Selfishness driving reductive evolution shapes interdependent patterns in spatially structured microbial communities

Abstract

AbstractMicrobes release a wide variety of metabolites to the environment that benefit the whole population, called public goods. Public goods sharing drives adaptive function loss, and allows the rise of metabolic cross-feeding. However, how public goods sharing governs the succession of communities over evolutionary time scales remains unclear. To resolve this issue, we constructed an individual-based model, where an autonomous population that possessed functions to produce three essential public goods, was allowed to randomly lose functions. Simulations revealed that function loss genotypes could evolve from the autonomous ancestor, driven by the selfish public production trade-off at the individual level. These genotypes could then automatically develop to three possible types of interdependent patterns: complete functional division, one-way dependency, and asymmetric functional complementation, which were influenced by function cost and function redundancy. In addition, we found random evolutionary events, i.e., the priority and the relative spatial positioning of genotype emergence, are also important in governing community assembly. Moreover, communities occupied by interdependent patterns exhibited better resistance to environmental perturbation, suggesting such patterns are selectively favored. Our work integrates ecological interactions with evolution dynamics, providing a new perspective to explain how reductive evolution shapes microbial interdependencies and governs the succession of communities.