Long‐term life‐history consequences of ectoparasite‐modulated growth and development

Many parasites affect the development and survival of offspring. Because passerines exhibit determinate growth, parasites may have lasting effects on phenotypes. The life‐history consequences of parasite‐induced developmental modifications have rarely been analyzed, and require long‐term experimental studies. Here we present the results of a four‐year experimental study on the effects of a hematophagous ectoparasite, the hen flea (Ceratophyllus gallinae), on growth, survival, and lifetime reproductive success of nestlings of the Great Tit (Parus major). In a design A, half of the nests were heat‐treated several times per year to kill parasites, while in the other half, fleas were allowed to immigrate naturally over several years. To allow for the estimation and statistical control of effects due to potentially nonrandom phenotype distribution within this design, a second design, design B, was applied. In design B, all nests were heat treated to kill parasites after nest box occupation, and the subsequent infestation of half of the nests was then randomized in space and time. In both designs, the fleas significantly reduced nestling body size but did not significantly affect the probability of nestling recruitment as local breeders. Parasitism reduced the clutch size of the nestlings' first recorded clutch, and of the subsequent clutches, and reduced the total number of recruits produced per nestling over the entire study period. Because body size of the recruited nestlings, both at the end of growth and as recruits, was not significantly different between treatments, the reduced fitness was not an indirect consequence of parasite‐modified body size. This study provides experimental evidence for parasite‐induced effects during growth on survival and development of offspring and shows the consequences of this phenotypic modification on lifetime reproductive success. It shows that parasite‐induced effects during growth are important for understanding optimal resource allocation and life‐history evolution under parasitism.