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The recognition of and differential responses to salient stimuli are among the main drivers of behavioral plasticity, yet, how animals evolve and modulate functional responses to novel classes of antagonistic stimuli remain poorly understood. We studied free-living male red-winged blackbirds (Agelaius phoeniceus) to test whether gene expression responses in blood are distinct or shared between patterns of aggressive behavioral responses directed at simulated conspecific versus heterospecific intruders. In this species, males defend territories against conspecific males and respond aggressively to female brown-headed cowbirds (Molothrus ater), a brood parasite that commonly lays eggs in blackbird nests. Both conspecific songs and parasitic calls elicited aggressive responses from focal subjects and caused a downregulation in genes associated with immune system response, relative to control calls of a second, harmless heterospecific species. In turn, only the conspecific song treatment elicited an increase in singing behavior and an upregulation of genes associated with metabolic processes relative to the two heterospecific calls. Our results suggest that aspects of antagonistic behaviors to both conspecifics and brood parasites can be mediated by similar physiological responses, suggestive of shared molecular and behavioral pathways involved in the recognition and reaction to both evolutionarily old and new enemies.

How does a naive, young animal decide from which adults to learn behavior? Obligate brood parasitic birds, including brown-headed cowbirds (Molothrus ater), face a particular challenge in learning species-specific behaviors; they lay their eggs in the nest of another species, and juveniles are raised without exposure to adult conspecifics. Nevertheless, male cowbirds need to learn a conspecific song to attract appropriate mates, and female cowbirds need to learn to identify conspecific males for mating. Traditionally, it was thought that parasitic bird species rely purely on instinctual species recognition [1-4], but an alternative is that a species-specific trait serves as a "password" [5], a non-learned cue for naive animals that guides decisions regarding from whom to learn. Here, we tested the hypothesis that the adult "chatter call" enhances the learning of specific songs in juvenile cowbirds. We exposed acoustically naive juvenile male and female cowbirds to songs paired with chatter calls and found that the chatter call enhanced song production learning in males and induced a neurogenomic profile of song familiarity in females, even for heterospecific songs. Thus, a combination of experience-independent and -dependent mechanisms converges to explain how young cowbirds emerge from another species' nest yet learn behaviors from conspecifics. Identifying whether such password-based mechanisms relate to perceptual and behavioral learning in non-parasitic taxa will contribute to our general understanding of the development of social recognition systems., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

Amongst an array of stimuli from countless species, animals must recognize salient signals, including those of their own species. In songbirds, behavioral tests have demonstrated that preferences for conspecific male songs are determined by both preexisting biases and social experience with a male 'tutor' during the sensitive period for learning. Although immediate early gene expression (e.g. ZENK) and electrophysiological experiments generally find greater neural responses for conspecific songs, it remains unclear whether distinct mechanisms, such as sensory gating, are engaged to filter out irrelevant heterospecific songs. Here we compare the transcriptomic profiles, via RNA-seq, of non-singing females of a songbird, the zebra finch (Taeniopygia guttata), by focusing on the auditory forebrain, a region known to be critical in the processing of conspecific vs. heterospecific songs. Gene expression profiles demonstrate that different neural mechanisms are involved in the processing of conspecific versus heterospecific Bengalese finch (Lonchura striata) songs. In particular, one gene known to mediate sensory gating, the alpha 3 subunit member of nicotinic cholinergic receptors (CHRNA3), was significantly downregulated in response to hearing Bengalese finch song, but not when young females were tutored by a Bengalese male during early development. Overall, our results confirm previous behavioral and physiological studies, such that heterospecific-tutored individuals processed both conspecific and tutor songs similarly. Using transcriptomic profiling of peripheral blood samples, we also demonstrate the methodological potential of non-terminal sampling to identify transcriptomic biomarkers for conspecific auditory recognition. These results show how experience and inherited preferences facilitate the neural processing of salient songs by female songbirds., (Copyright © 2018 Elsevier B.V. All rights reserved.)