Abstract
Some rodents produce ultrasonic vocalizations (USVs) for social communication using an aerodynamic whistle, a unique vocal production mechanism not found in other animals. The functional anatomy and evolution of this sound production mechanism remains unclear. Using laryngeal airway reconstruction, we identified anatomical specializations critical for USV production. A robust laryngeal cartilaginous framework supports a narrow supraglottal airway. An intralaryngeal airsac-like cavity termed the ventral pouch was present in three muroid rodents (suborder Myomorpha), but was absent in a heteromyid rodent (suborder Castorimorpha) that produces a limited vocal repertoire and no documented USVs. Small lesions to the ventral pouch in laboratory rats caused dramatic changes in USV production, supporting the hypothesis that an interaction between a glottal exit jet and the alar edge generates ultrasonic signals in rodents. The resulting undulating airflow around the alar edge interacts with the resonance of the ventral pouch, which may function as a Helmholtz resonator. The proposed edge-tone mechanism requires control of intrinsic laryngeal muscles and sets the foundation for acoustic variation and diversification among rodents. Our work highlights the importance of anatomical innovations in the evolution of animal sound production mechanisms.
Highlights
Rodents employ diverse vocal behaviour in a variety of social contexts [1,2,3,4,5,6]
Roberts [14,29,30] pioneered the investigation of the functional morphology of rodent laryngeal anatomy and its importance for ultrasonic vocalizations (USVs) production
Vocalizations used in social communication are among the most diverse and elaborate displays in the animal kingdom, yet our understanding of the physiological mechanisms driving acoustic divergence remains understudied [56]
Summary
Rodents employ diverse vocal behaviour in a variety of social contexts [1,2,3,4,5,6]. Rats and mice produce both audible and ultrasonic vocalizations (USVs) [7], with fundamental frequencies between 100 and 120 000 Hz. Ultrasonic whistling is the most notable behaviour and the only clear example of sound production by a whistle mechanism among vertebrates, besides human whistling [8]. Ultrasonic whistling is the most notable behaviour and the only clear example of sound production by a whistle mechanism among vertebrates, besides human whistling [8] Such a whistle mechanism has been suspected in birds, frogs, dolphins and non-human primates [9,10,11,12,13], it has been convincingly demonstrated using heliox experiments only in laboratory mice [14], rats [15] and grasshopper mice [16]. Understanding the evolution and physiological mechanisms of how aerodynamic energy is converted into sound remains controversial and often detached from anatomical detail
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