Rapid adaptation accelerates competitive suppression in a parasite community

Environmental stress leads to changes in community composition by altering competitive hierarchies and pushing taxa towards extinction. Parasites and their communities are particularly vulnerable to stress due to environmental sensitivity of infection steps and dependence on host fitness. Parasite populations might avoid extinction through evolutionary rescue-whereby rapid adaptation to stress enables persistence-but the impacts of adaptation to stress on parasite communities remain unclear. Here, we study the evolutionary and ecological impact of thermal stress in a simple parasite community by propagating populations of two viral parasites (bacteriophages φ14-1 and φLUZ19) of Pseudomonas aeruginosa in monoculture and co-culture under two thermal conditions: a control temperature (37°C) and a high temperature that restricts φ14-1 growth (42°C). We show that rapid thermal adaptation of φ14-1 facilitated persistence in monoculture. Rescue of this phage in co-culture made it a superior competitor, and it replaced φLUZ19 as the dominant phage at high temperature. We determine that thermal adaptation occurred through mutations in genes linked to attachment to bacterial hosts and within-host replication. We also show that competitive suppression by φ14-1 constrained φLUZ19 molecular evolution. Our findings suggest that rapid adaptation to environmental stress can prevent the extinction of some parasites but may inadvertently destabilise the community and facilitate further species loss. This work underscores the need to take an eco-evolutionary approach to predict the responses of communities to global climate change.