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In many social animals, early exposure to conspecific stimuli is critical for the development of accurate species recognition. Obligate brood parasitic songbirds, however, forego parental care and young are raised by heterospecific hosts in the absence of conspecific stimuli. Having evolved from non-parasitic, parental ancestors, how brood parasites recognize their own species remains unclear. In parental songbirds (e.g. zebra finch Taeniopygia guttata), the primary and secondary auditory forebrain areas are known to be critical in the differential processing of conspecific vs. heterospecific songs. Here we demonstrate that the same auditory brain regions underlie song discrimination in adult brood parasitic pin-tailed whydahs (Vidua macroura), a close relative of the zebra finch lineage. Similar to zebra finches, whydahs showed stronger behavioral responses during conspecific vs. heterospecific song and tone pips as well as increased neural responses within the auditory forebrain, as measured by both functional magnetic resonance imaging (fMRI) and immediate early gene (IEG) expression. Given parallel behavioral and neuroanatomical patterns of song discrimination, our results suggest that the evolutionary transition to brood parasitism from parental songbirds likely involved an "evolutionary tinkering" of existing proximate mechanisms, rather than the wholesale reworking of the neural substrates of species recognition.

A host that has been targeted by an avian brood parasite can recover most of its potential fitness loss by ejecting the foreign egg(s) from its nest. The propensity for some hosts to engage in egg rejection behavior has put selective pressure on their parasites to evolve mimetic eggshells resembling the host’s own shell colors and maculation. In turn, hosts have counterevolved increasingly more sophisticated detection methods such as narrowing visual egg acceptance thresholds or using social cues to recognize parasitism. However, multiple cognitive mechanisms acting simultaneously could theoretically interfere with one another and ultimately decrease egg rejection accuracy, especially if these heuristics yield differing targets for rejection. By painting hosts own eggs, we studied a host species of the common cuckoo Cuculus canorus, the great reed warbler Acrocephalus arundinaceus, and tested its responses to the presence of “foreign” eggs of varying quantity, colors, and uniformity. Using reflectance spectra of egg background coloration and avian perceptual modeling, we then estimated the sensory thresholds triggering egg rejection by this host for each treatment. As previously reported, rejection rates were positively related to the perceptual distance between own and foreign eggs in the nests in all treatments. However, rejection thresholds were more permissive (error prone) both with greater proportions of foreign eggs per clutch and/or when the suite of foreign eggs was perceptually more variable within the nest. These results suggest that parasites, through multiple parasitism, can partially overcome the evolution of hosts’ recognition of mimetic parasite eggs.

Conspecific brood parasitism (CP) is a facultative breeding tactic whereby females lay their eggs in the nests of conspecifics. In some species, potential hosts have evolved the ability to identify and reject foreign eggs from their nest. Previous studies suggest that the ubiquitous house sparrow Passer domesticus in Spain and South Africa employs both CP and egg rejection, while a population in China does not. Given the species’ invasive range expansions, the house sparrow represents a potentially excellent global model system for parasitic egg rejection across variable ecological conditions. We examined the responses of house sparrows to experimental parasitism at three geographically distinct locations (in Israel, North America, and New Zealand) to provide a robust test of how general the findings of the previous studies are. In all three geographic regions egg rejection rates were negligible and not statistically different from background rates of disappearance of control eggs, suggesting that the house sparrow is not a suitable model species for egg rejection experiments on a global scale.

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