Sonic Motor Pathways in Piranhas with a Reassessment of Phylogenetic Patterns of Sonic Mechanisms among Teleosts

Abstract

Sound production has evolved independently a number of times among teleost fishes. In most cases, sound is generated by fast contracting muscles that vibrate the swim bladder by way of their direct attachment (intrinsic muscles) or indirectly by way of other skeletal elements (extrinsic muscles). This study focuses on the red and black piranha, Pygocentrus nattereri and Serrasalmus rhombeus (superorder Ostariophysi, Order Characiformes), that have extrinsic swim bladder sonic muscles innervated by the third and fourth spinal nerves. This innervation pattern diverges from that found in most teleosts, including the closely related catfishes (Ostariophysi, Siluriformes), where sonic muscles are innervated by ventral occipital nerve roots that arise just caudal to the vagus nerve. Here, we tested the hypothesis that piranhas would also differ from most other teleosts in the location of their sonic motor neurons. Following biotin labeling of branches of the third and fourth spinal nerves that innervate the sonic muscles in the red and black piranha, sonic motor neurons were identified amongst other non-sonic motor neurons in the central part of the spinal cord, slightly ventrolateral to the central canal. To our knowledge, this is the first example of sonic motor neurons positioned entirely within the spinal cord. In the other species so far studied, sonic motor neurons form well-defined nuclei that extend from far caudal levels of the medulla into the rostral spinal cord and are located either within the ventral motor column or near the midline, close to or just ventrolateral to the fourth ventricle and central canal. A piranha-like pattern may be more widespread among characiforms and is likely present in other teleost orders, e.g., Sciaenidae (drumfishes), that also have sonic muscles innervated by spinal nerves.