Shared developmental and evolutionary origins for neural basis of vocal–acoustic and pectoral–gestural signaling

Abstract

Acoustic signaling behaviors are widespread among bony vertebrates, which include the majority of living fishes and tetrapods. Developmental studies in sound-producing fishes and tetrapods indicate that central pattern generating networks dedicated to vocalization originate from the same caudal hindbrain rhombomere (rh) 8-spinal compartment. Together, the evidence suggests that vocalization and its morphophysiological basis, including mechanisms of vocal-respiratory coupling that are widespread among tetrapods, are ancestral characters for bony vertebrates. Premotor-motor circuitry for pectoral appendages that function in locomotion and acoustic signaling develops in the same rh8-spinal compartment. Hence, vocal and pectoral phenotypes in fishes share both developmental origins and roles in acoustic communication. These findings lead to the proposal that the coupling of more highly derived vocal and pectoral mechanisms among tetrapods, including those adapted for nonvocal acoustic and gestural signaling, originated in fishes. Comparative studies further show that rh8 premotor populations have distinct neurophysiological properties coding for equally distinct behavioral attributes such as call duration. We conclude that neural network innovations in the spatiotemporal patterning of vocal and pectoral mechanisms of social communication, including forelimb gestural signaling, have their evolutionary origins in the caudal hindbrain of fishes.