The interplay between ecological networks drives host-plasmid community dynamics

Ying-Jie Wang , Kaitlin Schaal, Johannes Nauta, Armun Liaghat, Manlio De Domenico, James Hall, Shai Pilosof

Plasmids drive evolution by transferring traits across microbial hosts. Transmission depends on both host–plasmid (infection) and plasmid–plasmid (compatibility) interactions, yet how the structure of these networks shapes transmission remains poorly understood. We hypothesized that these two ecological networks interact in non-additive ways to influence community outcomes. To test this, we developed a stochastic agent-based model that embeds both network structures and simulates coupled host–plasmid dynamics. We systematically varied the structure of each network, both individually and in combination, to isolate the effect of structure on host-plasmid dynamics. A modular (interactions organized into clusters) and hub (interactions concentrated on the highly connected) plasmid-plasmid compatibility network promoted transient host coexistence, while a modular host-plasmid infection network promoted plasmid diversity and stable host coexistence. Importantly, structured networks interacted non-additively, and their impact was most apparent when plasmid carriage imposed a moderate fitness cost on hosts. For example, combining a modular infection network with a hub compatibility network reversed the expected plasmid prevalence patterns, demonstrating that the structure of one network can counteract the effects of the other. We further re-parameterized our model to recapitulate empirical host-plasmid community dynamics, showing that infection network structure can strongly shape plasmid prevalence even in the presence of substantial biological heterogeneity. Our results highlight the necessity of jointly considering host–plasmid infection and plasmid–plasmid compatibility networks to understand host–plasmid community dynamics and their eco-evolutionary potential. More broadly, this work provides an initial mechanistic framework for generating testable hypotheses and underscores that systems involving multiple hosts and infectious agents require explicit consideration of how different ecological networks interact to shape community dynamics.