Shared transcriptional responses to con- and heterospecific behavioral antagonists in a wild songbird.

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.

An Acoustic Password Enhances Auditory Learning in Juvenile Brood Parasitic Cowbirds.

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.

When are egg-rejection cues perceived? A test using thermochromic eggs in an avian brood parasite host.

At the core of recognition systems research are questions regarding how and when fitness-relevant decisions made. Studying egg-rejection behavior by hosts to reduce the costs of avian brood parasitism has become a productive model to assess cognitive algorithms underlying fitness-relevant decisions. Most of these studies focus on how cues and contexts affect hosts' behavioral responses to foreign eggs; however, the timing of when the cues are perceived for egg-rejection decisions is less understood. Here, we focused the responses of American robins Turdus migratorius to model eggs painted with a thermochromic paint. This technique modified an egg's color with predictably varying temperatures across incubation: at the onset of incubation, the thermochromic model egg was cold and perceptually similar to a static blue model egg (mimicking the robin's own blue-green egg color), but by the end of an incubation bout, it was warm and similar to a static beige egg (mimicking the ground color of the egg of the robin's brood parasite, the brown-headed cowbird Molothrus ater). Thermochromic eggs were rejected at statistically intermediate rates between those of the static blue (mostly accepted) and static beige (mostly rejected) model eggs. This implies that at the population level, egg-rejection relevant cues are not perceived solely when arriving to or solely when departing from the nest. We also found that robins rejected their own eggs more often when exposed to color-changing model eggs relative to static eggs, suggesting that recognizing variable foreign eggs entails costly rejection errors for this host species.