The potential for non-adaptive origins of evolutionary innovations in central carbon metabolism

Biological systems are rife with examples of pre-adaptations or exaptations. They range from the molecular scale - lens crystallins, which originated from metabolic enzymes - to the macroscopic scale, such as feathers used in flying, which originally served thermal insulation or waterproofing. An important class of exaptations are novel and useful traits with non-adaptive origins. Whether such origins could be frequent cannot be answered with individual examples, because it is a question about a biological system's potential for exaptation. We here take a step towards answering this question by analyzing central carbon metabolism, and novel traits that allow an organism to survive on novel sources of carbon and energy. We have previously applied flux balance analysis to this system and predicted the viability of 10¹⁵ metabolic genotypes on each of ten different carbon sources.

We here use this exhaustive genotype-phenotype map to ask whether a central carbon metabolism that is viable on a given, focal carbon source C - the equivalent of an adaptation in our framework - is usually or rarely viable on one or more other carbon sources C _new - a potential exaptation. We show that most metabolic genotypes harbor potential exaptations, that is, they are viable on one or more carbon sources C _new . The nature and number of these carbon sources depends on the focal carbon source C itself, and on the biochemical similarity between C and C _new . Moreover, metabolisms that show a higher biomass yield on C, and that are more complex, i.e., they harbor more metabolic reactions, are viable on a greater number of carbon sources C _new .

A high potential for exaptation results from correlations between the phenotypes of different genotypes, and such correlations are frequent in central carbon metabolism. If they are similarly abundant in other metabolic or biological systems, innovations may frequently have non-adaptive ("exaptive") origins.