Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning.

Vision represents an excellent model for studying adaptation, given the genotype-to-phenotype-map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we characterized the visual system of Neotropical Characiformes, which is the result of several spectral tuning mechanisms acting in concert including gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2-chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the entire opsin gene repertoire of characiforms is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS- and RH1-duplicates originated from a teleost specific whole-genome duplication as well as characiform-specific duplication events. Both LWS-opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS-paralogs has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. In addition, characiforms exhibited species-specific differences in opsin expression. Finally, we found interspecific and intraspecific variation in the use of A1/A2-chromophores correlating with the light environment. These multiple mechanisms may be a result of the highly diverse visual environments where Characiformes have evolved.