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Parasites can have dramatic effects on life-history decisions of hosts such as timing of reproduction, clutch size, and investment in individual offspring, depending on the timing of parasite effects on host fitness. Moreover, parasites may influence the optimum values of important life-history traits such as clutch size and brood size by having different fitness effects for large and for small values. Here, by analyzing data from a Magpie (Pica pica) population sympatric with the Great Spotted Cuckoo (Clamator glandarius), we demonstrated that Magpies laying a large clutch suffer less from parasitism than do those laying a small clutch, because the first have a higher probability of successfully raising some of their own offspring. Therefore, we predicted that (1) Magpie hosts in sympatry with Great Spotted Cuckoos should produce more eggs, and (2) eggs should be smaller than those in areas of allopatry. We also predicted that (3) this change in life history should be directly related to selection pressures by cuckoos, as evidenced from current levels of parasitism and Magpie rejection of cuckoo model eggs. We tested these predictions by comparing the life-history parameters of 15 European host populations that are either sympatric or allopatric with the parasite. In accordance with predictions, we found an increase in clutch size and a decrease in egg volume of Magpies in populations sympatric with the Great Spotted Cuckoo, as compared to allopatric populations, even when statistically controlling for laying date and latitude. By using parasitism rate and experimentally testing the ability of Magpies to recognize and reject mimetic and nonmimetic model eggs, we were able to test prediction 3 in the 15 Magpie populations. Clutch size was positively related to the rejection rate of nonmimetic model eggs, whereas mean egg volume was significantly negatively related to the rejection rate of mimetic model eggs. These findings provide evidence of a strong influence of the parasitic Great Spotted Cuckoo on the life history of its Magpie host.