Vision frequently mediates critical behaviours, and photoreceptors must respond to the light available to accomplish these tasks. Most photoreceptors are thought to contain a single visual pigment, an opsin protein bound to a chromophore, which together determine spectral sensitivity. Mechanisms of spectral tuning include altering the opsin, changing the chromophore and incorporating pre-receptor filtering. A few exceptions to the use of a single visual pigment have been documented in which a single mature photoreceptor coexpresses opsins that form spectrally distinct visual pigments, and in these exceptions the functional significance of coexpression is unclear. Here we document for the first time photoreceptors coexpressing spectrally distinct opsin genes in a manner that tunes sensitivity to the light environment. Photoreceptors of the cichlid fish, Metriaclima zebra, mix different pairs of opsins in retinal regions that view distinct backgrounds. The mixing of visual pigments increases absorbance of the corresponding background, potentially aiding the detection of dark objects. Thus, opsin coexpression may be a novel mechanism of spectral tuning that could be useful for detecting prey, predators and mates. However, our calculations show that coexpression of some opsins can hinder colour discrimination, creating a trade-off between visual functions.

Animals vary in their sensitivities to different wavelengths of light. Sensitivity differences can have fitness implications in terms of animals’ ability to forage, find mates and avoid predators. As a result, visual systems are likely selected to operate in particular lighting environments and for specific visual tasks. This review focuses on cichlid vision, as cichlids have diverse visual sensitivities, and considerable progress has been made in determining the genetic basis for this variation. We describe both the proximate and ultimate mechanisms shaping cichlid visual diversity using the structure of Tinbergen’s four questions. We describe 1) the molecular mechanisms that tune visual sensitivities including changes in opsin sequence and expression; 2) the evolutionary history of visual sensitivity across the African cichlid flocks; 3) the ontological changes in visual sensitivity and how modifying this developmental program alters sensitivities among species; and 4) the fitness benefits of spectral tuning mechanisms with respect to survival and mating success. We further discuss progress to unravel the gene regulatory networks controlling opsin expression and suggest that a simple genetic architecture contributes to the lability of opsin gene expression. Finally, we identify unanswered questions including whether visual sensitivities are experiencing selection, and whether similar spectral tuning mechanisms shape visual sensitivities of other fishes.

Critical behaviors such as predation and mate choice often depend on vision. Visual systems are sensitive to the spectrum of light in their environment, which can vary extensively both within and among habitats. Evolutionary changes in spectral sensitivity contribute to divergence and speciation. Spectral sensitivity of the retina is primarily determined by visual pigments, which are opsin proteins bound to a chromophore. We recently discovered that photoreceptors in different regions of the retina, which view objects against distinct environmental backgrounds, coexpress different pairs of opsins in an African cichlid fish, Metriaclima zebra. This coexpression tunes the sensitivity of the retinal regions to the corresponding backgrounds and may aid detection of dark objects, such as predators. Although intraretinal regionalization of spectral sensitivity in many animals correlates with their light environments, it is unknown whether variation in the light environment induces developmentally plastic alterations of intraretinal sensitivity regions. Here, we demonstrate with fluorescent in situ hybridization and qPCR that the spectrum and angle of environmental light both influence the development of spectral sensitivity regions by altering the distribution and level of opsins across the retina. Normally M. zebra coexpresses LWS opsin with RH2Aα opsin in double cones of the ventral but not the dorsal retina. However, when illuminated from below throughout development, adult M. zebra coexpressed LWS and RH2Aα in double cones both dorsally and ventrally. Thus, environmental background spectra alter the spectral sensitivity pattern that develops across the retina, potentially influencing behaviors and related evolutionary processes such as courtship and speciation.