Learned use of an innate sound-meaning association in birds

Abstract

Signals in vocal communication systems range from innate to learned. Although innate and learned signals are often assumed to be independent, Darwin speculated that they could be evolutionarily related, with the former being the foundation of the latter even in our own communication system, language. Here we test this hypothesis by studying the vocal communication systems of avian hosts of brood parasites. First, we show that 21 bird species separated by approximately 53 million years of evolution produce structurally similar 'whining' vocalizations towards their respective brood parasites. Exploring the social correlates of whining vocalization production, we find that species that produce this vocalization often exist in areas with dense parasite-host networks, suggesting that its production facilitates interactions among host species. Experiments across three continents show that this vocalization is referential towards brood parasites in multiple host species, that hearing them elicits an innate rapid recruiting response, and that host species from different continents respond equally to the whining vocalizations of each other, indicating that convergent use facilitates cooperative defences across species. Our results provide an example of a referential animal vocalization for which sound production in the correct context is learned but for which hearing it elicits an innate response, representing an intermediate between innate and learned signals.