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

Hauser, Frances1; Xiao, Dawn1; Van Nynatten, Alexander1; Brochu-DeLuca, Kristen1; Rajakulendran, Thanara1; Elbassiouny, Ahmed1; Sivanesan, Harunya1; Sivananthan, Pradeega1; Crampton, William2; Lovejoy, Nathan R.1

Published Jan 16, 2024 on Dryad. https://doi.org/10.5061/dryad.7m0cfxq1x

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Jan 16, 2024 version files 2.01 MB

Abstract

Active electroreception — the ability to detect objects and communicate with conspecifics via the detection and generation of electric organ discharges (EODs) — has evolved convergently in several fish lineages. South American electric fishes (Gymnotiformes) are a highly species-rich group, possibly in part due to evolution of an electric organ (EO) that produces diverse EODs. Neofunctionalization of a voltage-gated sodium channel accompanied the evolution of electrogenic tissue from muscle and resulted in a novel gene (scn4aa) uniquely expressed in the EO. Here, we investigate the link between variation in scn4aa and differences in EOD waveform. We combine gymnotiform scn4aa sequences encoding the C-terminus of the Nav1.4a protein with biogeographic data and EOD recordings. We test whether physiological transitions among EOD types accompany differential selection pressures on scn4aa. We found positive selection on scn4aa coincided with shifts in EOD types. Species that evolved in the absence of predators, which likely selected for reduced EOD complexity, exhibited increased scn4aa evolutionary rates. We model mutations in the protein that may underlie changes in protein function and discuss our findings in the context of gymnotiform signalling ecology. Together, this work sheds light on the selective forces underpinning major evolutionary transitions in electric signal production.