1. For iteroparous organisms life-history theory predicts a trade-off between current and future reproduction, and therefore the evolution of host responses to current parasite infestation that will maximize lifetime reproductive success. The parasite-induced variation in reproductive success is thus not the net result of parasite infestation alone, but the parasite-mediated outcome of optimal resource allocation among current and future reproductive events. Understanding the importance of parasites for the evolution of host life history therefore requires an experimental investigation of the effects of parasites over the host's life span. Such studies are currently scant.
2. We manipulated the load of an ectoparasite, the hen flea (Ceratophyllus gallinae), in the nests of its most common host, the great tit (Parus major), over a period of 4 years and recorded, the components of current and future reproductive success including survival, divorce, breeding dispersal and various reproductive parameters. Finally we assessed, for females only as paternity of males was unknown, the lifetime reproductive success as a close correlate of Darwinian fitness.
3. For current reproduction, our experiment demonstrates that parasites reduce current reproductive success via an increase in the probability of nest failure during incubation and the nestling period. In the presence of fleas, clutch size and the number of fledglings were reduced while the incubation and the nestling period were prolonged. Thus parasitism led to an increase in parental effort but nevertheless reduced current reproductive success.
4. For future reproduction, the experiment shows that females breeding in infested nests dispersed over longer distances between breeding attempts. The divorce rate following infestation, the probability of breeding locally in the future and residual reproductive success were not affected significantly by ectoparasites. The study thus suggests that hen fleas play a minor role in shaping the trade-off between current and future reproduction.
5. Lifetime reproductive success of females, measured as the total number of locally recruiting offspring over the 4 experimental years, was reduced significantly by ectoparasites. The negative effect of parasites arose by a reduction of the number of fledglings per breeding attempt rather than by a reduction of the number of breeding attempts.