The evolution of autonomy from two cooperative specialists in fluctuating environments

Abstract

From microbes to humans, organisms perform numerous tasks for their survival, including food acquisition, migration, and reproduction. A complex biological task can be performed by either an autonomous organism or by cooperation among several specialized organisms. However, it remains unclear how autonomy and cooperation evolutionarily switch. For example, it remains unclear whether and how a group of cooperative specialists can evolve into an autonomous organism. Here, we address this question by experimentally evolving a mutualistic microbial consortium composed of two specialists that cooperatively degrade naphthalene. We observed that autonomous genotypes capable of performing the entire naphthalene degradation pathway evolved from two cooperative specialists and came to dominate the microbial community. This evolutionary transition was driven by the horizontal gene transfer between the two specialists. However, this evolution was exclusively observed to occur in the fluctuating environment supplied with either naphthalene or pyruvate, where mutualism and competition between the two specialists alternated. The naphthalene-supplied environment exerts selective pressure that favors the expansion of autonomous genotypes but was associated with both low cell density and low coexistence levels. In contrast, the pyruvate-supplying environment promoted the coexistence and cell density of the cooperative specialists, thereby increasing the likelihood of horizontal gene transfer. Using a mathematical model, we quantitatively demonstrate that environmental fluctuations facilitate the evolution of autonomy through HGT when the relative growth rate and carrying capacity of the cooperative specialists allow enhanced coexistence and higher cell density in the competitive environment. Together, our results demonstrate that mutualistic cooperation can evolve into autonomous organisms through direct genetic exchange under specific conditions, including the alternation of mutualism and competition in fluctuating environments in a manner frequently occurring in nature.