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

Abstract

Dependencies among microorganisms often appear mutualistic, as microbes grow faster together than alone. However, the Black Queen hypothesis (BQH) posits that these dependencies are underpinned by benefits from ‘cheating’ when others supply necessary common goods (CGs). The BQH often describes the evolution of a pair of ecotypes, a cooperator producing a CG and a cheater free-riding upon it. With multiple goods, their production can be centralized, with one ecotype producing everything and others cheating. We previously proposed an alternative BQH endpoint describing a community of ‘mutual cheating’, with production distributed over multiple interdependent ecotypes. Here, we present an individual-based eco-evolutionary model that predicts BQH dynamics resulting in various endpoints, including both distributed and centralizedproduction, and novel intermediate ecosystems involving apparent functional redundancy. These endpoints critically depend on the interaction range, the number of beneficiaries a producer can locally support. The intermediate ecosystems involve stable coexistence among ecotypes partially distributing production, with this coexistence punctuated by rare evolutionary transitions resulting in further distribution. These punctuated dynamics arise from cheaters stalling the division of labour by occupying the limited space within the producers’ interaction ranges. Overall, our findings unveil complex evolutionary dynamics beyond the simple cheater–cooperator narrative, broadening the predictions of BQH.