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Evolutionary capacitance as a general feature of complex gene networks

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  • Aviv Bergman

    (Stanford University
    Stanford University)

  • Mark L. Siegal

    (Stanford University)

Abstract

An evolutionary capacitor buffers genotypic variation under normal conditions, thereby promoting the accumulation of hidden polymorphism. But it occasionally fails, thereby revealing this variation phenotypically1. The principal example of an evolutionary capacitor is Hsp90, a molecular chaperone that targets an important set of signal transduction proteins. Experiments in Drosophila and Arabidopsis have demonstrated three key properties of Hsp90: (1) it suppresses phenotypic variation under normal conditions and releases this variation when functionally compromised; (2) its function is overwhelmed by environmental stress; and (3) it exerts pleiotropic effects on key developmental processes1,2. But whether these properties necessarily make Hsp90 a significant and unique facilitator of adaptation1,2,3,4,5,6,7,8,9,10 is unclear. Here we use numerical simulations of complex gene networks, as well as genome-scale expression data from yeast single-gene deletion strains, to present a mechanism that extends the scope of evolutionary capacitance beyond the action of Hsp90 alone. We illustrate that most, and perhaps all, genes reveal phenotypic variation when functionally compromised, and that the availability of loss-of-function mutations accelerates adaptation to a new optimum phenotype. However, this effect does not require the mutations to be conditional on the environment. Thus, there might exist a large class of evolutionary capacitors whose effects on phenotypic variation complement the systemic, environment-induced effects of Hsp90.

Suggested Citation

  • Aviv Bergman & Mark L. Siegal, 2003. "Evolutionary capacitance as a general feature of complex gene networks," Nature, Nature, vol. 424(6948), pages 549-552, July.
  • Handle: RePEc:nat:nature:v:424:y:2003:i:6948:d:10.1038_nature01765
    DOI: 10.1038/nature01765
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    Citations

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    Cited by:

    1. Stefano Ciliberti & Olivier C Martin & Andreas Wagner, 2007. "Robustness Can Evolve Gradually in Complex Regulatory Gene Networks with Varying Topology," PLOS Computational Biology, Public Library of Science, vol. 3(2), pages 1-10, February.
    2. Rodríguez, Ricardo A. & Duncan, Janelle M. & Vanni, Michael J. & Melkikh, Alexey V. & Delgado, Juan D. & Riera, Rodrigo & Herrera, Ada M. & Camarena, Tomás & Quirós, Ángel & Fernández-Palacios, José M, 2017. "Exploring the analytical consequences of ecological subjects unwittingly neglected by the mainstream of evolutionary thought," Ecological Modelling, Elsevier, vol. 355(C), pages 70-83.
    3. Wang, Fei & Yang, Yongqing & Hu, Manfeng & Xu, Xianyun, 2015. "Projective cluster synchronization of fractional-order coupled-delay complex network via adaptive pinning control," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 434(C), pages 134-143.
    4. Zhang, Yan-Jie & Liu, Song & Yang, Ran & Tan, Ying-Ying & Li, Xiaoyan, 2019. "Global synchronization of fractional coupled networks with discrete and distributed delays," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 514(C), pages 830-837.
    5. Zhu, Ruiyuan & Guo, Yingxin & Wang, Fei, 2020. "Quasi-synchronization of heterogeneous neural networks with distributed and proportional delays via impulsive control," Chaos, Solitons & Fractals, Elsevier, vol. 141(C).
    6. Dawei Ding & Ya Wang & Yongbing Hu & Zongli Yang & Hongwei Zhang & Xu Zhang, 2022. "Pinning synchronization and parameter identification of fractional-order complex-valued dynamical networks with multiple weights," The European Physical Journal B: Condensed Matter and Complex Systems, Springer;EDP Sciences, vol. 95(8), pages 1-12, August.
    7. Casper J Breuker & James S Patterson & Christian Peter Klingenberg, 2006. "A Single Basis for Developmental Buffering of Drosophila Wing Shape," PLOS ONE, Public Library of Science, vol. 1(1), pages 1-7, December.
    8. Tracy Chih-Ting Koubkova-Yu & Jung-Chi Chao & Jun-Yi Leu, 2018. "Heterologous Hsp90 promotes phenotypic diversity through network evolution," PLOS Biology, Public Library of Science, vol. 16(11), pages 1-29, November.
    9. Krishnan, Arun & Tomita, Masaru & Giuliani, Alessandro, 2008. "Evolution of gene regulatory networks: Robustness as an emergent property of evolution," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 387(8), pages 2170-2186.

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