Only accessible information is useful: insights from gradient-mediated patterning

Abstract

Information theory is gaining popularity as a tool to characterize performance of biological systems. However, information is commonly quantified without reference to whether or how a system could extract and use it; as a result, information-theoretic quantities are easily misinterpreted. Here, we take the example of pattern-forming developmental systems which are commonly structured as cascades of sequential gene expression steps. Such a multi-tiered structure appears to constitute sub-optimal use of the positional information provided by the input morphogen because noise is added at each tier. However, one must distinguish between the total information in a morphogen and information that can be usefully extracted and interpreted by downstream elements. We demonstrate that quantifying the information that is accessible to the system naturally explains the prevalence of multi-tiered network architectures as a consequence of the noise inherent to the control of gene expression. We support our argument with empirical observations from patterning along the major body axis of the fruit fly embryo. We use this example to highlight the limitations of the standard information-theoretic characterization of biological signalling, which are frequently de-emphasized, and illustrate how they can be resolved.