Optimal tuning not required: Birds communicate effectively with mismatched auditory filters.

Abstract

Birds have one of the most remarkable vocal capacities of vertebrates. Yet we know little about the relationship between their hearing and their vocal capacities at large phylogenetic scales, and whether these traits coevolve in a tight or loose fashion. Here we collected vocal and auditory data for 72 bird species from 15 different orders, and tested if hearing is finely tuned to the spectral composition of their vocalizations (i.e., the matched-filter hypothesis). We found bird audition not to be predictive of vocal frequency, and mismatches between hearing and vocalizations to be widespread. We show that the source of these mismatches is allometric: the auditory tuning and the spectral composition of vocalizations scale with body weight to different degrees. Despite the general frequency mismatches, bird hearing remains remarkably sensitive to the main spectral component of their vocalizations. Our results challenge the view that sensory systems must be finely tuned only to conspecific signals for communication to be effective. Our results suggest that selection for a broad auditory tuning has allowed birds to effectively communicate with conspecifics while at the same time permitting general environmental awareness using auditory cues. We argue that the relationship between hearing and vocalizations in birds is better described by the concept of diffuse coevolution, where organism evolve in relation to their broader ecological context instead than on a strictly dyadic fashion. Significance StatementAnimal communication theory often states that signalers and perceivers coevolve, yet the spread and nature of this relationship remains unclear. We tested whether the auditory tuning of birds is tightly matched to the frequency content of their vocalizations -an expected outcome of strong coevolution and the matched-filter hypothesis. We show that although birds hearing does not precisely align with their vocalizations, birds are still highly sensitive to the sounds they produce. This is due to the broad tuning of the avian auditory systems, which supports effective conspecific communication while also allowing the detection of other ecologically relevant sounds. Thus, birds exemplify diffuse rather than tightly coupled coevolution in communication systems.