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.
Highlights
We investigated how voltage-gated sodium (Nav) channels contributed to the evolution of a novel electric organ system in the Apteronotids—a lineage of weakly electric fish
When combinations of these substitutions are introduced into a human sodium channel, they produce a significant persistent sodium current (INAP). This is the first sodium channel that generates a physiological persistent current without the aid of auxiliary proteins [24,25,26]. These findings indicate two phenomena: (1) paralogs of the same muscletype Nav channel have been implicated in the evolution of three separate electrocommunication systems within teleost fishes and (2) a molecular adaptation for the extremely high firing frequencies observed in an electric organ derived from neural cells was in part mediated by a new gene that originated from the duplication of a muscle-expressing gene
To identify Nav channels expressed in the EMNs, we generated transcriptomes from the posterior spinal cords and trunk muscle of adults of 3 species of Apteronotids (A. albifrons, A. leptorhynchus, and Parapteronotus hasemani), one myogenic electric gymnotiform (Eigenmannia virescens), and a catfish (Ictalurus punctatus) as a nonelectric outgroup
Summary
Animals were acquired through the aquarium trade. Fish were euthanized according to ethical guidelines set by IACUC at UT Austin and Indiana University Bloomington. Skeletal muscle samples were taken from the midtrunk hypaxial location and the spinal cord from the mid to tail location of 3 adult A. albifrons, I. punctatus, and E. virescens, as well as 1 adult A. leptorhynchus and P. hasemanii. Tissue samples were flash frozen in liquid nitrogen, and total RNA was extracted and DNA removed, following previously described protocols [23]. Total RNA samples were submitted to the University of Texas at Austin core genomics facility, where ribosomal RNA was removed; paired-end 100 bp RNA-seq (A. albifrons and I. punctatus) or paired-end 150 bp RNA-seq (E. virescens, A. leptrohynchus, and P. hasemanii) was performed on an Illumina HiSeq 2000 to produce between 30 and 34 million reads per sample.
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