Information theory can help quantify the potential of new phenotypes to originate as exaptations

Abstract

Exaptations are adaptive traits that do not originate <jats:italic>de novo</jats:italic> but from other adaptive traits. They include complex macroscopic traits, such as the middle ear bones of mammals, which originated from reptile jaw bones, but also molecular traits, such as new binding sites of transcriptional regulators. What determines whether a trait originates <jats:italic>de novo</jats:italic> or as an exaptation is unknown. I here use simple information theoretic concepts to quantify a molecular phenotype’s potential to give rise to new phenotypes. These quantities rely on the amount of genetic information needed to encode a phenotype. I use these quantities to estimate the propensity of new transcription factor binding phenotypes to emerge <jats:italic>de novo</jats:italic> or exaptively, and do so for 187 mouse transcription factors. I also use them to quantify whether an organism’s viability in one of 10 different chemical environment is likely to arise exaptively. I show that informationally expensive traits are more likely to originate exaptively. Exaptive evolution is only sometimes favored for new transcription factor binding, but it is always favored for the informationally complex metabolic phenotypes I consider. As our ability to genotype evolving populations increases, so will our ability to understand how phenotypes of ever-increasing informational complexity originate in evolution.