Rapid evolution of a voltage-gated sodium channel gene in a lineage of electric fish leads to a persistent sodium current

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Abstract

Most weakly electric fish navigate and communicate by sensing electric signals generated by their muscle-derived electric organs. Adults of one lineage (Apteronotidae), which discharge their electric organs in excess of 1 kHz, instead have an electric organ derived from the axons of specialized spinal neurons (electromotorneurons [EMNs]). EMNs fire spontaneously and are the fastest-firing neurons known. This biophysically extreme phenotype depends upon a persistent sodium current, the molecular underpinnings of which remain unknown. We show that a skeletal muscle–specific sodium channel gene duplicated in this lineage and, within approximately 2 million years, began expressing in the spinal cord, a novel site of expression for this isoform. Concurrently, amino acid replacements that cause a persistent sodium current accumulated in the regions of the channel underlying inactivation. Therefore, a novel adaptation allowing extreme neuronal firing arose from the duplication, change in expression, and rapid sequence evolution of a muscle-expressing sodium channel gene.

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Thompson, A., Infield, D. T., Smith, A. R., Smith, G. T., Ahern, C. A., & Zakon, H. H. (2018). Rapid evolution of a voltage-gated sodium channel gene in a lineage of electric fish leads to a persistent sodium current. PLoS Biology, 16(3). https://doi.org/10.1371/journal.pbio.2004892

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