Variable light environments induce plastic spectral tuning by regional opsin coexpression in the African cichlid fish, Metriaclima zebra

Abstract

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.

Retinal specialization through spatially varying cell densities and opsin coexpression in cichlid fish

“…Thus coexpression in double cones is low in the dorsotemporal retina. To further characterize this infrequent dorsotemporal coexpression, we re-examined previously fixed retinal samples from two fish shown to have unusually high coexpression in the more dorsal and temporal regions (Dalton et al, 2014(Dalton et al, , 2015. This extended the five regions transected previously to more globally sample opsin expression across the entire retina, similarly to what we did for the single cones in the present study.…”

“…All fish were reared in the same light environment, which, compared with natural M. zebra habitat, is rich in long wavelength light and has no ultraviolet light (Dalton et al, 2015). Rearing and handling of fish were carried out in accordance with an approved IACUC protocol (University of Maryland R15-54).…”

“…To map expression of opsins in single cones across the retina, we performed double labeling fluorescent in situ hybridization on whole retinas according to published methods (Allison et al, 2010;Barthel and Raymond, 2000;Dalton et al, 2014Dalton et al, , 2015. After euthanizing fish, we removed retinas and fixed them in 4% paraformaldehyde overnight.…”

“…We also performed this whole-retina examination on two retinas that we had probed in our previous studies of double cone opsin expression. We used one retina that was probed for RH2Aalpha and LWS (individual RI1 in table S3 from Dalton et al, 2015) and one probed for RH2B and RH2Abeta (individual 15 in fig. 3c from Dalton et al, 2014).…”

Exploring visual plasticity: dietary carotenoids can change color vision in guppies (Poecilia reticulata)

“…Traditionally, color vision was thought to only vary across species, but recent work in several taxa has found that color vision can also vary across populations [e.g., bluefin killifish (Fuller et al 2004), cichlids , stickleback (Flamarique et al 2013), guppies and close relatives (Sandkam et al 2015a, b)] which can be due to both genetic variation and plasticity (Fuller et al 2005;O'Quin et al 2012;Ehlman et al 2015; reviewed in Carleton et al 2016). Several studies have recently shown that visual systems are plastic with respect to developmental stage, time of day, and lighting environment (Fuller and Claricoates 2011;Johnson et al 2013;Flamarique et al 2013;Dalton et al 2015;Ehlman et al 2015;Sakai et al 2016).…”