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Avian brood parasitism reduces the success of parasitized broods, yet most hosts of brown-headed cowbirds, Molothrus ater, neither desert parasitized clutches nor eject parasite eggs. We investigated whether spatial and temporal patterns of repeated cowbird parasitism on individuals influence the benefits of desertion or ejection in prothonotary warblers, Protonotaria citrea, and red-winged blackbirds, Agelaius phoeniceus. First, we demonstrated spatiotemporal correlation of parasitism across subsequent years of breeding for individual females of both host species. Repeated parasitism of individual warblers occurred because females used the same nestboxes repeatedly, but parasitism was not related to cowbird preference for particular host females’ phenotypes in either species. Second, we found that nest desertion by warblers was disfavoured because parasitism of sequential nesting attempts within a breeding season was significantly correlated for replacement clutches but not for second broods. In blackbirds, nest desertion was also not favoured because the likelihood of parasitism remained constant between first and replacement clutches of the same year. We then examined the relative fitnesses of two different cognitive pathways in the development of parasite rejection mechanisms based on a theoretical model for the benefits of egg ejection. Our models showed that the benefit of ejecting cowbird eggs based on learning to recognize the hosts’ own eggs would be consistently reduced with repeated parasitism. In contrast, the benefits of an experience-independent egg-ejection mechanism would remain constant in the face of structured cowbird parasitism. Limited horizontal transmission of brood parasitism may affect host-parasite coevolution both by diminishing the fitness benefits of host resistance to costly parasitism and by shaping the ontogeny of hosts’ recognition systems in response to repeated parasitism. (c) 2006 The Association for the Study of Animal Behaviour Published by Elsevier Ltd. All rights reserved.