A linear reciprocal relationship between robustness and plasticity in homeostatic biological networks

PLoS One. 2023 Jan 26;18(1):e0277181. doi: 10.1371/journal.pone.0277181. eCollection 2023.

Abstract

In physics of living systems, a search for relationships of a few macroscopic variables that emerge from many microscopic elements is a central issue. We evolved gene regulatory networks so that the expression of core genes (partial system) is insensitive to environmental changes. Then, we found the expression levels of the remaining genes autonomously increase to provide a plastic (sensitive) response. A feedforward structure from the non-core to core genes evolved autonomously. Negative proportionality was observed between the average changes in core and non-core genes, reflecting reciprocity between the macroscopic robustness of homeostatic genes and plasticity of regulator genes. The proportion coefficient between those genes is represented by their number ratio, as in the "lever principle", whereas the decrease in the ratio results in a transition from perfect to partial adaptation, in which only a portion of the core genes exhibits robustness against environmental changes. This reciprocity between robustness and plasticity was satisfied throughout the evolutionary course, imposing an evolutionary constraint. This result suggests a simple macroscopic law for the adaptation characteristic in evolved complex biological networks.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biological Evolution*
  • Gene Regulatory Networks*
  • Homeostasis

Grants and funding

This work was partially supported by the Japan Society for the Promotion of Science (JSPS) (https://www.jsps.go.jp/english/) KAKENHI (17H06386, 20H00123) to K.K., by JSPS KAKENHI (21K15048) to T.S.H., by Novo Nordisk Fonden (https://novonordiskfonden.dk/) to K.K. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.