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Parasites may, in multi-parasite systems, block the defenses of their hosts and thus thwart host recognition of parasites by frequency-dependent selection. Nest defenses as frontline may block or promote the subsequent stage of defenses such as egg recognition. We conducted comparative studies of the defensive strategies of a host of the Oriental cuckoo Cuculus optatus, the yellow-bellied prinia Prinia flaviventris, in mainland China with multiple species of cuckoos and in Taiwan with a single cuckoo species. Cuckoo hosts did not exhibit aggression toward cuckoos in the presence of multiple cuckoo species but showed strong aggressive defenses of hosts directed toward cuckoos in Taiwan. Furthermore, the cuckoo host in populations with a single cuckoo species was able to distinguish adults of its brood parasite, the Oriental cuckoo, from adult common cuckoos (Cuculus canorus). This represents the first case in which a cuckoo host has been shown to specifically distinguish Oriental cuckoo, from other Cuculus species. Hosts ejected eggs at a higher rate in a single cuckoo species system than in a multi-species cuckoo system, which supports the strategy facilitation hypothesis. Granularity analysis of variation in egg phenotype based on avian vision modeling supported the egg signature hypothesis in hosts because Taiwanese prinias increased consistency in the appearance of their eggs within individual hosts thus favoring efficient discrimination against cuckoo eggs. This study significantly improves our knowledge of intraspecific variation in antiparasitism behavior of hosts between single- and multi-cuckoo systems.

Avian hosts of brood parasites can evolve anti‐parasitic defenses to recognize and reject foreign eggs from their nests. Theory predicts that higher inter‐clutch and lower intra‐clutch variation in egg appearance facilitates hosts to detect parasitic eggs as egg‐rejection mainly depends on the appearance of the egg. Therefore, we predict that egg patterns and rejection rates will differ when hosts face different intensity of cuckoo parasitism. We tested this prediction in two populations of the plain prinia Prinia inornata: Guangxi in mainland China with high diversity and density of cuckoo species, and Taiwan where there is only one breeding cuckoo species, the oriental cuckoo Cuculus optatus. As expected, egg patterns were similar within clutches but different among clutches (polymorphic eggs) in the mainland population, while the island population produced more uniform egg morphs. Furthermore, the mainland population showed a high rate of egg rejection, while the island population exhibited dramatically reduced egg grasp‐rejection ability in the absence of parasitism by the common cuckoo Cuculus canorus. Our study suggests that prinias show lower intra‐clutch consistency in egg colour and lose egg‐rejecting ability under relaxed selection pressure from brood parasitism.

Background: Obligate brood parasites exert strong selective pressure on target hosts. In response, hosts typically evolve anti-parasitism strategies, of which egg recognition is one of the most efficient. Generally, host egg-recognition capacity is determined using model eggs. Previous studies have shown that some host species, which are capable of detecting parasite eggs, do not reject model eggs. However, it is unknown that whether the reaction to model eggs varies among distinct populations of the same host in relation to the degree of parasitism pressure. Results: Here, we compared the rejection frequencies of model eggs and real eggs between mainland and island populations of the plain prinia (Prinia inornata), which are respectively sympatric and allopatric with their brood parasite, the common cuckoo (Cuculus canorus). Our results indicated that the mainland and island populations rejected real eggs at similar rates, but rejected model eggs, which were similar in size to real eggs but heavier, at significantly different rates: the island population rejected fewer model eggs, possibly because the rejection motivation of this population was lower due to absence of parasitism. Conclusions: Our results indicated that some factors affecting the decision to reject, such as rejection motivation, varied according to the degree of parasitism pressure, and thus influenced the frequency of egg rejection. Furthermore, our results suggested that model eggs should be used with caution in comparative studies of egg recognition abilities among species or populations subjected to different intensities of brood parasitism. That is, model eggs may fail to accurately detect egg recognition in host populations with little to no risk of parasitism.

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