Fine‐tuning light sensitivity in the starry flounder (Platichthys stellatus) retina: Regional variation in photoreceptor cell morphology and opsin gene expression

Abstract

Vertebrate color vision relies on the differential expression of visual pigment proteins (opsins) in cone photoreceptors of the retina. The diversity of opsins and their retinal expression patterns appear greatest for animals that experience variable light habitats, as is the case with flatfishes. Yet, opsin repertoires and expression patterns in this group of fishes are poorly described. Here, we unveil the visual opsin expression patterns of juvenile starry flounder (Platichthys stellatus) and describe the localization of cone types, their visual pigments and opsin expression. Juvenile starry flounder express eight opsins (Rh1, Sws1, Sws2A1, Sws2A2, Sws2B, Rh2A1, Rh2A2, Lws) and possess a corresponding number of photoreceptor visual pigments, with peak absorbance ranging from 369 to 557 nm. Retinal (vitamin A1) was the only chromophore detected in the retina. Intraretinal variation in opsin abundance consisted of greater expression of both RH2, and lesser expression of SWS1 and both SWS2A, opsin transcripts in the dorsal compared to the ventral retina. Overall cone density was greater in the dorsal retina which was also characterized by a larger proportion of unequal double cones compared with the ventral retina. Together, our results suggest that large opsin repertoires serve to optimize visual function under variable light environments by differential expression of opsin subsets with retinal location.

Parallel opsin switches in multiple cone types of the starry flounder retina: tuning visual pigment composition for a demersal life style

“…These bandwidths were also greater than those predicted for such pigments using empirical models based on opsin conjugation to A1 retinal chromophore 3 (Table 1 ). Such results suggested the contribution of multiple opsins to the S (445) and M (536) visual pigment absorbance curves since analyses of retinal extracts using High Performance Liquid Chromatography revealed the same A1 retinal chromophore as present in younger fish 34 (Fig. 2 ).…”

“…In a previous investigation, eight visual pigments were measured, using microspectrophotometry, that corresponded to seven cone opsins and one rod opsin (whose transcripts were quantified by digital PCR) in the retina of the young, post-metamorphic starry flounder (~5–15 g in weight) 34 . The correspondence between visual pigments and opsin types was as follows: UV(369)-SWS1, S(415)-SWS2B, S(437)-SWS2A2, S(456)-SWS2A1, M(527)-RH2A1, M(545)-RH2A2, L(557)-LWS, and rod (507)-RH1.…”

Light induced changes in starry flounder (Platichthys stellatus) opsin expression and its influence on vision estimated from a camouflage-based behavioural assay

“…Microspectrophotometry data indicate that all are translated and that just one type of chromophore is used (9). We predicted opsin expression would be modified by a seven-week exposure to distinct light environments and that changes in opsin expression over that length of time would influence vision.…”

“…It may be that a large visual opsin repertoire is a 'toolkit', with subsets of opsins used at different stages of development, in different light environments, or indeed in particular regions of the retina. Several authors have reported observations consistent with this hypothesis: developmental variation (6), geographic distribution based on light environment (7), and regions of the retina (8,9). Despite correlations between opsin repertoire or expression patterns and the light environment, clear connections between variation in opsin expression and visual performance have rarely been demonstrated outside of humans.…”

“…Flounder camouflage match natural substrates well when modeled to mono-, di-, and tri-chromatic visual systems (16), however, here we elected to use checkboards (as in Mäthger et al 2006 (17)) to elicit an exaggerated pattern response. We held starry flounder (Platichthys stellatus), a flatfish possessing eight visual opsin genes (9), in outdoor aquaria exposed to either sunlight or greenfiltered light anticipating opsin expression would adjust to each environment as in Fuller & Claricoates (2011) (18). We quantified the starry flounder's camouflage response to measure the effect of opsin expression variation on vision.…”