Contingent evolution of alternative metabolic network topologies determines whether cross-feeding evolves

Abstract

Metabolic exchange is widespread in natural microbial communities and an important driver of ecosystem structure and diversity, yet it remains unclear what determines whether microbes evolve division of labor or maintain metabolic autonomy. Here we use a mechanistic model to study how metabolic strategies evolve in a constant, one resource environment, when metabolic networks are allowed to freely evolve. We find that initially identical ancestral communities of digital organisms follow different evolutionary trajectories, as some communities become dominated by a single, autonomous lineage, while others are formed by stably coexisting lineages that cross-feed on essential building blocks. Our results show how without presupposed cellular trade-offs or external drivers such as temporal niches, diverse metabolic strategies spontaneously emerge from the interplay between ecology, spatial structure, and metabolic constraints that arise during the evolution of metabolic networks. Thus, in the long term, whether microbes remain autonomous or evolve metabolic division of labour is an evolutionary contingency.