Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-23T03:45:09.408Z Has data issue: false hasContentIssue false
  • English
  • Français

Variation in opsin transcript expression explains intraretinal differences in spectral sensitivity of the northern anchovy

Published online by Cambridge University Press:  23 April 2018

ILARIA SAVELLI  and
IÑIGO NOVALES FLAMARIQUE
ILARIA SAVELLI
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada
IÑIGO NOVALES FLAMARIQUE*
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada Department of Biology, University of Victoria, Victoria, British Columbia V8W 2Y2, Canada
*
*Address correspondence to: Iñigo Novales Flamarique. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Vertebrate retinal photoreceptors house visual pigments that absorb light to begin the process of vision. The light absorbed by a visual pigment depends on its two molecular components: protein (opsin) and chromophore (a vitamin A derivative). Although an increasing number of studies show intraretinal variability in visual pigment content, it is only for two mammals (human and mouse) and two birds (chicken and pigeon) that such variability has been demonstrated to underlie differences in spectral sensitivity of the animal. Here, we show that the spectral sensitivity of the northern anchovy varies with retinal quadrant and that this variability can be explained by differences in the expression of opsin transcripts. Retinal (vitamin A1) was the only chromophore detected in the retina, ruling out this molecular component as a source of variation in spectral sensitivity. Chromatic adaptation experiments further showed that the dorsal retina had the capacity to mediate color vision. Together with published results for the ventral retina, this study is the first to demonstrate that intraretinal opsin variability in a fish drives corresponding variation in the animal’s spectral sensitivity.

Keywords

AnchovyCone photoreceptorChromophoreOptic nerveColor vision
Type
Research Article
Information
Visual Neuroscience , Volume 35 , 2018 , E005
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Applebury, M.L., Antoch, M.P., Blaxter, L.C., Chun, L.L., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A. & Robbins, J.T. (2000). The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513–523.CrossRefGoogle Scholar
Arrese, C.A., Oddy, A.Y., Runham, P.B., Hart, N.S., Shand, J., Hunt, D.M. & Beazley, L.D. (2005). Cone topography and spectral sensitivity in two potentially trichromatic marsupials, the quokka (Setonix brachyurus) and quenda (Isoodon obesulus). Proceedings of the Royal Society B: Biological Sciences 272, 791–796.CrossRefGoogle ScholarPubMed
Baden, T., Schubert, T., Chang, L., Wei, T., Zaichuk, M., Wissinger, B. & Euler, T. (2013). A tale of two retinal domains: Near-optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution. Neuron 80, 1206–1217.CrossRefGoogle ScholarPubMed
Caceci, C.M. & Cacheris, W.P. (1984). Fitting curves to data, the Simplex algorithm is the answer. Byte 5, 340–360.Google Scholar
Calderone, J.B. & Jacobs, G.H. (1995). Regional variations in the relative sensitivity to UV light in the mouse retina. Visual Neuroscience 12, 463–468.CrossRefGoogle ScholarPubMed
Calderone, J.B. & Jacobs, G.H. (2003). Spectral properties and retinal distributions of ferret cones. Visual Neuroscience 20, 11–17.CrossRefGoogle ScholarPubMed
Chen, Y., Znoiko, S., DeGrip, W.J., Crouch, R.K. & Ma, J.X. (2008). Salamander blue-sensitive cones lost during metamorphosis. Photochemistry & Photobiology 84, 855–862.CrossRefGoogle ScholarPubMed
Cheng, C.L. & Novales Flamarique, I. (2007). Chromatic organization of cone photoreceptors in the retina of rainbow trout: Single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development. Journal of Experimental Biology 210, 4123–4135.CrossRefGoogle ScholarPubMed
Curcio, C.A., Allen, K.A., Sloan, K.R., Lerea, C.L., Hurley, J.B., Klock, I.B. & Milam, A.H. (1991). Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. Journal of Comparative Neurology 312, 610–624.CrossRefGoogle ScholarPubMed
Dalton, B.E., de Busserolles, F., Marshall, N.J. & Carleton, K.L. (2017). Retinal specialization through spatially varying cell densities and opsin coexpression in cichlid fish. Journal of Experimental Biology 220, 266–277.Google ScholarPubMed
DeMarco, P.J. & Powers, M.K. (1991). Spectral sensitivity of on and off responses from the optic nerve of goldfish. Visual Neuroscience 6, 207–217.CrossRefGoogle Scholar
Fineran, B.A. & Nicol, J.A.C. (1978). Studies of the photoreceptors of Anchoa mitchilli and Anchoa hepsetus Engraulidae with particular reference to the cones. Philosophical Transactions of the Royal Society B: Biological Sciences 283, 5–60.Google Scholar
Fleishman, L.J., Loew, E.R. & Whiting, M.J. (2011). High sensitivity to short wavelengths in a lizard and implications for understanding the evolution of visual pigments in lizards. Proceedings of the Royal Society B: Biological Sciences 278, 2891–2899.CrossRefGoogle Scholar
Hárosi, F.I. (1994). An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34, 1359–1367.CrossRefGoogle ScholarPubMed
Hárosi, F.I. & Novales Flamarique, I. (2012). Functional significance of the taper of vertebrate cone photoreceptors. Journal of General Physiology 139, 159–187.CrossRefGoogle ScholarPubMed
Hayasi, S. (1963). A note on the biology and fishery of the Japanese anchovy, Engraulis japonica (Houtuyn). California Cooperative Oceanic Fisheries Investigations 11, 44–57.Google Scholar
Heß, M. (2009). Triple cones in the retinae of three anchovy species: Engraulis encrasicolus, Cetengraulis mysticetus and Anchoa macrolepidota (Engraulididae, Teleostei). Vision Research 49, 1569–1582.CrossRefGoogle Scholar
Heß, M., Melzer, R.R., Eser, R. & Smola, U. (2006). The structure of anchovy outer retinae (Engraulididae, Clupeiformes)—A comparative light- and electron-microscopy study using museum-stored material. Journal of Morphology 267, 1356–1380.CrossRefGoogle ScholarPubMed
Hughes, A., Saszik, S., Bilotta, J., DeMarco, P.J. Jr. & Patterson, W.F. II (1998). Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Visual Neuroscience 15, 1029–1037.CrossRefGoogle Scholar
Isayama, T., Chen, Y., Kono, M., Fabre, E., Slavsky, M., DeGrip, W.J., Ma, J-X., Crouch, R. & Makino, C.L. (2014). Co-expression of three opsins in cone photoreceptors of the salamander, Ambystoma tigrinum. Journal of Comparative Neurology 522, 2249–2265.CrossRefGoogle Scholar
Iwanicki, T.W., Novales Flamarique, I., Ausió, J., Morris, E. & Taylor, J.S. (2017). Fine tuning light sensitivity in the starry flounder (Platichthys stellatus) retina: Regional variation in photoreceptor cell morphology and opsin gene expression. Journal of Comparative Neurology 525, 2328–2342.CrossRefGoogle ScholarPubMed
Kondrashev, S.L., Gnyubkina, V.P. & Zueva, L.V. (2012). Structure and spectral sensitivity of photoreceptors of two anchovy species: Engraulis japonicus and Engraulis encrasicolus. Vision Research 68, 19–27.CrossRefGoogle ScholarPubMed
Kondrashev, S.L., Kornienko, M.S., Gnyubkina, V.P. & Frolova, L.T. (2016). Intraretinal variability and specialization of cones in Japanese anchovy (Engraulis japonicus, Engraulidae). Journal of Morphology 277, 472–481.CrossRefGoogle ScholarPubMed
Kondrashev, S.L., Miyazaki, T., Lamash, N.E. & Tsuchiya, T. (2013). Three cone opsin genes determine the properties of the visual spectra in the Japanese anchovy, Engraulis japonicus (Engraulidae, Teleostei). Journal of Experimental Biology 216, 1041–1052.Google ScholarPubMed
Leal, M. & Fleishman, L.J. (2002). Evidence for habitat partitioning based on adaptation to environmental light in a pair of sympatric lizard species. Proceedings of the Royal Society B: Biological Sciences 269, 351–359.CrossRefGoogle Scholar
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC t method. Methods 25, 402–408.CrossRefGoogle Scholar
Lukáts, Á., Szabó, A., Röhlich, P., Vígh, B. & Szél, Á. (2005). Photopigment coexpression in mammals: Comparative and developmental aspects. Histology and Histopathology 20, 551–574.Google ScholarPubMed
McDonald, C.G. & Hawryshyn, C.W. (1995). Intraspecific variation of spectral sensitivity in threespine stickleback (Gasterosteus acuelatus) from different photic regimes. Journal of Comparative Physiology A 176, 255–260.CrossRefGoogle Scholar
McKeefy, D.J., Murray, I.J. & Parry, N.R. (2007). Perceived shifts in saturation and hue of chromatic stimuli in the near peripheral retina. Journal of the Optical Society of America A 24, 3168–3179.CrossRefGoogle Scholar
Miyazaki, T., Kondrashev, S.L., Kasagi, S., Mizusawa, K. & Takahashi, A. (2017). Sequence and localization of an ultraviolet (sws1) opsin in the retina of the Japanese sardine Sardinops melanostictus (Teleostei: Clupeiformes). Journal of Fish Biology 90, 954–967.CrossRefGoogle ScholarPubMed
Neitz, M., Balding, S.D., McMahon, C., Sjoberg, S.A. & Neitz, J. (2006). Topography of long- and middle-wavelength sensitive cone opsin gene expression in human and Old World monkey retina. Visual Neuroscience 23, 379–385.CrossRefGoogle ScholarPubMed
Novales Flamarique, I. (2011). Unique photoreceptor arrangements in a fish with polarized light discrimination. Journal of Comparative Neurology 519, 714–737.CrossRefGoogle Scholar
Novales Flamarique, I. (2013). Opsin switch reveals function of the ultraviolet cone in fish foraging. Proceedings of the Royal Society B: Biological Sciences 280, 20122490.CrossRefGoogle ScholarPubMed
Novales Flamarique, I. (2016). Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones. Proceedings of the Royal Society B: Biological Sciences 283, 20160058.CrossRefGoogle ScholarPubMed
Novales Flamarique, I. (2017). A vertebrate retina with segregated colour and polarization sensitivity. Proceedings of the Royal Society B: Biological Sciences 284, 20170759.CrossRefGoogle ScholarPubMed
Novales Flamarique, I. & Hárosi, F.I. (1999). Photoreceptor pigments of the blueback herring (Alosa aestivalis, Clupeidae) and the Atlantic silverside (Menidia menidia, Atherinidae). Biological Bulletin 197, 235–236.CrossRefGoogle Scholar
Novales Flamarique, I. & Hárosi, F.I. (2002). Visual pigments and dichroism of anchovy cones: A model system for polarization detection. Visual Neuroscience 19, 467–473.CrossRefGoogle Scholar
Novales Flamarique, I. & Hawryshyn, C.W. (1997). Is the use of underwater polarized light by fish restricted to crepuscular time periods? Vision Research 37, 975–989.CrossRefGoogle ScholarPubMed
Novales Flamarique, I. & Hawryshyn, C.W. (1998). Photoreceptor types and their relation to the spectral and polarization sensitivities of clupeoid fishes. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 182, 793–803.CrossRefGoogle Scholar
Novales Flamarique, I. & Wachowiak, M. (2015). Functional segregation of retinal ganglion cell projections to the optic tectum of rainbow trout. Journal of Neurophysiology 114, 2703–2717.CrossRefGoogle Scholar
Novales Flamarique, I., Cheng, C.L., Bergstrom, C. & Reimchen, T.E. (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.Google Scholar
Novales Flamarique, I., Mueller, G.A., Cheng, C.L. & Figiel, C.R. (2007). Communication using eye roll reflective signalling. Proceedings of the Royal Society B: Biological Sciences 274, 877–882.CrossRefGoogle ScholarPubMed
Palacios, A.G., Goldsmith, T.H. & Bernard, G.D. (1996). Sensitivity of cones from a cyprinid fish (Danio aequipinnatus) to ultraviolet and visible light. Visual Neuroscience 13, 411–421.CrossRefGoogle ScholarPubMed
Remy, M. & Emmerton, J. (1989). Behavioural spectral sensitivities of different retinal areas in pigeons. Behavioural Neuroscience 103, 170–177.CrossRefGoogle ScholarPubMed
Risner, M.L., Lemerise, E., Vukmanic, E.V. & Moore, A. (2006). Behavioral spectral sensitivity of the zebrafish (Danio rerio). Vision Research 46, 2625–2635.CrossRefGoogle ScholarPubMed
Roorda, A. & Williams, D.R. (1999). The arrangement of the three cone classes in the living human eye. Nature 397, 520–522.CrossRefGoogle ScholarPubMed
Sabbah, S., Lamela Laria, R., Gray, S.M. & Hawryshyn, C.W. (2010). Functional diversity in the color vision of cichlid fishes. BMC Biology 8, 133.CrossRefGoogle ScholarPubMed
Sakai, Y., Ohtsuki, H., Kasagi, S., Kawamura, S. & Kawata, M. (2016). Effects of light environment during growth on the expression of cone opsin genes and behavioral spectral sensitivities in guppies (Poecilia reticulata). BMC Evolutionary Biology 16, 106.CrossRefGoogle ScholarPubMed
Savelli, I., Novales Flamarique, I., Iwanicki, T. & Taylor, J.S. (2018). Parallel opsin switches in multiple cone types of the starry flounder retina: Tuning visual pigment composition for a demersal life style. Scientific Reports 8, 4763.CrossRefGoogle ScholarPubMed
Sirovich, L. & Abramov, I. (1977). Photopigments and pseudo-pigments. Vision Research 17, 5–16.CrossRefGoogle ScholarPubMed
Takechi, M. & Kawamura, S. (2005). Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. Journal of Experimental Biology 208, 1337–1345.CrossRefGoogle ScholarPubMed
Temple, S., Hart, N.S., Marshall, N.J. & Collin, S.P. (2010). A spitting image: Specializations in archerfish eyes for vision at the interface between air and water. Proceedings of the Royal Society B: Biological Sciences 277, 2607–2615.CrossRefGoogle ScholarPubMed
Van Nynatten, A., Bloom, D., Chang, B.S.W. & Lovejoy, N. (2015). Out of the blue: Adaptive visual pigment evolution accompanies Amazon invasion. Biology Letters 11, 20150349.CrossRefGoogle ScholarPubMed
Wortel, J.F., Rugenbrink, H. & Nuboer, J.F.W. (1987). The photopic spectral sensitivity of the dorsal and ventral retinae of the chicken. Journal of Comparative Physiology A 160, 151–154.CrossRefGoogle Scholar
Wortel, J.F., Wubbels, R.J. & Nuboer, J.F.W. (1984). Photopic spectral sensitivities of the red and yellow field of the pigeon retina. Vision Research 24, 1107–1113.CrossRefGoogle ScholarPubMed
Weimerskirch, H., Bertrand, S., Silva, J., Bost, C. & Peraltilla, S. (2012). Foraging in Guanay cormorant and Peruvian booby, the major guano-producing seabirds in the Humboldt Current System. Marine Ecology Progress Series 458, 231–245.CrossRefGoogle Scholar