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Relationship among phenotypic plasticity, phenotypic fluctuations, robustness, and evolvability; Waddington’s legacy revisited under the spirit of Einstein

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Abstract

Questions on possible relationship between phenotypic plasticity and evolvability, and that between robustness and evolution have been addressed over decades in the field of evolution-development. Based on laboratory evolution experiments and numerical simulations of gene expression dynamics model with an evolving transcription network, we propose quantitative relationships on plasticity, phenotypic fluctuations, and evolvability. By introducing an evolutionary stability assumption on the distribution of phenotype and genotype, the proportionality among phenotypic plasticity against environmental change, variances of phenotype fluctuations of genetic and developmental origins, and evolution speed is obtained. The correlation between developmental robustness to noise and evolutionary robustness to mutation is analysed by simulations of the gene network model. These results provide quantitative formulation on canalization and genetic assimilation, in terms of fluctuations of gene expression levels.

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References

  • Abe H and Go N 1980 Noninteracting local-structure model of folding and unfolding transition in globular proteins. I. Formulation; Biopolymers 20 1013

    Article  Google Scholar 

  • Alon U, Surette M G, Barkai N and Leibler S 1999 Robustness in bacterial chemotaxis; Nature (London) 397 168–171

    Article  CAS  Google Scholar 

  • Ancel L W and Fontana W 2002 Plasticity, evolvability, and modularity in RNA; J. Exp. Zool. 288 242–283

    Article  Google Scholar 

  • Bar-Even A, Paulsson J, Maheshri N, Carmi M, O’shea E, Pilpel Y and Barkai N 2006, Noise in protein expression scales with natural protein abundance; Nat. Genet. 38 636–643

    Article  CAS  Google Scholar 

  • Barkai N and Leibler S 1997 Robustness in simple biochemical networks; Nature (London) 387 913–917

    Article  CAS  Google Scholar 

  • Callahan H S, Pigliucci M and Schlichting C D 1997 Developmental phenotypic plasticity: where ecology and evolution meet molecular biology; Bioessays 19 519–525

    Article  CAS  Google Scholar 

  • Ciliberti S, Martin O C and Wagner A 2007 Robustness can evolve gradually in complex regulatory gene networks with varying topology; PLoS Comp. Biol. 3 e15

    Article  Google Scholar 

  • de Visser J A, Hermisson J, Wagner G P, Ancelmeyers L, Bagheri-Chichian H, Blanchard J L, Lin C, Cheverud J M. et al. 2003 Evolution and detection of genetic robustness; Evolution 57 1959–1972

    PubMed  Google Scholar 

  • Eigen M and Schuster P 1979 The hypercycle (Heidelberg: Springer)

    Book  Google Scholar 

  • Einstein A 1926 Investigation on the Theory of of Brownian Movement (Collection of papers ed. by R Furth), Dover (reprinted 1956)

  • Elowitz M B, Levine A J, Siggia E D and Swain P S 2002 Stochastic gene expression in a single cell; Science 297 1183–1187

    Article  CAS  Google Scholar 

  • Fisher R A 1930 The genetical theory of natural selection (Oxford University Press) (reprinted 1958)

  • Furusawa C and Kaneko K 2008 A generic mechanism for adaptive growth rate regulation; PLoS Comput. Biol 4 e3

    Article  Google Scholar 

  • Furusawa C, Suzuki T, Kashiwagi A, Yomo T and Kaneko K 2005 Ubiquity of log-normal distributions in intra-cellular reaction dynamics; Biophysics 1 25–31

    Article  CAS  Google Scholar 

  • Gibson G and Wagner G P 2000 Canalization in evolutionary genetics: a stabilizing theory?; Bioessays 22 372–380

    Article  CAS  Google Scholar 

  • Glass L and Kauffman S A 1973 The logical analysis of continuous, non-linear biochemical control networks; J. Theor. Biol. 39 103–129

    Article  CAS  Google Scholar 

  • Hasty J, Pradines J, Dolnik M and Collins J J 2000 Noise-based switches and amplifiers for gene expression; Proc. Natl. Acad. Sci. USA 97 2075–2080

    Article  CAS  Google Scholar 

  • Ito Y, Toyota H, Kaneko K and Yomo T 2009 How evolution affects phenotypic fluctuation; Mol. Syst. Biol. 5 264

    Article  Google Scholar 

  • Kaern M, Elston T C, Blake W J and Collins J J 2005 Stochasticity in gene expression: from theories to phenotypes; Nat. Rev. Genet. 6 451–464

    Article  CAS  Google Scholar 

  • Kaneko K 2006 Life: An introduction to complex systems biology (Heidelberg and New York: Springer)

    Book  Google Scholar 

  • Kaneko K 2007 Evolution of robustness to noise and mutation in gene expression dynamics; PLoS ONE 2 e434

    Article  Google Scholar 

  • Kaneko K 2008 Shaping Robust system through evolution; Chaos 18 026112

    Article  Google Scholar 

  • Kaneko K and Furusawa C 2006 An evolutionary relationship between genetic variation and phenotypic fluctuation; J. Theor. Biol. 240 78–86

    Article  Google Scholar 

  • Kaneko K and Furusawa C 2008 Consistency principle in biological dynamical systems; Theor. Biosci. 127 195–204

    Article  Google Scholar 

  • Kaneko K and Yomo T 1999 Isologous diversification for robust development of cell society; J. Theor. Biol. 199 243–256

    Article  CAS  Google Scholar 

  • Kaneko K and Yomo T 2000 Sympatric Speciation: compliance with phenotype diversification from a single genotype; Proc. R. Soc. B London 267 2367–2373

    Article  CAS  Google Scholar 

  • Kaneko K 2002 Symbiotic sympatric speciation: Compliance with interaction-driven phenotype differentiation from a single genotype; Popul. Ecol. 44 71–85

    Article  Google Scholar 

  • Kashiwagi A, Urabe I, Kaneko K and Yomo T 2006 Adaptive response of a gene network to environmental changes by attractor selection; PLoS ONE 1 e49

    Article  Google Scholar 

  • Kirschner M W and Gerhart J C 2005 The plausibility of life (Yale University Press)

  • Krishna S, Banerjee B, Ramakrishnan T V and Shivashankar G V 2005 Stochastic simulations of the origins and implications of long-tailed distributions in gene expression; Proc. Natl. Acad. Sci. USA 102 4771–4776

    Article  CAS  Google Scholar 

  • Kubo R, Toda M and Hashitsume N 1985 Statistical Physics II: (English translation; Springer).

  • Landry C R, Lemos B, Rifkin S A, Dickinson W J and Hartl D L 2007 Genetic properties influencing the evolvability of gene expression; Science 317 118–121

    Article  CAS  Google Scholar 

  • Lehner B 2008 Selection to minimize noise in living systems and its implications for the evolution of gene expression; Mol. Syst. Biol. 4 170

    Article  Google Scholar 

  • Li F, Long T, Lu Y, Ouyang Q and Tang C 2004 The yeast cellcycle network is robustly designed; Proc. Natl. Acad. Sci. USA 101 10040–10046

    Google Scholar 

  • McAdams H H and Arkin A 1997 Stochastic mechanisms in gene expression; Proc. Natl. Acad. Sci. USA 94 814–819

    Article  CAS  Google Scholar 

  • Mjolsness E, Sharp D H and Reinitz J 1991 A connectionist model of development; J. Theor. Biol. 152 429–453

    Article  CAS  Google Scholar 

  • Onuchic J N, Wolynes P G, Luthey-Schulten Z and Socci N D 1995 Toward an outline of the topography of a realistic protein-folding funnel; Proc. Natl. Acad. Sci. USA 92 3626–3630

    Article  CAS  Google Scholar 

  • Oosawa F 1975 Effect of the field fluctuation on a macromolecular system; J. Theor. Biol. 52 175

    Article  CAS  Google Scholar 

  • Pigliucci M, Murren C J and Schlichting C D 2006 Phenotypic plasticity and evolution by genetic assimilation; J. Exp. Biol. 209 2362–2367

    Article  Google Scholar 

  • Salazar-Ciudad I, Garcia-Fernandez J and Sole R V 2000 Gene networks capable of pattern formation: from induction to reaction-diffusion; J. Theor. Biol. 205 587–603

    Article  CAS  Google Scholar 

  • Sakata A, Hukushima K and Kaneko K 2009 Funnel landscape and mutational robustness as a result of evolution under thermal noise; Phys. Rev. Lett. 102 148101

    Article  Google Scholar 

  • Sato K and Kaneko K 2007 Evolution equation of phenotype distribution: general formulation and application to error catastrophe; Phys. Rev. E 75 061909

    Article  Google Scholar 

  • Sato K, Ito Y, Yomo T and Kaneko K 2003 On the relation between fluctuation and response in biological systems; Proc. Natl. Acad. Sci. USA 100 14086–14090

    Article  CAS  Google Scholar 

  • Schmalhausen I I 1949 Factors of evolution: The theory of stabilizing selection (Chicago: University of Chicago Press) (reprinted 1986).

    Google Scholar 

  • Spudich J L and Koshland D E Jr 1976 Non-genetic individuality: chance in the single cell; Nature (London) 262 467–471

    Article  CAS  Google Scholar 

  • Ueda M, Sako Y, Tanaka T, Devreotes P and Yanagida T 2001 Single-molecule analysis of chemotactic signaling in Dictyostelium cells; Science 294 864–867

    Article  CAS  Google Scholar 

  • Waddington C H 1942 Canalization of development and the inheritance of acquired characters; Nature (London) 150 563–565

    Article  Google Scholar 

  • Waddington C H 1953 Genetic assimilation of an acquired character; Evolution 7 118–126

    Article  Google Scholar 

  • Waddington C H 1957 The strategy of the genes (London: Allen and Unwin)

    Google Scholar 

  • Wagner A 2000 Robustness against mutations in genetic networks of yeast; Nat. Genet. 24 355–361

    Article  CAS  Google Scholar 

  • Wagner A 2005 Robustness and evolvability in living systems (Princeton, NJ: Princeton University Press)

    Google Scholar 

  • Wagner G P, Booth G and Bagheri-Chaichian H 1997 A population genetic theory of canalization; Evolution 51 329–347

    Article  Google Scholar 

  • Wang J, Huang B, Xia X and Sun Z 2006 Funneled landscape leads to robustness of cellular networks: MAPK signal transduction; Biophys. J. 91 L54–L56

    Article  CAS  Google Scholar 

  • Weinig C 2000 Plasticity versus canalization: Population differences in the timing of shade-avoidance responses; Evolution 54 441–451

    Article  CAS  Google Scholar 

  • West-Eberhard M J 2003 Developmental plasticity and evolution (Oxford: Oxford University Press)

    Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Pure and Applied Sciences, University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo, 153-8902, Japan

    Kunihiko Kaneko

  2. ERATO Complex Systems Biology Project, JST, 3-8-1 Komaba, Meguro-ku, Tokyo, 153-8902, Japan

    Kunihiko Kaneko

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  1. Kunihiko Kaneko
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Correspondence to Kunihiko Kaneko.

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Kaneko, K. Relationship among phenotypic plasticity, phenotypic fluctuations, robustness, and evolvability; Waddington’s legacy revisited under the spirit of Einstein. J Biosci 34, 529–542 (2009). https://doi.org/10.1007/s12038-009-0072-9

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