Modulation of bioelectric cues in the evolution of flying fishes

Changes to allometry, or the relative proportions of organs and tissues within organisms, is a common means for adaptive character change in evolution. However, little is understood about how relative size is specified during development and shaped during evolution. Here, through a phylogenomic analysis of genome-wide variation in 35 species of flying fishes and relatives, we identify genetic signatures in both coding and regulatory regions underlying the convergent evolution of increased paired fin size and aerial gliding behaviors. To refine our analysis, we intersected convergent phylogenomic signatures with mutants with altered fin size identified in distantly related zebrafish. Through these paired approaches, we identify a surprising role for an L-type amino acid transporter, lat4a, and the potassium channel, kcnh2a, in the regulation of fin proportion. We show that interaction between these genetic loci in zebrafish closely phenocopies the observed fin proportions of flying fishes. The congruence of experimental and phylogenomic findings point to conserved, non-canonical signaling integrating bioelectric cues and amino acid transport in the establishment of relative size in development and evolution. •Aerial gliding evolved in fishes through differential allometric growth of paired fins•The amino acid transporter lat4a and the potassium channel kcnh2a regulate fin size•Convergence and selection in lat4a and bioelectric signaling genes in flying fishes•Interaction between lat4a and kcnh2a establishes flying fish bauplan in zebrafish Daane et al. intersect patterns of genome evolution in flying fishes with genetic screens in zebrafish to identify a role for the amino acid transporter lat4a and the potassium channel kcnh2a in regulating fin size. A combination of alleles from both genes is sufficient to reproduce the flying fish fin bauplan in the distantly related zebrafish.