Emergence of enhanced metabolic entanglement during experimental evolution of an interkingdom microbial community

Obligate symbioses have likely evolved through multiple intermediate steps, resulting in a gradual erosion of independence of initially autonomous entities. Here we observed progression towards an increased entanglement for an engineered mutualistic consortium between Escherichia coli and Saccharomyces cerevisiae. Experimental evolution of this interkingdom community led to a rapid enhancement of metabolic cooperation between partners, including the reinforcement of both selfish and social traits, along with the emergence of a novel dependence of yeast on the bacterial partner for ammonium assimilation. Selection on social traits repeatedly occurred indirectly, via pleiotropies and trade-offs within the cellular regulatory networks, and without the requirement for group selection. We propose that such indirect selection on traits may be a common mechanism in evolutionary transitions towards sociality.