On the accessibility of adaptive phenotypes of a bacterial metabolic network

TL;DR

This study explores how environmental quality affects the ease of access to adaptive phenotypes in E. coli's metabolic network, revealing that poorer environments create more rugged genotype-phenotype maps, but populations can still adapt via neutral drift.

Contribution

It introduces an analysis of environmental impact on the accessibility of adaptive phenotypes using a flux-balance model and information theory, highlighting the role of GPM ruggedness and information transmission.

Findings

GPM is more rugged in poorer environments, reducing phenotype accessibility.

Approximately 74% of genotypes can be neutral in the most rugged environments.

Higher normalized mutual information correlates with increased adaptive phenotype accessibility.

Abstract

The mechanisms by which adaptive phenotypes spread within an evolving population after their emergence are understood fairly well. Much less is known about the factors that influence the evolutionary accessibility of such phenotypes, a pre-requisite for their emergence in a population. Here, we investigate the influence of environmental quality on the accessibility of adaptive phenotypes of Escherichia coli's central metabolic network. We used an established flux-balance model of metabolism as the basis for a genotype-phenotype map (GPM). We quantified the effects of seven qualitatively different environments (corresponding to both carbohydrate and gluconeogenic metabolic substrates) on the structure of this GPM. We found that the GPM has a more rugged structure in qualitatively poorer environments, suggesting that adaptive phenotypes could be intrinsically less accessible in such environments. Nevertheless, on average ~74% of the genotype can be altered by neutral drift, in the environment where the GPM is most rugged; this could allow evolving populations to circumvent such ruggedness. Furthermore, we found that the normalized mutual information (NMI) of genotype differences relative to phenotype differences, which measures the GPM's capacity to transmit information about phenotype differences, is positively correlated with (simulation-based) estimates of the accessibility of adaptive phenotypes in different environments. These results are consistent with the predictions of a simple analytic theory and they suggest an intuitive information-theoretic principle for evolutionary adaptation; adaptation could be faster in environments where the GPM has a greater capacity to transmit information about phenotype differences.