Stereotyped configuration of trachea and paired bronchi is common to all amniotes, and cartilaginous rings are observed in both the bronchi and trachea ( 49). Tracheal cartilage morphologies (red) are highly irregular (i.e., not ring-shaped) in lissamphibians ( 29), and irregular, forked rings are also sometimes observed in mammals ( 88). Cricoid cartilage (light green) is absent in some lissamphibians.

Paired arytenoid cartilages (dark green) are present in most tetrapods ( 26). ( Upper, Left to Right) Schematic diagrams depict airway morphology in caecilians, frog, salamander, rat, gecko, tortoise, alligator, and a duck. Tetrapod phylogeny showing the sequence of the acquisition of different airway traits through evolutionary time. Alternatively, vocal folds could have remained viable in the larynx (perhaps with reduced or diminishing efficacy), but a syrinx evolved to supplement sound production, which was followed by loss of the larynx sound source.įig. Novel selective regimes unrelated to sound production could have led to the loss of sound production in the larynx, and subsequently a new vocal organ arose in a new position under selection for acoustic function. Given that the larynx is not involved in sound production in birds, there are two scenarios for syrinx evolution. However, sometime before the origin of crown birds, the vocal function of the larynx was lost, and a novel structure, the syrinx, was gained at the tracheobronchial juncture ( Figs. Outgroup reptiles also are capable of vocal communication using the same structures ( 6, 7). The extant sister taxon of birds, crocodilians, communicates with sounds produced via vocal folds in the larynx ( 5). A New Structure Without a New FunctionĪssessing novelty in a structure requires knowledge of potentially homologous structures present in an individual, in outgroups, or estimated in ancestral taxa ( 2– 4). We will go on to show how an integrated approach incorporating data and perspectives from developmental biology, vocal physiology, and paleontology defines a promising agenda for understanding the evolution of the syrinx. We will discuss the evolution of the avian syrinx at multiple levels of biological organization-developmental, structural, and functional-and consider on which of these levels, if any, the syrinx has homologs in nonavian taxa. Here, we focus on one critically understudied and undertheorized aspect of avian evolutionary novelty, the origin of the evolutionarily novel sound-producing organ of birds, the syrinx. Further, while avian vocalization has evolved through changes in both the neural control of vocalization and the vocal structures themselves, comparatively little attention has been paid to the latter. While analyses have traced the deep origins of the genes involved in feather development, and fossils have illuminated the evolutionary paths to branched feathers and to the origin of flight, little similar work has been undertaken to approach the complex novelty of bird vocal production. Several novel traits have played key roles in the evolution of birds, including, for example, feathers, flight, and song ( 1). The syrinx, along with other evolutionary novelties in sensory and signaling modalities, may more commonly involve structural changes that contribute to or modify an existing function rather than those that enable new functions. We find that the syrinx falls into an unusual category of novel structures: those having significant functional overlap with the structures they replace. Further, unlike all other vertebrate vocal organs, the syrinx is not derived from a known valve precursor, and its origin involves a transition from an evolutionary “spandrel” in the respiratory tract, the site where the trachea meets the bronchi, to a target for novel selective regimes. In contrast with laryngeal cartilages that support vocal folds in other vertebrates, we find no evidence that individual cartilage rings anchoring vocal folds in the syrinx have homology with any specific elements in outgroups. Here, we review the identity of structures in the avian vocal organ, the syrinx, and bring together developmental data on airway patterning, structural data from across tetrapods, and mathematical modeling to assess what is novel. However, when many previously proposed evolutionary novelties have been illuminated by genetic, developmental, and fossil data, they have refined and narrowed our concept of biological “newness.” For example, they show that these novelties can occur at one or multiple levels of biological organization. In its most basic conception, a novelty is simply something new.

Syrinx musition