Functional diversity in the color vision of cichlid fishes

Abstract

Abstract Background Color vision plays a critical role in visual behavior. An animal's capacity for color vision rests on the presence of differentially sensitive cone photoreceptors. Spectral sensitivity is a measure of the visual responsiveness of these cones at different light wavelengths. Four classes of cone pigments have been identified in vertebrates, but in teleost fishes, opsin genes have undergone gene duplication events and thus can produce a larger number of spectrally distinct cone pigments. In this study, we examine the question of large-scale variation in color vision with respect to individual, sex and species that may result from differential expression of cone pigments. Cichlid fishes are an excellent model system for examining variation in spectral sensitivity because they have seven distinct cone opsin genes that are differentially expressed. Results To examine the variation in the number of cones that participate in cichlid spectral sensitivity, we used whole organism electrophysiology, opsin gene expression and empirical modeling. Examination of over 100 spectral sensitivity curves from 34 individuals of three species revealed that (1) spectral sensitivity of individual cichlids was based on different subsets of four or five cone pigments, (2) spectral sensitivity was shaped by multiple cone interactions and (3) spectral sensitivity differed between species and correlated with foraging mode and the spectral reflectance of conspecifics. Our data also suggest that there may be significant differences in opsin gene expression between the sexes. Conclusions Our study describes complex opponent and nonopponent cone interactions that represent the requisite neural processing for color vision. We present the first comprehensive evidence for pentachromatic color vision in vertebrates, which offers the potential for extraordinary spectral discrimination capabilities. We show that opsin gene expression in cichlids, and possibly also spectral sensitivity, may be sex-dependent. We argue that females and males sample their visual environment differently, providing a neural basis for sexually dimorphic visual behaviour. The diversification of spectral sensitivity likely contributes to sensory adaptations that enhance the contrast of transparent prey and the detection of optical signals from conspecifics, suggesting a role for both natural and sexual selection in tuning color vision.