An experimental test of host specialization in a ubiquitous polar ectoparasite: a role for adaptation?

The evolution of host specificity is considered to be an essential mechanism driving parasite diversity. It may be governed by adaptive constraints that lead to host-dependent fitness trade-offs. Alternatively, specificity may arise via transmission constraints that isolate parasite populations, without necessarily involving adaptation per se. Here, we ask whether the repeated observation of host-associated genetic races across the worldwide distribution of the seabird ectoparasite Ixodes uriae is associated with host adaptation. We conducted a field-based experiment to test for adaptive specialisation in host races of I. uriae. We transferred unengorged ticks of two life stages (nymphs and adults) originating from three host species (black-legged kittiwake, common guillemot and Atlantic puffin) onto young kittiwake nestlings and followed attraction and attachment rates, engorgement times and feeding success of the transplanted ticks. All ticks were also typed genetically to match exploitation patterns with genetic differences among races. Ticks from atypical hosts were significantly less attracted to nestlings than ticks from the typical host, and showed lower feeding success and higher mortality. The degree of host specificity matched patterns of neutral genetic variation among races, with puffin ticks being more specific than guillemot ticks. Differences in specificity were also apparent among tick life stages, suggesting that nymphal ticks may be less discriminating of host type than adult ticks. Our results indicate that the genetic divergence previously observed among sympatric I. uriae host races is at least partially linked to adaptive specialisation to the host species and not simply to host-mediated transmission. They also suggest that the adaptation process may evolve differently in different life stages based on trade-offs with physiological constraints. The identification of the selective forces acting in host specialization will now be necessary to better characterize these patterns and to understand how transmission interacts with the adaptation process to generate parasite biodiversity.