Modularity, criticality, and evolvability of a developmental gene regulatory network

  1. Berta Verd  Is a corresponding author
  2. Nicholas AM Monk
  3. Johannes Jaeger  Is a corresponding author
  1. Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Spain
  2. University of Sheffield, United Kingdom

Abstract

The existence of discrete phenotypic traits suggests that the complex regulatory processes which produce them are functionally modular. These processes are usually represented by networks. Only modular networks can be partitioned into intelligible subcircuits able to evolve relatively independently. Traditionally, functional modularity is approximated by detection of modularity in network structure. However, the correlation between structure and function is loose. Many regulatory networks exhibit modular behaviour without structural modularity. Here we partition an experimentally tractable regulatory network-the gap gene system of dipteran insects-using an alternative approach. We show that this system, although not structurally modular, is composed of dynamical modules driving different aspects of whole-network behaviour. All these subcircuits share the same regulatory structure, but differ in components and sensitivity to regulatory interactions. Some subcircuits are in a state of criticality, while others are not, which explains the observed differential evolvability of the various expression features in the system.

Data availability

Gap gene expression data used to solve and fit the full model are available as supplementary information (S1_Data.ods; https://doi.org/10.1371/journal.pbio.2003174.s009) in Verd et al. (2018, PLoS Biology) . They were published previously in Ashyraliev et al. (2009, PLoS Comp Biol 5: e1000548). Optimizaton and simulation code is available freely online at: https://subversion.assembla.com/svn/flysa.

Article and author information

Author details

  1. Berta Verd

    EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
    For correspondence
    bertaverd@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9835-009X
  2. Nicholas AM Monk

    School of Mathematics and Statistics, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5465-4857
  3. Johannes Jaeger

    EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
    For correspondence
    yoginho@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Funding

MINECO (BFU2009-10184/BFU2012-33775/SEV-2012-0208)

  • Johannes Jaeger

Plan Nacional Grant (BFU2009-10184/BFU2012-33775)

  • Johannes Jaeger

European Commission (FP7-KBBE-2011-5/289434 (BioPreDyn))

  • Johannes Jaeger

MEC-EMBL

  • Johannes Jaeger

La Caixa Savings Bank

  • Berta Verd

KLI Klosterneuburg.

  • Berta Verd
  • Johannes Jaeger

Wissenschaftskolleg zu Berlin

  • Johannes Jaeger

Max-Planck-Gesellschaft

  • Johannes Jaeger

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2019, Verd et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Berta Verd
  2. Nicholas AM Monk
  3. Johannes Jaeger
(2019)
Modularity, criticality, and evolvability of a developmental gene regulatory network
eLife 8:e42832.
https://doi.org/10.7554/eLife.42832

Share this article

https://doi.org/10.7554/eLife.42832

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