Life cycles shape parasite evolution: comparative population genetics of salmon trematodes.

Abstract

Little is known about what controls effective sizes and migration rates among parasite populations. Such data are important given the medical, veterinary, and economic (e.g., fisheries) impacts of many parasites. The autogenic-allogenic hypothesis, which describes ecological patterns of parasite distribution, provided the foundation on which we studied the effects of life cycles on the distribution of genetic variation within and among parasite populations. The hypothesis states that parasites cycling only in freshwater hosts (autogenic life cycle) will be more limited in their dispersal ability among aquatic habitats than parasites cycling through freshwater and terrestrial hosts (allogenic life cycle). By extending this hypothesis to the level of intraspecific genetic variation, we examined the effects of host dispersal on parasite gene flow. Our a priori prediction was that for a given geographic range, autogenic parasites would have lower gene flow among subpopulations. We compared intraspecific mitochondrial DNA variation for three described species of trematodes that infect salmonid fishes. As predicted, autogenic species had much more highly structured populations and much lower gene flow among subpopulations than an allogenic species sampled from the same locations. In addition, a cryptic species was identified for one of the autogenic trematodes. These results show how variation in life cycles can shape parasite evolution by predisposing them to vastly different genetic structures. Thus, we propose that knowledge of parasite life cycles will help predict important evolutionary processes such as speciation, coevolution, and the spread of drug resistance.