Tbx2a modulates switching of opsin gene expression

ABSTRACT Differences in sensory tuning are reported to maintain species boundaries and may even lead to speciation. Variation in the tuning of color vision is likely due to differences in the expression of opsin genes. Over 1,000 species of African cichlid fishes provide an excellent model system for studying the genetic basis of opsin gene expression because of the presence of seven distinct genes, yet individual species typically express only a divergent set of three opsins. The evolution of such shifts is expected to arise through either (a) two simultaneous regulatory changes (one for each opsin), or (b) one regulatory change that simultaneously promotes expression of one opsin while repressing another. Here, we used QTL analyses, genome sequencing, and gene expression studies to identify the transcription factor Tbx2a as likely driving a switch between LWS and RH2 opsin expression. Binding sites for Tbx2a in the LWS promoter and the highly conserved Locus Control Region of RH2 act to concurrently promote LWS expression while repressing RH2 expression. Our data support the hypothesis that instant changes in visual tuning can be achieved by switching the expression of multiple genes by a single mutation and do not require independent changes in the regulatory regions of each opsin.