (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264 705712.
Changeux, J. P., Courrege, P. and Danchin, A. (1973) A theory of the epigenesis of neuronal networks by selective stabilization of synapses. Proceedings of the National Academy of Sciences of the United States of America 70 29742978.
Chelly, J., Concordet, J. P., Kaplan, J. C. and Kahn, A. (1989) Illegitimate transcription: transcription of any gene in any cell type. Proceedings of the National Academy of Sciences of the United States of America 86 26172621.
Clark, M. B.et al. (2011) The reality of pervasive transcription. PLoS Biology 9 e1000625.
Cox, R. S. 3rd, Dunlop, M. J. and Elowitz, M. B. (2010) A synthetic three-color scaffold for monitoring genetic regulation and noise. Journal of Biological Engineering 4 10.
Cremer, T., Cremer, M., Dietzel, S., Müller, S., Solovei, I. and Fakan, S. (2006) Chromosome territories a functional nuclear landscape. Current Opinion in Cell Biology 18 307316.
Crick, F. H. C. (1958) On Protein Synthesis. Symposia of the Society for Experimental Biology 12 138163.
Darwin, C. (1859) On the Origins of Species, John Murray.
Darwin, C. and Wallace, A. R. (1858) On the Tendency of Species to form Varieties; and on the Perpetuation of Varieties and Species by Natural Means of Selection. Journal of the Proceedings of the Linnean Society of London Zoology 3 4650.
Davidson, E. H.et al. (2002) A genomic regulatory network for development. Science 295 16691678.
Delaye, L. and Moya, A. (2010) Evolution of reduced prokaryotic genomes and the minimal cell concept: variations on a theme. Bioessays 32 281287.
Edelman, G. M. (1987) Neural Darwinism: The Theory of Neuronal Group Selection, Basic Books, New York.
Edelman, G. M. and Mountcastle, V. B. (1978) The Mindful Brain: Cortical Organization and the Group Selective Theory of Higher Brain Function, MIT Press.
Eldredge, N. and Gould, S. J. (1972) Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf, T. J. M. (ed.) Models in Paleobiology, Freeman, Cooper and Company 82115.
Ellis, R. J. (2001) Macromolecular crowding: obvious but underappreciated. Trends in Biochemical Sciences 26 597604.
Elowitz, M. B., Levine, A. J., Siggia, E. D. and Swain, P. S. (2002) Stochastic gene expression in a single cell. Science 297 11831186.
Engel, G. S.et al. (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446 782786.
Ferguson, M. L.et al. (2012) Reconciling molecular regulatory mechanisms with noise patterns of bacterial metabolic promoters in induced and repressed states. Proceedings of the National Academy of Sciences of the United States of America 109 155160.
Fiering, S., Whitelaw, E. and Martin, D. I. (2000) To be or not to be active: the stochastic nature of enhancer action. Bioessays 22 381387.
Franco, M. I., Turin, L., Mershin, A. and Skoulakis, E. M. (2011) Molecular vibration-sensing component in Drosophila melanogaster olfaction. Proceedings of the National Academy of Sciences of the United States of America 108 37973802.
Gordon, A. J. E., Halliday, J. A., Blankschien, M. D., Burns, P. A., Yatagai, F. and Herman, C. (2009) Transcriptional Infidelity Promotes Heritable Phenotypic Change in a Bistable Gene Network. PLoS Biology 7: e1000044.
Gould, S. J. and Lewontin, R. C. (1979) The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme. Proceedings of the Royal Society B: Biological Sciences 205 581598.
Guptasarma, P. (1995) Does replication-induced transcription regulate synthesis of the myriad low copy number proteins of escherichia coli? Bioessays 17 987997.
Heams, T. (2004) Approche endodarwinienne de la variabilité intercellulaire de l'expression génétique, Ph.D. Thesis, Institut national agronomique Paris-Grignon, Paris, France. (Available at http://pastel.archives-ouvertes.fr/pastel-00001189.)
Hettinger, T. P. (2011) Olfaction is a chemical sense, not a spectral sense. Proceedings of the National Academy of Sciences of the United States of America 108 E349.
Hooshangi, S. and Weiss, R. (2006) The effect of negative feedback on noise propagation in transcriptional gene networks. Chaos 16 026108.
Jacob, F. (1970) La logique du vivant, une histoire de l'hérédité. Gallimard. (English translation: The Logic of Life, a history of heredity, Pantheon Books, New York, 1974.)
Jacob, F. and Monod, J. (1961) Genetic regulatory mechanisms in the synthesis of proteins. Journal of Molecular Biology 3 318356.
Jerne, N. (1955) The natural selection theory of antibody formation. Proceedings of the National Academy of Sciences of the United States of America 41 849857.
Kaern, M., Elston, T. C., Blake, W. J. and Collins, J. J. (2005) Stochasticity in gene expression: from theories to phenotypes. Nature Reviews Genetics 6 451464.
Kaufmann, B. B., Yang, Q., Mettetal, J. T. and van Oudenaarden, A. (2007) Heritable stochastic switching revealed by single-cell genealogy. PLoS Biology 5 e239.
Klug, A. (1974) Rosalind Fanklin and the double helix. Nature 248 787788.
Koonin, E. V. (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Reviews Microbiology 1 127136.
Kupiec, J. J. (1981) Théorie probabiliste de la différenciation cellulaire. XIIème rencontre de Méribel 161–163.
Kupiec, J. J. (1983) A probabilist theory for cell differentiation, embryonic mortality and DNA C-value paradox. Speculations in Science and Technology 6 471478.
Kupiec, J. J. (1986) A probabilist theory for cell differentiation: the extension of Darwinian principles to embryogenesis. Speculations in Science and Technology 9 1922.
Kupiec, J. J. (1996) A chance-selection model for cell differentiation. Cell Death and Differentiation 3 385390.
Kupiec, J. J. (1997) A Darwinian theory for the origin of cellular differentiation. Molecular Genetics and Genomics 255 201208.
Kupiec, J. J. (2008) L'Origine des Individus, Fayard, Paris. (English translation: The Origin of Individuals, World Scientific, 2009.)
Laforge, B., Guez, D., Martinez, M. and Kupiec, J. J. (2005) Modeling embryogenesis and cancer: an approach based on an equilibrium between the autostabilization of stochastic gene expression and the interdependence of cells for proliferation. Progress in Biophysics and Molecular Biology 89 93120.
Lehner, B. (2008) Selection to minimise noise in living systems and its implications for the evolution of gene expression. Molecular Systems Biology 4 170.
Lenormand, T., Roze, D. and Rousset, F. (2009) Stochasticity in evolution. Trends in Ecology and Evolution 24 157165.
Longo, G. and Tendero, P. E. (2007) The Differential Method and the Causal Incompleteness of Programming Theory in Molecular Biology. Foundations of Science 12 337366.
Maeda, K.et al. (2008) Chemical compass model of avian magnetoreception. Nature 453 387390.
Madlung, A. and Comai, L. (2004) The Effect of Stress on Genome regulation and Structure. Annals of Botany 94 481495.
Martincorena, I., Seshasayee, A. S. N. and Luscombe, N. M. (2012) Evidence of non-random mutation rates suggests an evolutionary risk management strategy. Nature 485 9598.
Mayr, E. (1961) Cause and effect in biology. Science 134 15011506.
McAdams, H. H. and Arkin, A. (1997) Stochastic mechanisms in gene expression. Proceedings of the National Academy of Sciences of the United States of America 94 814819.
McAdams, H. H. and Arkin, A. (1999) It's a noisy business! Genetic regulation at the nanomolar scale. Trends in Genetics 15 6569.
Merlin, F. (2009) Chance and the sources of biological variation: a critical analysis of a multiple notion, Ph.D. thesis, Institut d'Histoire et Philosophie des Sciences, Université Paris-1, Paris, France.
Mettetal, J. T. and van Oudenaarden, A. (2007) Necessary noise. Science 317 463464.
Michaelson, J. (1993) Cellular selection in the genesis of multicellular organization. Laboratory Investigation 69 136151.
Mikeladze-Dvali, T.et al. (2005) The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 122 775787.
Morange, M. (1994) Histoire de la biologie moléculaire, La Découverte, Paris. (English translation: A History of molecular biology, Harvard University Press, 2000.)
Murphy, K. F., Adams, R. M., Wang, X., Balázsi, G. and Collins, J. J. (2010) Tuning and controlling gene expression noise in synthetic gene networks. Nucleic Acids Research 38 27122726.
Newlands, S.et al. (1998) Transcription occurs in pulses in muscle fibers. Genes and Development 12 27482758.
Nijhout, H. F. (2006) Stochastic gene expression: dominance, thresholds and boundaries. In: Veitia, R. A., (ed.) The Biology of Genetic Dominance, Landes Biosciences 6175.
Noble, D. (2006) The Music Of Life, Oxford University Press.
Parada, L. A., Roix, J. J. and Misteli, T. (2003) An uncertainty principle in chromosome positioning. Trends in Cell Biology 13 393396.
Pilpel, Y. (2011) Noise in biological systems: pros, cons, and mechanisms of control. Methods in Molecular Biology 759 407425.
Polev, D. (2012) Transcriptional noise as a driver of gene evolution. Journal of Theoretical Biology 293 2733.
Raj, A. and van Oudenaarden, A. (2008) Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135 216226.
Raser, J. M. and O'Shea, E. K. (2005) Noise in gene expression: origins, consequences, and control. Science 309 20102013.
Ritz, T., Thalau, P., Phillips, J. B., Wiltschko, R. and Wiltschko, W. (2004) Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429 177180.
Ro, D. K.et al. (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440 940943.
Rojo, D. R.et al. (2011) Influence of stochastic gene expression on the cell survival rheostat after traumatic brain injury. PLoS One 6 e23111.
Rosenberg, A. (2001) Discussion note: Indeterminism, probability, and randomness in evolutionary theory. Philosophy of Science 68 (4)536544.
Ross, I. L., Browne, C. M. and Hume, D. A. (1994) Transcription of individual genes in eukaryotic cells occurs randomly and infrequently. Immunology and Cell Biology 72 177185.
Roux, W. (1881) Der Kampf der Teile im Organismus. Ein Beitrag zur Vervollständigung der mechanischen Zweckmäß igkeitslehre, Engelmann, Leipzig.
Ruvinsky, A. (2009) Genetics and Randomness, CRC Press.
Schrödinger, E. (1944) What is Life? The Physical Aspect of the Living Cell, Cambridge University Press.
Springer, M. and Paulsson, J. (2006) Biological physics: harmonies from noise. Nature 439 2728.
Spudich, J. L. and Koshland, D. E. Jr. (1976) Non-genetic individuality: chance in the single cell. Nature 262 467471.
Stockholm, D.et al. (2007) The origin of phenotypic heterogeneity in a clonal cell population in vitro. PLoS One 2 e394.
Szczebara, F. M.et al. (2003) Total biosynthesis of hydrocortisone from a simple carbon source in yeast. Nature Biotechnology 21 143149.
Tamames, J., Gil, R., Latorre, A., Peretó, J., Silva, F. J. and Moya, A. (2007) The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evolutionary Biology 7 181.
Thattai, M. and van Oudenaarden, A. (2001) Intrinsic noise in gene regulatory networks. Proceedings of the National Academy of Sciences of the United States of America 98 86148619.
Till, J. E., Mc Culloch, E. A. and Siminovitch, L. (1964) A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming. Proceedings of the National Academy of Sciences of the United States of America 51 2936.
Tonegawa, S. (1976) Reiteration frequency of immunoglobulin light chain genes: further evidence for somatic generation of antibody diversity. Proceedings of the National Academy of Sciences of the United States of America 73 203207.
Uversky, V. N. (2011) Intrinsically disordered proteins from A to Z. International Journal of Biochemistry and Cell Biology 43 10901103.
Velasco, J. D. (2012) Objective and subjective probability in gene expression. Progress in Biophysics and Molecular Biology 110 (1)510.
Watson, J. D. and Crick, F. H. (1953) Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171 737738.
Werndl, C. (2012) Probability, Indeterminism and Biological Processes. In: Dieks, D., Wenceslao, J. G., Hartmann, S., Stoeltzner, M. and Weber, M. (eds.) Probabilities, Laws and Structures, The Philosophy of Science in a European Perspective, Volume 3, Springer-Verlag 263277.
Wernet, M. F., Mazzoni, E. O., Celik, A., Duncan, D. M., Duncan, I. and Desplan, C. (2006) Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 440 (7081) 174180.
Wijgerde, M., Grosveld, F. and Fraser, P. (1995) Transcription complex stability and chromatin dynamics in vivo. Nature 377 209213.
Zhou, T., Chen, L. and Aihara, K. (2005) Molecular communication through stochastic synchronization induced by extracellular fluctuations. Physical Review Letters 95 178103.
Zurek, W. (2009) Quantum Darwinism. Nature Physics 5 181188.
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