Abstract

The ability to imitate sounds depends on a process called vocal production learning, a rare evolutionary trait. In addition to the few mammalian groups that possess this ability, vocal production learning has evolved independently in three avian clades: songbirds, parrots, and hummingbirds. Although the anatomy and mechanisms of sound production in songbirds are well understood, little is known about the hummingbird’s vocal anatomy. We use high-resolution micro-computed tomography (μCT) and microdissection to reveal the three-dimensional structure of the syrinx, the vocal organ of the black jacobin (Florisuga fusca), a phylogenetically basal hummingbird species. We identify three features of the black jacobin’s syrinx: (i) a shift in the position of the syrinx to the outside of the thoracic cavity and the related loss of the sterno-tracheal muscle, (ii) complex intrinsic musculature, oriented dorso-ventrally, and (iii) ossicles embedded in the medial vibratory membranes. Black jacobin´s intrinsic musculature oriented dorso-ventrally appears being a hummingbird specific novelty, likely due to the extra-thoracic location of syrinx that uncouples syrinx movements from extensive flight-related thorax constraints. Their syrinx morphology allows vibratory decoupling, precise control of complex acoustic parameters, and a large motor redundancy that may be key biomechanical factors leading to acoustic complexity and thus facilitating the occurrence of vocal production learning.