Testing for local host-parasite adaptation: an experiment with Gyrodactylus ectoparasites and guppy hosts

Hosts and parasites are in a perpetual co-evolutionary "arms race". Due to their short generation time and large reproductive output, parasites are commonly believed to be ahead in this race, although increasing evidence exists that parasites are not always ahead in the arms race - in part owing to evolutionary lineage and recent ecological history. We assess local adaptation of hosts and parasites, and determine whether adaptation was influenced by ecological or evolutionary history, using full reciprocal cross-infections of four Gyrodactylus ectoparasite populations and their four guppy (Poecilia reticulata) host populations in Trinidad. To consider effects of evolutionary lineage and recent ecology, these four populations were collected from two different river drainages (Marianne and Aripo) and two different predation environments (high and low). The highest infection levels were obtained when parasites from the Aripo lineage infected guppies from the Marianne lineage, indicating a higher infectivity, virulence and/or reproductive success of the Aripo parasites. Aripo lineage guppies were also better able to limit Gyrodactylus population growth than guppies from the Marianne River, indicating their strong "resistance" to Gyrodactylus regardless of the source of the parasite. Predation environment had no detectable influence on host-parasite population dynamics of sympatric or allopatric combinations. The much stronger effect of evolutionary lineage (i.e., river) than recent ecological history (i.e., predation) emphasises its importance in driving co-evolutionary dynamics, and should be explored further in future studies on local host-parasite adaptation.