True recognition of nestlings by hosts selects for mimetic cuckoo chicks

Cuckoos lay their eggs in other birds’ nests, whereafter the young cuckoo hatches, ejects its nestmates, and monopolizes the care of the host parents. Theory predicts that hosts should not evolve to recognize and reject cuckoo chicks because of the risk of mistakenly imprinting on a cuckoo chick in their first brood and thereafter always rejecting their own chicks. However, recent studies have revealed some hosts do reject cuckoo chicks from the nest, indicating that these hosts’ recognition systems either do not rely on first brood imprinting, or use cues that are independent of chick phenotype. Here, we investigate the proximate mechanisms of chick rejection behaviour in the large-billed gerygone (Gerygone magnirostris), a host of the little bronze-cuckoo (Chalcites minutillus). We find that gerygones use true template-based recognition based on at least one visual chick trait (the amount of hatchling down-feathers), and that this is further mediated by experience of adult cuckoos at the nest during egg-laying. Given the theoretical constraints of acquiring recognition templates via imprinting, gerygones must possess a template of own-chick appearance that is largely innate. This true recognition has facilitated the evolution of very rapid hatchling rejection and, in turn, striking visual mimicry of host young by little-bronze cuckoo chicks.