Host–parasitoid evolution in a metacommunity

Patch size and isolation are predicted to alter both species diversity and evolution; yet, there are few empirical examples of eco-evolutionary feedback in metacommunities. We tested three hypotheses about eco-evolutionary feedback in a gall-forming fly, Eurosta solidaginis and two of its natural enemies that select for opposite traits: (i) specialization and poor dispersal ability constrain a subset of natural enemies from occupying small and isolated patches, (ii) this constraint alters selection on the gall fly, causing phenotypic shifts towards traits resistant to generalist and dispersive enemies in small and isolated patches, and (iii) reduced dispersal evolves in small, isolated populations. We sampled patches in a natural metacommunity and found support for all hypotheses; Eurosta's specialist wasp parasitoid attacked fewer galls in small and isolated patches, generating a selection gradient that favoured small galls resistant to predation by a dispersive and generalist bird predator. Phenotype distributions matched this selection gradient, and these phenotypic differences were maintained in a common garden experiment. Finally, we found lower dispersal abilities in small and isolated patches, a phenotypic shift that aids in the maintenance of local adaptation. We suggest that the trophic rank and the species traits of consumers are central to evolution in metacommunities.