Morphological diversity of acoustic and electric communication systems of mochokid catfish

Abstract

Mochokid catfish offer a distinct opportunity to study a communication system transitioning to a new signaling channel because some produce sounds and others electric discharges. Both signals are generated using an elastic spring system (ESS), which includes a protractor muscle innervated by motoneurons within the protractor nucleus that also has a motoneuron afferent population. Synodontis grandiops and S. nigriventris produce sounds and electric discharges, respectively, and their ESSs show several morphological and physiological differences. The extent to which these differences explain different signal types remains unclear. Here, we compare ESS morphologies and behavioral phenotypes among five mochokids. S. grandiops and S. nigriventris were compared with Synodontis eupterus that is known to produce both signal types, and representative members of two sister genera, Microsynodontis cf. batesii and Mochokiella paynei, for which no data were available. We provide support for the hypothesis that peripheral and central components of the ESS are conserved among mochokids. We also show that the two nonsynodontids are only sonic, consistent with sound production being an ancestral character for mochokids. Even though the three sound producing-only species differ in some ESS characters, several are similar and likely associated with only sound production. We propose that the ability of S. eupterus to generate both electric discharges and sounds may depend on a protractor muscle intermediate in morphology between sound producing-only and electric discharge-only species, and two separate populations of protractor motoneurons. Our results further suggest that an electrogenic ESS in synodontids is an exaptation of a sound producing ESS.

Vocal and Electric Fish: Revisiting a Comparison of Two Teleost Models in the Neuroethology of Social Behavior

“…Scale bar is 50 ms for top four species shown and 500 ms for S. nigriventris . Modified and adapted from Kéver et al (2020) and Kéver et al (2021) .…”

“…Electrogenic catfish have smaller Müllerian rami compared to their vocal relatives ( Kéver et al, 2021 ) and marked differences in the ultrastructure of the protractor muscle. In sound-producing species, this muscle has many myofibrils organized into highly ordered sarcomeres like other skeletal muscles, while in ED producing species, the muscle is largely missing this pattern of contractile elements ( Boyle et al, 2014 ), with myocytes that resemble the independently evolved myogenic electrocytes of gymnotiform and mormyrids.…”

“…The protractor muscle is innervated by the hindbrain motor nucleus, which receives input from several premotor neural populations ( Hagedorn et al, 1990 ; Ladich and Bass, 1996 ; Kéver et al, 2020 , 2021 ). The overall organization of this circuit is similar to the comparable circuit in toadfishes (see section “Neural Circuitry Generating Vocal and Electric Signals” above): a medially fused nucleus with large motoneurons and surrounding premotoneurons.…”

“…However, some, such as Synodontis eupterus , can produce both vocal and electric signals in different phases of social behavior. In S. eupterus , the ESS phenotype (e.g., the density of myofibrils in the protractor muscle and the length of the Mullerian ramus) is intermediate between vocal-only or electric-only species ( Hagedorn et al, 1990 ; Boyle et al, 2014 ; Kéver et al, 2021 ). In addition, the neural circuit that controls the ESS, has a larger pool of motoneurons compared to the homologous circuit in closely related species that produce only sonic or only electric signals.…”

“…The available phylogenetic evidence suggests that vocal signaling is the ancestral condition among mochokid catfishes ( Kéver et al, 2021 ). However, many of the investigated species in the genus Synodontis appear to have transitioned partly or entirely to electric signaling (see above).…”