Ecology directs host-parasite coevolutionary trajectories across Daphnia-microparasite populations

Abstract

Host-parasite interactions often fuel coevolutionary change. However, parasitism is one of a myriad of possible ecological interactions in nature. Biotic (e.g., predation) and abiotic (e.g., temperature) variation can amplify or dilute parasitism as a selective force on hosts and parasites, driving population variation in (co)evolutionary trajectories. We dissected the relationships between wider ecology and coevolutionary trajectory using 16 ecologically complex Daphnia magna-Pasteuria ramosa ponds seeded with an identical starting host (Daphnia) and parasite (Pasteuria) population. We show, using a time-shift experiment and outdoor population data, how multivariate biotic and abiotic ecological differences between ponds caused coevolutionary divergence. Wider ecology drove variation in host evolution of resistance, but not parasite infectivity; parasites subsequently coevolved in response to the changing complement of host genotypes, such that parasites adapted to historically resistant host genotypes. Parasitism was a stronger interaction for the parasite than for its host, likely because the host is the principal environment and selective force, whereas for hosts, parasite-mediated selection is one of many sources of selection. Our findings reveal the mechanisms through which wider ecology creates coevolutionary hotspots and coldspots in biologically realistic arenas of host-parasite interaction, and sheds light on how the ecological theatre can affect the (co)evolutionary play.