Heritable variation in host quality as measured through an ectoparasite's performance

Abstract

Obligate parasites need one or more hosts to complete their life cycle. However, hosts might show intraspecific variation in quality with respect to the parasites themselves, thus affecting on-host and off-host parasite performance. High heritability in host quality for the parasite may therefore exert long-lasting selective pressures on the parasite and influence host-parasite coevolution. However, the amount of variation and heritability in host quality are unknown for most parasite species, especially in wild populations of hosts. Both measures were estimated in a wild-caught bird Parus major that was experimentally infested by two developmental stages (larva and nymph) of a ectoparasite (the tick Ixodes arboricola). We examined variation in host quality through variation in tick performance, namely the on-host performance (attachment success, feeding time, engorgement weight and feeding success) and the off-host performance (moulting time, moulting success and overall survival). Herein we also investigated the influence on tick performance of host traits linked with the bird's life history and physiology such as body condition, sex, age and haematocrit. By correlating tick performance variables between larvae and nymphs feeding on the same bird at different times, we found a significant correlation in attachment success, suggesting consistent among-host variation for this performance measure, but no significant larva-nymph correlations for the other tick variables. Animal models relating tick performance variables to the host pedigree showed a strong heritable signal for host quality as measured through tick feeding time, and lower but substantial estimates in other performance variables. With regard to the host traits, feeding success and survival of tick larvae were lower on female birds, and nymphal survival was higher on older birds. Larval feeding time was negatively correlated with host haematocrit. This is one of the first studies showing consistent intraspecific variation and heritability of host quality for a multi-stage ectoparasite.