Obligate mutualistic cooperation limits evolvability

Abstract

Cooperative mutualisms are widespread in nature and play fundamental roles in many ecosystems. Due to the often obligate nature of these interactions, the Darwinian fitness of the participating individuals is not only determined by the information encoded in their own genomes, but also the traits and capabilities of their corresponding interaction partners. Thus, a major outstanding question is how obligate cooperative mutualisms affect the ability of organisms to respond to environmental change with evolutionary adaptation. Here we address this issue using a mutualistic cooperation between two auxotrophic genotypes of Escherichia coli that reciprocally exchange costly amino acids. Amino acid-supplemented monocultures and unsupplemented cocultures were exposed to stepwise increasing concentrations of different antibiotics. This selection experiment revealed that metabolically interdependent bacteria were generally less able to adapt to environmental stress than autonomously growing strains. Moreover, obligate cooperative mutualists frequently regained metabolic autonomy, thus resulting in a collapse of the mutualistic interaction. Together, our results identify a limited evolvability as a significant evolutionary cost that individuals have to pay when entering into an obligate mutualistic cooperation.