Expression evolution facilitated the convergent neofunctionalization of a sodium channel gene

Ion channels have played a substantial role in the evolution of novel traits across all of the domains of life. A fascinating example of a novel adaptation is the convergent evolution of electric organs in the Mormyroid and Gymnotiform electric fishes. The regulated currents that flow through ion channels directly generate the electrical signals which have evolved in these fish. Here, we investigated how the expression evolution of two sodium channel paralogs (Scn4aa and Scn4ab) influenced their convergent molecular evolution following the teleost-specific whole-genome duplication. We developed a reliable assay to accurately measure the expression stoichiometry of these genes and used this technique to analyze relative expression of the duplicate genes in a phylogenetic context. We found that before a major shift in expression from skeletal muscle and neofunctionalization in the muscle-derived electric organ, Scn4aa was first downregulated in the ancestors of both electric lineages. This indicates that underlying the convergent evolution of this gene, there was a greater propensity toward neofunctionalization due to its decreased expression relative to its paralog Scn4ab. We investigated another derived muscle tissue, the sonic organ of Porichthys notatus, and show that, as in the electric fishes, Scn4aa again shows a radical shift in expression away from the ancestral muscle cells into the evolutionarily novel muscle-derived tissue. This study presents evidence that expression downregulation facilitates neofunctionalization after gene duplication, a pattern that may often set the stage for novel trait evolution after gene duplication.