Host condition and host immunity affect parasite fitness in a bird–ectoparasite system

Summary Parasites might preferentially feed on hosts in good nutritional condition as such hosts provide better resources for the parasites’ own growth, survival and reproduction. However, hosts in prime condition are also better able to develop costly immunological or physiological defence mechanisms, which in turn reduce the parasites’ reproductive success. The interplay between host condition, host defence and parasite fitness will thus play an important part in the dynamics of host–parasite systems. In a 2 × 2 design, we manipulated both the access to food in great tit Parus major broods and the exposure of the nestlings to hen fleas Ceratophyllus gallinae , a common ectoparasite of hole‐breeding birds. We subsequently investigated the role of manipulated host condition, host immunocompetence, and experimentally induced host defence in nestlings on the reproductive success of individual hen flea females. The food supplementation of the nestlings significantly influenced the parasites’ reproductive success. Female fleas laid significantly more eggs when feeding on food‐supplemented hosts. Previous parasite exposure of the birds affected the reproductive success of fleas. However, the impact of this induced host response on flea reproduction depended on the birds’ natural level of immunocompetence, assessed by the phytohaemagglutinin (PHA) skin test. Flea fecundity significantly decreased with increasing PHA response of the nestlings in previously parasite‐exposed broods. No relationship between flea fitness and host immunocompetence was, however, found in previously unexposed broods. The PHA response thus correlates with the nestlings’ ability to mount immunological or physiological defence mechanisms against hen fleas. No significant interaction effect between early flea exposure and food supplementation on the parasites’ reproductive success was found. Our study shows that the reproductive success of hen fleas is linked to the hosts’ food supply early in life and their ability to mount induced immunological or physiological defence mechanisms. These interactions between host quality and parasite fitness are likely to influence host preference, host choice and parasite virulence and thus the evolutionary dynamics in host–parasite systems.