Evolution of robustness to noise and mutation in gene expression dynamics

PLoS One. 2007 May 9;2(5):e434. doi: 10.1371/journal.pone.0000434.

Abstract

Phenotype of biological systems needs to be robust against mutation in order to sustain themselves between generations. On the other hand, phenotype of an individual also needs to be robust against fluctuations of both internal and external origins that are encountered during growth and development. Is there a relationship between these two types of robustness, one during a single generation and the other during evolution? Could stochasticity in gene expression have any relevance to the evolution of these types of robustness? Robustness can be defined by the sharpness of the distribution of phenotype; the variance of phenotype distribution due to genetic variation gives a measure of 'genetic robustness', while that of isogenic individuals gives a measure of 'developmental robustness'. Through simulations of a simple stochastic gene expression network that undergoes mutation and selection, we show that in order for the network to acquire both types of robustness, the phenotypic variance induced by mutations must be smaller than that observed in an isogenic population. As the latter originates from noise in gene expression, this signifies that the genetic robustness evolves only when the noise strength in gene expression is larger than some threshold. In such a case, the two variances decrease throughout the evolutionary time course, indicating increase in robustness. The results reveal how noise that cells encounter during growth and development shapes networks' robustness to stochasticity in gene expression, which in turn shapes networks' robustness to mutation. The necessary condition for evolution of robustness, as well as the relationship between genetic and developmental robustness, is derived quantitatively through the variance of phenotypic fluctuations, which are directly measurable experimentally.

MeSH terms

  • Biological Evolution*
  • Gene Expression*
  • Genotype
  • Models, Theoretical
  • Mutation*
  • Phenotype