Interaction range of common goods shapes Black Queen dynamics beyond the cheater-cooperator narrative

Abstract

Dependencies among microorganisms often appear mutualistic in the lab, as microbes grow faster together than alone. However, according to the Black Queen (BQ) hypothesis, these dependencies are underpinned by the evolutionary benefits from loss-of-function mutations when others in the community can supply the necessary common goods. BQ dynamics often describe a cheater-cooperator scenario, where some ecotypes, the "cheaters," produce no common goods and rely on others, the "cooperators", for survival. We have previously proposed that in systems with multiple common goods, an alternative endpoint for BQ dynamics can emerge. This endpoint describes an ecosystem of interdependent ecotypes engaging in "mutual cheating", i.e. where common good production is distributed. However, even with multiple goods the common good production can be centralized, i.e. with one ecotype providing all common goods for the ecosystem. Here, we present an eco-evolutionary model that reveals that BQ dynamics can result in both distributed- or centralized common good production. The interaction range, i.e. the number of beneficiaries a producer can support, distinguishes between these two endpoints. While many ecosystems evolve to be maximally distributed or maximally centralized, we also find intermediate ecosystems, where ecotypes that appear redundant are coexisting for long periods of time. Due to the limited interaction range, these redundant ecotypes are unable to distribute the production of common goods fully due to the presence of non-producing types. Despite non-producers thus stalling the division of labor, we observe that sudden structural shifts can occur that purge the non-producers from the ecosystem. Overall, our findings broaden the understanding of BQ dynamics, unveiling complex interactions beyond the simple cheater-cooperator narrative.