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Evidence for Non-neutral Evolution in a Sodium Channel Gene in African Weakly Electric Fish (Campylomormyrus, Mormyridae)

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Abstract

Voltage-gated sodium channels, Nav1, play a crucial role in the generation and propagation of action potentials and substantially contribute to the shape of their rising phase. The electric organ discharge (EOD) of African weakly electric fish (Mormyroidea) is the sum of action potentials fired from all electrocytes of the electric organ at the same time and hence voltage-gated sodium channels are one factor—together with the electrocyte’s morphology and innervation pattern—that determines the properties of these EODs. Due to the fish-specific genome duplication, teleost fish possess eight copies of sodium channel genes (SCN), which encode for Nav1 channels. In mormyroids, SCN4aa is solely expressed in the electrocytes of the adult electric organ. In this study, we compared entire SCN4aa sequences of six species of the genus Campylomormyrus and identified nonsynonymous substitutions among them. SCN4aa in Campylomormyrus exhibits a much higher evolutionary rate compared to its paralog SCN4ab, whose expression is not restricted to the electric organ. We also found evidence for strong positive selection on the SCN4aa gene within Mormyridae and along the lineage ancestral to the Mormyridae. We have identified sites at which all nonelectric teleosts are monomorphic in their amino acid, but mormyrids have different amino acids. Our findings confirm the crucial role of SCN4aa in EOD evolution among mormyrid weakly electric fish. The inferred positive selection within Mormyridae makes this gene a prime candidate for further investigation of the divergent evolution of pulse-type EODs among closely related species.

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(adapted from Feulner et al. 2008a)

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Acknowledgments

We acknowledge assistance during labwork from Julien Hempel, Katja Havenstein, and Anja Ernst. We thank Francesco Lamanna for fruitful discussions. Financial support is acknowledged from Deutsche Forschungsgemeinschaft (TI 349/1) and the University of Potsdam.

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Correspondence to Ralph Tiedemann.

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Paul, C., Kirschbaum, F., Mamonekene, V. et al. Evidence for Non-neutral Evolution in a Sodium Channel Gene in African Weakly Electric Fish (Campylomormyrus, Mormyridae). J Mol Evol 83, 61–77 (2016). https://doi.org/10.1007/s00239-016-9754-8

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  • DOI: https://doi.org/10.1007/s00239-016-9754-8

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