Modularity, criticality, and evolvability of a developmental gene regulatory network
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
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.
Reviewing Editor
- Lee Altenberg, The KLI Institute, United States
Version history
- Received: January 14, 2019
- Accepted: June 5, 2019
- Accepted Manuscript published: June 6, 2019 (version 1)
- Version of Record published: July 22, 2019 (version 2)
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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