Derived loss of signal complexity and plasticity in a genus of weakly electric fish

Abstract

Signal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. Signal mimicry, mate recognition, and sexual selection are potential factors maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.

Ecologically mediated differences in electric organ discharge drive evolution in a sodium channel gene in South American electric fishes

“…Second, much like other sensory systems, the EOD is a highly complex phenotype determined by variation across multiple levels of biological organization. EOD variation is also modulated by EO structure [4,46], electrocyte innervation and morphology [22], ion channel repertoire and spatial distribution [49,50] and post-translational modifications of ion channels [23]. Cross-disciplinary investigation combining these variables with taxonomically extensive comparative genomics and transcriptomics [14,[50][51][52], model-based analyses of selection on genes [53] and analyses of abiotic and biotic conditions [54], represents a powerful way to understand gymnotiform electric signal diversity moving forwards.…”

“…For example, at the neuroanatomical level, differential innervation of electrocytes plays a role: in monophasic Electrophorus and Gymnotus obscurus , electrocytes are only electrically excitable on one face, while species with complex EODs exhibit excitability on both electrocyte faces [4,22,45,46]. By contrast, despite expressing voltage-gated sodium channels on both electrocyte faces, Brachyhypopomus bennetti produces a monophasic discharge and its electrocytes are innervated only on the posterior face [23]. At the molecular level, B. bennetti does not appear to have unique mutations in the C-terminus compared to its non-monophasic sister taxon (electronic supplementary material, tables S5,S6).…”

“…Among Gymnotiformes with pulse-type EODs, signals span a wide range of complexity: many species produce a complex multiphasic signal, and others a simple monophasic pulse [1,4,20]. At the physiological and neuroanatomical level, variation in electrocyte size and innervation patterns, the spatial distribution of ion channels across the electrocyte membrane, diversity of ion channels and finally ion channel protein structure likely mediate this diversity in EOD types [4,19,21–23].

Figure 1( a ) In Gymnotiformes, the electric organ is derived from either skeletal muscle tissue (myogenic) or neural tissue (neurogenic).

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