The retinas of many vertebrates have cone photoreceptors that express multiple visual pigments. In many of these animals, including humans, the original cones to appear in the retina (which express UV or blue opsin) may change opsin types, giving rise to new spectral phenotypes. Here we used microspectrophotometry and in situ hybridization with cDNA probes to study the distribution of UV and blue cones in the retinas of four species of Pacific salmon (coho, chum, chinook, and pink salmon), in the Atlantic salmon, and in the rainbow/steelhead trout. In Pacific salmon and in the trout, all single cones express a UV opsin at hatching (lambda(max) of the visual pigment approximately 365 nm), and these cones later transform into blue cones by opsin changeover (lambda(max) of the blue visual pigment approximately 434 nm). Cones undergoing UV opsin downregulation exhibit either of two spectral absorbance profiles. The first is characterized by UV and blue absorbance peaks, with blue absorbance dominating the base of the outer segment. The second shows UV absorbance diminishing from the outer segment tip to the base, with no sign of blue absorbance. The first absorbance profile indicates a transformation from UV to blue phenotype by opsin changeover, while the second type suggests that the cone is undergoing apoptosis. These two events (transformation and loss of corner cones) are closely associated in time and progress from ventral to dorsal retina. Each double cone member contains green (lambda(max) approximately 510 nm) or red (lambda(max) approximately 565 nm) visual pigment (double cones are green/red pairs), and, like the rods (lambda(max) approximately 508 nm), do not exhibit opsin changeover. Unlike Pacific salmonids, the Atlantic salmon shows a mixture of UV and blue cones and a partial loss of corner cones at hatching. This study establishes the UV-to-blue cone transformation as a general feature of retinal growth in Pacific salmonids (genus Oncorhynchus).
Here, we used in situ hybridization with species-specific riboprobes and microspectrophotometry on rainbow trout retina to show that: (1) single cones in the juvenile switch opsin expression from SWS1 to SWS2, (2) this switch is not reversed in the adult, i.e. all single cones in the main retina continue to express SWS2 opsin, and (3) opsin switches do not occur in double cones: each member expresses one opsin, maximally sensitive to green (RH2) or red (LWS) light. The opsin switch in the single cones of salmonid fishes may be a general process of chromatic organization that occurs during retinal development of most vertebrates.Supplementary material available online at
Although several studies have shown that ultraviolet (UV) wavelengths are important in naturally occurring, visually guided behaviours of vertebrates, the function of the UV cone in such behaviours is unknown. Here, I used thyroid hormone to transform the UV cones of young rainbow trout into blue cones, a phenomenon that occurs naturally as the animal grows, to test whether the resulting loss of UV sensitivity affected the animal's foraging performance on Daphnia magna, a prey zooplankton. The distances and angles at which prey were located (variables that are known indicators of foraging performance) were significantly reduced for UV knock-out fish compared with controls. Optical measurements and photon-catch calculations revealed that the contrast of Daphnia was greater when perceived by the visual system of control versus that of thyroid-hormone-treated fish, demonstrating that the UV cone enhanced the foraging performance of young rainbow trout. Because most juvenile fishes have UV cones and feed on zooplankton, this finding has wide implications for understanding the visual ecology of fishes. The enhanced target contrast provided by UV cones could be used by other vertebrates in various behaviours, including foraging, mate selection and communication.
Each cone photoreceptor in the retina responds to light in a limited range of wavelengths, giving it a spectral phenotype. This phenotype is determined by the most prevalent of the photoreceptor's visual-pigment proteins (opsins) and is assumed to remain unchanged during an animal's lifetime. Here we show that in the Pacific pink salmon, Oncorhynchus gorbuscha, single cones can switch their spectral phenotype from ultraviolet to blue by regulating the production of the appropriate opsins as the fish grow older. This photoreceptor plasticity may operate to modulate colour vision as the salmon's lifestyle changes.
SUMMARYVertebrate colour vision is mediated by the differential expression of visual pigment proteins (opsins) in retinal cone photoreceptors. Many species alter opsin expression during life, either as part of development or as a result of changes in habitat. The latter, a result of phenotypic plasticity, appears common among fishes, but its cellular origin and ecological significance are unknown. Here, we used adult threespine stickleback fish from different photic regimes to investigate heritable variability and phenotypic plasticity in opsin expression. Fish from clear waters had double cones that expressed long (LWS) and middle (RH2) wavelength opsins, one per double cone member. In contrast, fish from red light-shifted lakes had double cones that were >95% LWS/LWS pairs. All fish had single cones that predominantly expressed a short wavelength (SWS2) opsin but ultraviolet cones, expressing a SWS1 opsin, were present throughout the retina. Fish from red light-shifted lakes, when transferred to clear waters, had a ~2% increase in RH2/LWS double cones, though double cone density remained constant. Comparison of visual pigment absorbance and light transmission in the environment indicated that the opsin complements of double cones maximized sensitivity to the background light, whereas single cones had visual pigments that were spectrally offset from the dominant background wavelengths. Our results indicate that phenotypic plasticity in opsin expression is minor in sticklebacks and of questionable functional significance. Supplementary material available online at
We measured the spectral distributions of the underwater total and polarized light fields in the upper photic zone of meso-eutrophic waters (i.e., blue-green waters containing medium to high chlorophyll a concentrations). Per cent polarization levels during the day were always lower than 40%, but at crepuscular times these values could increase to 67%. A corresponding change occurred in the spectral distribution, with proportionately more shorter wavelength photons contributing to the total spectrum during crepuscular periods. Electrophysiological recordings from the optic nerve of rainbow trout subjected to light stimuli of varying polarization percentages show that the animal's threshold for detecting polarized light is between 63 and 72%. These physiological findings suggest that the use of water-induced polarized light cues by rainbow trout and similar percomorph fish should be restricted to crepuscular time periods.
The aquatic stages of amphibians may be sensitive to increased levels of solar ultraviolet B radiation (UV-B, 280–320 nm) that have been observed at higher latitudes over the past several decades, but the effects on most species are unknown. We exposed eggs and larvae of Hyla regilla and Rana aurora to three experimental treatments: (1) solar UV < 450 nm blocked (control), (2) ambient solar UV, and (3) solar UV-B enhanced 15 and 30% above ambient levels at midday to simulate conditions predicted for the next decades at midlatitudes. The rearing containers were covered with acrylic filters to provide the desired radiation regimes. Hatching success of H. regilla did not differ among the treatments and was 87.7, 71.8, and 87.1% in April 1995 and 94.0, 85.1, and 97.4% in May 1995 for the control, ambient, and enhanced UV-B treatments, respectively. In contrast, hatching success of R. aurora in the enhanced UV-B treatment (56.0%) was lower than in the ambient UV (89.8%) and control (81.0%) treatments. Larval survival over the first 2 months of development was reduced to 18.4% for H. regilla and 2.6% for R. aurora in the enhanced UV-B treatment compared with the ambient UV and control treatments. We conclude that ambient UV levels at the study site did not affect the embryonic or early larval survival of either of the species tested under the experimental conditions, but both species are potentially vulnerable to increases in solar UV-B.
Thyroid hormone induces a UV (SWS1)-to-blue (SWS2) opsin switch in the retina of young salmonid fishes that is identical with that occurring during natural development. The switch occurs in differentiated photoreceptors, is reversible (maintained by thyroid hormone exposure), and can be induced only before its natural onset. Thyroid hormone did not cause changes in the number of proliferating cells in the ONL. These results conform to the dynamics of thyroid hormone-induced opsin expression in the mouse and are consistent with the opsin plasticity found in differentiated photoreceptors of the fruit fly, Drosophila melanogaster. This work establishes a role for thyroid hormone in triggering opsin switches in the vertebrate retina.
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