7. Flamarique, IN; Fujihara, R; Yazawa, R; Bolstad, K; Gowen, B; Yoshizaki, G. (2021) Disrupted eye and head development in rainbow trout with reduced ultraviolet (sws1) opsin expression.J. Comp. Neurol. 529: 3013-3031 Disrupted eye and head development in rainbow trout with reduced ultraviolet (sws1) opsin expression
AB5407; CRISPR; Cas9; fish; photoreceptor; retina; sws1 antiserum; visual opsin
Visual opsins are proteins expressed by retinal photoreceptors that capture light to begin the process of phototransduction. In vertebrates, the two types of photoreceptors (rods and cones) express one or multiple opsins and are distributed in variable patterns across the retina. Some cones form opsin retinal gradients, as in the mouse, whereas others form more demarcated opsin domains, as in the lattice-like mosaic retinas of teleost fishes. Reduced rod opsin (rh1) expression in mouse, zebrafish, and African clawed frog results in lack of photoreceptor outer segments (i.e., the cilium that houses the opsins) and, in the case of the mouse, to retinal degeneration. The effects of diminished cone opsin expression have only been studied in the mouse where knockout of the short-wavelength sensitive 1 (sws1) opsin leads to ventral retinal cones lacking outer segments, but no retinal degeneration. Here we show that, following CRISPR/Cas9 injections that targeted knockout of the sws1 opsin in rainbow trout, fish with diminished sws1 opsin expression exhibited a variety of developmental defects including head and eye malformations, underdeveloped outer retina, mislocalized opsin expression, cone degeneration, and mosaic irregularity. All photoreceptor types were affected even though sws1 is only expressed in the single cones of wild fish. Our results reveal unprecedented developmental defects associated with diminished cone opsin expression and suggest that visual opsin genes are involved in regulatory processes that precede photoreceptor differentiation. DOI PubMed
6. Flamarique, IN. (2017) A vertebrate retina with segregated colour and polarization sensitivity.Proceedings of the Royal Society B-Biological Sciences 284 A vertebrate retina with segregated colour and polarization sensitivity
anchovy; optic nerve; cone photoreceptor; axial dichroism
Besides colour and intensity, some invertebrates are able to independently detect the polarization of light. Among vertebrates, such separation of visual modalities has only been hypothesized for some species of anchovies whose cone photoreceptors have unusual ultrastructure that varies with retinal location. Here, I tested this hypothesis by performing physiological experiments of colour and polarization discrimination using the northern anchovy, Engraulis mordax. Optic nerve recordings showed that the ventro-temporal (VT), but not the ventro-nasal (VN), retina was polarization sensitive, and this coincided with the exclusive presence of polarization-sensitive photoreceptors in the VT retina. Spectral (colour) sensitivity recordings from the VN retina indicated the contribution of two spectral cone mechanisms to the optic nerve response, whereas only one contributed to the VT retina. This was supported by the presence of only one visual pigment in the VT retina and two in the VN retina, suggesting that only the VN retina was associated with colour sensitivity. Behavioural tests further demonstrated that anchovies could discriminate colour and the polarization of light using the ventral retina. Thus, in analogy with the visual system of some invertebrates, the northern anchovy has a retina with segregated retinal pathways for colour and polarization vision. DOI
5. Flamarique, IN. (2016) Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones.Proceedings of the Royal Society B-Biological Sciences 283 Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones
ultraviolet cone; retina; foraging; zebrafish
Ultraviolet (UV) cones are photoreceptors that sense light in the range 300-450 nm and are found in the retinas of non-mammalian vertebrates and small mammals. Despite their widespread presence across taxa, the functions that these cones exert in the lives of animals remain largely unknown. In this study, I used the zebrafish for (lots of rods) mutant, characterized by a diminished UV cone population compared to that of wild-type zebrafish, to test whether its foraging performance differed from that of the wild-type (control). The mean location distance and angle (variables that are reliable indicators of foraging performance) at which control fish detected zooplankton prey were, on average, 24 and 90% greater than corresponding measures for for fish. Such inferior foraging performance of the mutant could be explained by reduced contrast perception of the prey, resulting from the diminished population of UV cones and associated sensitivity. Thus, UV cones enhance the foraging performance of zebrafish, a crucial ecological function that may explain why small zooplanktivorous fishes retain UV cones throughout their lives. DOI
4. Flamarique, IN. (2013) Opsin switch reveals function of the ultraviolet cone in fish foraging.Proceedings of the Royal Society B-Biological Sciences 280: Opsin switch reveals function of the ultraviolet cone in fish foraging
visual pigment; cone photoreceptor; retina; rainbow trout
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. DOI
3. Flamarique, IN; Bergstrom, C; Cheng, CL; Reimchen, TE. (2013) Role of the iridescent eye in stickleback female mate choice.Journal of Experimental Biology 216: 2806-2812 Role of the iridescent eye in stickleback female mate choice
PREY-SEARCH BEHAVIOR; GASTEROSTEUS-ACULEATUS; THREESPINE STICKLEBACKS; NUPTIAL COLOR; 3-SPINED STICKLEBACKS; SPECTRAL SENSITIVITY; POLARIZED-LIGHT; VISUAL-SYSTEMS; ULTRAVIOLET; SIGNAL
Many vertebrates exhibit prominent body colours that are used in courtship and territorial communication. Some fishes also have an eye whose iris becomes iridescent during the mating season, as in the threespine stickleback. Behavioural studies in this species have focused on the redness of the throat/jaw as the primary determinant of female mate choice. Unlike the iridescent eye, however, the red throat/jaw is not present in all stickleback populations, suggesting that the colour of the eye may be equally important for female mate choice. Here, we used data on photoreceptors and environmental light to assess body conspicuousness and the colour contrast of courtship signals for stickleback populations living in a range of waters, from clear (mesotrophic) to red light shifted (dystrophic). This analysis indicated that the redness of the throat/jaw is expressed to enhance the contrast of the eye. To test the importance of eye colour as a courtship signal, we carried out mate choice experiments in which females were presented with identical videos of a courting male but for the colour of the eye and/or the throat/jaw. Females did not choose based on differences in throat/jaw redness between videos, but preferred males with the highest contrast between the eye and the throat/jaw. This result points to the blue iridescent eye as a primary courtship signal in stickleback female mate choice. DOI
2. Flamarique, IN; Cheng, CL; Bergstrom, C; Reimchen, TE. (2013) Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors.Journal of Experimental Biology 216: 656-667 Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors
INNER NUCLEAR LAYER; SALMONID FISHES; GASTEROSTEUS-ACULEATUS; CONE PHOTORECEPTORS; BLUEFIN KILLIFISH; LUCANIA-GOODEI; NUPTIAL COLOR; SINGLE CONES; POLARIZED-LIGHT; GENE-EXPRESSION
Vertebrate 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 similar to 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. DOI
