A comparative developmental study of the avian syrinx: Insights into the homology of the sound-producing muscles in birds

The anatomical innovation of sound-producing organs, which gives rise to a wide variety of sound signals, is one of the most fundamental factors leading to the explosive speciation of modern birds. Despite being a key clue to resolving the homology of sound-controlling muscles among birds, only few studies have explored the embryonic development of syringeal muscles. Using serial histological sections and immunohistochemistry, we described the three-dimensional anatomy and development of the cartilage, muscle, and innervation pattern of the tracheobronchi in three avian species: domestic fowls, cockatiels, and zebra finches. Crucially, the muscle primordia of the syringeal and tracheobronchial muscles develop from the caudal end of the lateral tracheal muscle in cockatiels and zebra finches. Furthermore, the tracheobronchial and syringeal muscle primordia of the zebra finches are subsequently split during embryonic development. Based on our findings on the identity of muscle primordia development and innervation pattern of the hypoglossal nerve between the cockatiels and zebra finches, we suggest that the muscle component traditionally documented as the superficial syringeal muscle in parrots is homologous to the tracheobronchial and ventral syringeal muscles of the zebra finches. These facts not only orchestrate the terminological discrepancies among previous studies, but also suggest that the syringeal muscles were acquired by the anatomical innovation of the lateral tracheal muscles in the common ancestor of the parrots and passerines, and further compartmentalized in the passerines, perhaps leading to a wide song repertoire for acoustic communication.