They say it takes a village to raise a child. But if you are a cowbird, left by your parents to be hatched and raised in the nest of unwitting foster parents, how do you know who your village is? If the signature behaviors of your bird identity are not instinctive, how do you know who to learn them from?

Cowbirds, like cuckoos and a few others, stealthily lay their eggs in the nests of other birds and leave their young to be raised by parents of another species. Mark Hauber (GNDP), Harley Jones Van Cleave Professor of Host-Parasite Interactions in the Department of Evolution, Ecology and Behavior at the University of Illinois in Urbana-Champaign, has studied these brood parasitic birds throughout his career. In a report available online this week in Current Biology, he and his coauthors shared the culmination of a decades-long effort to work out how cowbirds learn the courtship song that enables males to attract mates, and females to recognize them.

“I did my PhD on this question . . . how [cowbirds] recognize their own species when they have never seen their own species, which is of course what brood parasites do in general,” said Hauber, who is also a member of the Carl R. Woese Institute for Genomic Biology at Illinois, said.  “We wanted to finalize the research and ask the question, but does the password actually change the way you learn?”

The cowbird’s password, as Hauber and other songbird researchers refer to it, is a sound called the chatter call that to the human ear might sound a little bit like a monkey’s chattering or a fast-forwarded version of a rodent’s squeaks. To a young cowbird, Hauber and others believe it is an avian shibboleth; a sound that reaches into their brain and whispers, hey friend! This is the cowbird song. It’s your song too, so pay attention.

Hauber wanted to confirm that this hypothesized message yields tangible results—do cowbirds actually learn better after hearing the chatter call? To answer this question, Hauber worked with then-postdoctoral researcher Matthew Louder and lab manager Amber Louder, former IGB Fellows Sarah London and Christopher Balakrishnan, and East Carolina University graduate student Robert Driver.

The team of researchers hand-raised young male cowbirds, playing the juveniles pre-recorded calls: either a canary song paired with a cowbird chatter call, or the same canary song paired with a mourning dove coo.

“It could be that just coupling the canary song with any noise will trigger learning,” Hauber said. “Using the canary songs and then coupling it to the dove coo made a really nice negative control;” in other words, if any call paired with a song could trigger learning, the cowbirds would not perform the canary song any better when it was paired with their own species’ chatter.

Instead, Hauber and his colleagues found the opposite. Although the cowbirds never became fluent in the canary song—the team speculated that their differing anatomy or the lack of other social cues made it difficult for them to learn—it was immediately apparent that male birds who heard the chatter learned to produce a more canary-like song.

“I could listen to these songs, and I could tell that this was a chatter call tutor canary song because it was simpler; it had more structure, this sound always follows that sound,” Hauber said. “I could hear it from my own ears that it was going to work . . . it's one of those exciting moments when you're doing the stats but your ear is already telling you something.”

Hauber’s ear for birdsong told him the truth. Compared with the songs of the coo-trained birds, the songs of the chatter-trained bird were significantly more structured and more similar to the genuine canary song.

Assessing whether female cowbirds who heard the different call combinations had different learning experiences was more difficult, in part because the young females were not sexually mature enough to express song and mate preferences. Instead, the researchers repeatedly serenaded the juvenile females with one canary’s song paired with a chatter, and another canary’s song paired with a dove coo. They then played each female one of the two canary songs and analyzed subsequent gene activity in regions of the brain involved in song recognition. They also analyzed gene activity in response to canary song in the brains of chatter- and coo-trained males.

“We knew about a set of genes in the zebra finches that had to do with familiarity recognition and so we looked for those,” Hauber said; in addition, he said, the team performed more open-ended search for groups of genes with related functions that might be involved in each bird’s response to hearing a particular song. “That yielded these neuroplasticity and neurofamiliarity types of genes for the male and the females, respectively.”

In the brains of the males that had previously heard a canary song paired with a cowbird chatter, the canary song was noteworthy; the genes that responded when the male heard it again were related to altering and strengthening connections between brain cells, supporting continued learning of the song. In females, who use songs to recognize and distinguish mates, gene activity data suggested that the canary song previously paired with a chatter was more familiar, while that paired with the coo was more startlingly novel, as though no memory of hearing it before had been retained.

Hauber is excited to have rounded out a scientific answer to an intriguing question of cowbird natural history, but also to see how this knowledge could be leveraged to better understand the biology of many other species.

“To show that the chatter call impacts learning was never done and now we have done it,” he said. “Cowbirds are great because it's this system where instinct and learning and constraints come together . . . we need to seek out the contexts in which these early guided learning mechanisms should be important.”

Christopher Balakrishnan is now an Associate Professor of Biology at East Carolina University. Sarah London is an Associate Professor of Psychology at the University of Chicago. Matthew Louder is now a postdoctoral researcher at the University of Tokyo. This work was supported by the National Science Foundation.