Vertebrate Vocalizations

W e communicate through speech and language but also with our laughs and cries. Speech and language are learned behaviors that are intimately tied to human cognition. But the more basic pattern is that the structure of vocalization is innately specified; as any parent knows, babies require no practice to cry at birth. Species-specific “calls” are observed in diverse vertebrates and in numerous social contexts, but with a spotty distribution. Many amphibians, as well as some reptiles and fishes, are highly vocal animals. Most birds and mammals call. Did the neural structures for calling among this very broad group of animals arise from a single common ancestor? On page 417 in this issue, Bass et al. (1) address this question by examining the organization of neural networks underlying vocalization in fish. Vertebrates make sounds with an astounding variety of mechanisms, but use only some of these to produce most communication sounds. In terrestrial vertebrates, vocalizations are commonly produced by specialized organs that vibrate air as it moves from the lungs through respiratory tubes. Fishes do not have the vibration-producing structures of terrestrial vertebrates—the larynx in amphibians, reptiles, and mammals or the syrinx in birds—nor do they have an air-filled tube leading to the mouth. Instead, some fishes vocalize with the swim bladder, an air sac used mainly for buoyancy control and as an accessory respiratory organ. The swim bladder is vibrated by associated muscles and acts as a resonance chamber to amplify the sound. The social contexts of vocalizations are as diverse as their mechanics. Calls are used to communicate across as well as within species, and can be directed at individuals or groups. They are produced in numerous contexts such as aggression, fear, mating, and parent-offspring interactions, signaling intent or surprise (2). Given this substantial diversity in the mechanisms of vocal production and function, one might be tempted to assume that vocal systems arose multiple times across the vertebrates during evolution. An alternative hypothesis, given the existence of vocalizing animals in both of the major clades of Osteichthyes (bony fishes)—the Actinopterygii (ray-finned fishes) and Sarcopterygii (lobefinned fishes and terrestrial vertebrates)—is that a common origin for vertebrate vocalizations evolved before the divergence of these groups, more than 400 million years ago (3). To determine the relationships among vertebrate vocal systems, Bass et al. examined the spatial organization of neurons in the hindbrain vocalization neural network of three species of batracoid fish—the Gulf toadfish (Opsanus beta), the oyster toadfish (Opsanus tau) (see the figure), and the midshipman fish (Porichthys notatus)—and compared them to those of other vertebrates. These fishes are notable for their dramatic calling, used for attracting mates and for territorial defense. The swim bladder muscle used for these vocalizations is one the fastest known vertebrate muscles, contracting at up to 200 Hz (4). Such specializations make these species compelling models to study vocalizations in actinopterygian fishes. Bass et al. found that the vocal motor neurons of the toadfish are localized to a region that spans the rostral spinal cord and rhombomere 8, which is the caudal-most segment of the hindbrain. The authors also describe the position of several upstream neuronal elements of the vocalization circuit, including the vocal pacemaker neurons that control rhythmicity. These cells are also located in rhombomere 8, with the pacemaker neurons extending into rostral spinal cord, lateral to the vocal motor neurons. The positions of the vocal motor neurons and other neurons in this circuit are consistent with the organization of the vocal system in frogs, birds, and mammals, supporting the hypothesis that the neural basis of vocal circuits arose before the divergence of sarcopterygian and actinopterygian branches of the vertebrate phylogeny. Encompassing fishes, amphibians, reptiles, birds, and mammals, this is another remarkable example of a conserved vertebrate body plan (5). A single origin for aspects of the neural control of vocalizations leads to other questions about the system, including how much deeper into the history of vertebrates this circuit goes, and how it originated. Addressing such questions is limited by the small number of extant vertebrate outgroups to the bony fishes including Chondrichthyes (sharks, skates, rays, and chimeras) and Agnathans (hagfishes and lampreys), neither of which have air-filled spaces analogous to swim bladders or lungs, nor are known to produce sounds in ways similar to those of lung and swim bladder-based mechanisms. An additional complication is that there is no consistent relation between the vocal motor neurons and the cranial nerve through which they project to muscle. Batracoids and other actinopterygian fishes’ motoneurons project through the occipital nerve, whereas birds use the hypoglossal nerve and amphibians and mammals, the vagal nerve (1). With current data, the primitive condition of the vocal nerve for Osteichthyes remains unresolved. A complementary approach to examining gross morphology may be to look for molecular markers to help identify homologous circuit elements across diverse taxa. If vertebrates share a common hindbrain and spinal cord organization for vocalizations, does this also shed light on the evolution of vocal learning? The distribution of learned vocalizations across vertebrates indicates that this behavior has evolved multiple times. Among primates, only humans show compelling evidence of vocal learning. Among mammals, there is increasing evidence for vocal learning, but to date, only in two additional lineages, bats Did the mechanisms underlying vertebrate vocal abilities evolve from a single common ancestor? Vertebrate Vocalizations