From neurobiology to ecology and back: The zebra finch song as model system for biological integration

Vocal communication is a defining trait of humans and widespread across the animal kingdom. Vocal learning and the cultural transmission of sounds are key features of human speech but of unresolved evolutionary origins. Songbirds, similar to humans, acquire their vocalizations during a sensitive phase early in life by learning from conspecifics. Therefore, since the 1950s, song learning in birds has become a key model in identifying mechanisms and functions of vocal learning. Of the songbirds, the zebra finch (Taeniopygia castanotis) is the best-characterized animal model for vocal learning and its behavioral implications. Neurobiological and behavioral studies in controlled laboratory settings have provided detailed insights into the acquisition, control and function of birdsong. For zebra finches and other songbirds, however, the social and ecological conditions during vocal development differ between laboratory and natural settings, limiting the wider contextualization and integration of knowledge across biological disciplines. Recent field studies have increasingly unraveled the complexity of the social organization of zebra finches along with the context in which birds learn and sing in the wild. Here, we review key insights on vocal learning in the lab and what is known about zebra finch social organization and singing in the wild to lay out a path on how to integrate many of these insights. We then highlight how both neurobiologists and field behavioral ecologists can benefit from the broader perspective. Behavioral neuroscientists may be able to implement more ecologically relevant settings in their research, while insights and hypotheses from controlled laboratory experiments can inform field behavioral studies for refining existing paradigms and to stimulate new approaches. We outline how such integration can lead to scientific innovations to understand how individuals navigate their social and acoustic environments, how they select and prioritize learning from diverse song models, and how brains integrate real-world experience to guide song learning. We hope that this specific example can inspire and inform others who move from a reductionist approach towards studying ecologically relevant behaviors in naturalistic contexts.