A latent capacity for evolutionary innovation through exaptation in metabolic systems

A computational analysis of the ability of a metabolic reaction network to synthesize all biomass from a single source of carbon and energy shows that when such networks are required to be viable on one particular carbon source, they are typically also viable on multiple other carbon sources that were not targets of selection. This paper uses a systems biology approach to answer one of the oldest questions in evolutionary biology: what proportion of evolutionary innovations or adaptations have their origins in non-adaptive traits, or traits — such as feathers not for flying — whose benefits to a creature are unrelated to how they first arose. Aditya Barve and Andreas Wagner simulated real metabolic networks able to sustain life on different carbon sources. By sampling these networks, they found that networks viable on a specific carbon source were actually able to metabolize several other carbon sources. These results show that metabolic systems harbour multiple hidden pre-adaptations that might evolve into novel functions. This study also suggests that many innovations may have non-adaptive origins. Some evolutionary innovations may originate non-adaptively as exaptations, or pre-adaptations, which are by-products of other adaptive traits1,2,3,4,5. Examples include feathers, which originated before they were used in flight2, and lens crystallins, which are light-refracting proteins that originated as enzymes6. The question of how often adaptive traits have non-adaptive origins has profound implications for evolutionary biology, but is difficult to address systematically. Here we consider this issue in metabolism, one of the most ancient biological systems that is central to all life. We analyse a metabolic trait of great adaptive importance: the ability of a metabolic reaction network to synthesize all biomass from a single source of carbon and energy. We use novel computational methods to sample randomly many metabolic networks that can sustain life on any given carbon source but contain an otherwise random set of known biochemical reactions. We show that when we require such networks to be viable on one particular carbon source, they are typically also viable on multiple other carbon sources that were not targets of selection. For example, viability on glucose may entail viability on up to 44 other sole carbon sources. Any one adaptation in these metabolic systems typically entails multiple potential exaptations. Metabolic systems thus contain a latent potential for evolutionary innovations with non-adaptive origins. Our observations suggest that many more metabolic traits may have non-adaptive origins than is appreciated at present. They also challenge our ability to distinguish adaptive from non-adaptive traits.