Neuroanatomical and neurophysiological mechanisms of acoustic and weakly electric signaling in synodontid catfish

Abstract

To what extent do modifications in the nervous system and peripheral effectors contribute to novel behaviors? Using a combination of morphometric analysis, neuroanatomical tract‐tracing, and intracellular neuronal recording, we address this question in a sound‐producing and a weakly electric species of synodontid catfish, Synodontis grandiops , and Synodontis nigriventris , respectively. The same peripheral mechanism, a bilateral pair of protractor muscles associated with vertebral processes (elastic spring mechanism), is involved in both signaling systems. Although there were dramatic species differences in several morphometric measures, electromyograms provided strong evidence that simultaneous activation of paired protractor muscles accounts for an individual sound and electric discharge pulse. While the general architecture of the neural network and the intrinsic properties of the motoneuron population driving each target was largely similar, differences could contribute to species‐specific patterns in electromyograms and the associated pulse repetition rate of sounds and electric discharges. Together, the results suggest that adaptive changes in both peripheral and central characters underlie the transition from an ancestral sound to a derived electric discharge producing system, and thus the evolution of a novel communication channel among synodontid catfish. Similarities with characters in other sonic and weakly electric teleost fish provide a striking example of convergent evolution in functional adaptations underlying the evolution of the two signaling systems among distantly related taxa.

Morphological diversity of acoustic and electric communication systems of mochokid catfish

“…batesii and Mo. paynei was under the nuchal shield and not under the dorsal fin as reported for other synodontids investigated so far (Fine & Ladich, 2003;Hagedorn et al, 1990;Kéver et al, 2020;Ladich & Bass, 1996). In addition, the PM of Mi.…”

“…Boyle et al (2014) demonstrated the electric signals of S. nigriventris and S. eupterus (designated S. euptera by these authors), and the sounds of S. eupterus and S. grandiops. Following the same protocol, Kéver et al (2020) presented and analyzed additional recordings of S. nigriventris and S. grandiops. In the present study, the signaling behavior of nine Mo.…”

“…The ESS also includes a hindbrain motor circuit that drives the PM to generate a weakly electric and/or sonic signal. We recently showed morphological differences in the ESS between two synodontids, S. grandiops that is only a sound producer and S. nigriventris that only produces weakly electric discharges (Kéver, Bass, Parmentier, & Chagnaud, 2020) ( Figure 2a,b). For example, the ESA of S. grandiops has a larger plate but shorter stem of the MR, and a larger PM, whereas the PM of S.…”

“…Central differences include neurophysiological properties of protractor motoneurons and species-specific differences such as the number and dendritic arborization of protractor motoneurons. Even though some neurophysiological properties help to explain species differences in temporal properties (pulse repetition rate) of signals, it remains difficult to assign either these differences or morphological ones more broadly among synodontids or mochokids to production of either sounds or electric discharges based on a comparison of only two species (Kéver et al, 2020).…”

Evolution and Ecology in Widespread Acoustic Signaling Behavior Across Fishes

“…A particularly fascinating case of secondary loss concerns catfishes in the genus Synodontis ; some species are only soniferous and others only weakly electric (Boyle et al 2014). Weakly electric Synodontis have reduced sonic muscle characters, but share characters with myogenic electric organs (Kéver et al 2020).…”