Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T22:30:51.608Z Has data issue: false hasContentIssue false
  • English
  • Français

Eel visual pigments revisited: The fate of retinal cones during metamorphosis

Published online by Cambridge University Press:  06 March 2008

JAMES K. BOWMAKER ,
MA'AYAN SEMO ,
DAVID M. HUNT  and
GLEN JEFFERY
JAMES K. BOWMAKER*
Affiliation:
UCL Institute of Ophthalmology, University College London, London, United Kingdom
MA'AYAN SEMO
Affiliation:
UCL Institute of Ophthalmology, University College London, London, United Kingdom
DAVID M. HUNT
Affiliation:
UCL Institute of Ophthalmology, University College London, London, United Kingdom
GLEN JEFFERY
Affiliation:
UCL Institute of Ophthalmology, University College London, London, United Kingdom
*
Address correspondence and reprint requests to: J.K. Bowmaker, Division of Visual Science, UCL Institute of Ophthalmology, University College London, Bath Street, London EC1V 9El, UK. E-mail: j.bowmaker@ucl.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

During their complex life history, anguilliform eels go through a major metamorphosis when developing from a fresh water yellow eel into a deep-sea silver eel. In addition to major changes in body morphology, the visual system also adapts from a fresh water teleost duplex retina with rods and cones, to a specialized deep-sea retina containing only rods. The history of the rods is well documented with an initial switch from a porphyropsin to a rhodopsin (P5232 to P5011) and then a total change in gene expression with the down regulation of a “freshwater” opsin and its concomitant replacement by the expression of a typical “deep-sea” opsin (P5011 to P4821). Yellow eels possess only two spectral classes of single cones, one sensitive in the green presumably expressing an RH2 opsin gene and the second sensitive in the blue expressing an SWS2 opsin gene. In immature glass eels, entering into rivers from the sea, the cones contain mixtures of rhodopsins and porphyropsins, whereas the fully freshwater yellow eels have cone pigments that are almost pure porphyropsins with peak sensitivities at about 540–545 nm and 435–440 nm, respectively. However, during the early stages of metamorphosis, the pigments switch to rhodopsins with the maximum sensitivity of the “green”-sensitive cone shifting to about 525 nm, somewhat paralleling, but preceding the change in rods. During metamorphosis, the cones are almost completely lost.

Keywords

AnguillaYellow eelConeMetamorphosisVisual pigment
Type
Research Article
Information
Visual Neuroscience , Volume 25 , Issue 3 , May 2008 , pp. 249 - 255
Copyright
Copyright © Cambridge University Press 2008

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

REFERENCES

Beatty, D.D. (1975). Visual pigments of the American eel, Anguilla rostrata. Vision Research 15, 771–776.CrossRefGoogle ScholarPubMed
Berry, L., Brookes, D. & Walker, B. (1972). Problem of migration of European Eel (Anguilla anguilla). Science Progress 60, 465–485.Google Scholar
Bowmaker, J.K. (1995). The visual pigments of fish. Progress in Retina Eye Research 15, 1–31.CrossRefGoogle Scholar
Bowmaker, J.K., Astell, S., Hunt, D.M. & Mollon, J.D. (1991). Photosensitive and photo stable pigments in the retinae of Old World monkeys. Journal of Experimental Biology 156, 1–19.CrossRefGoogle Scholar
Bowmaker, J.K., Govardovskii, V.I., Shukolyukov, S.A., Zueva, L.V., Hunt, D.M., Sideleva, V.G. & Smirnova, O.G. (1994). Visual pigments and the photic environment: The cottoid fish of lake Baikal. Vision Research 34, 591–605.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. & Hunt, D.M. (2006). Evolution of vertebrate visual pigments. Current Biology 16, R484–R489.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. & Kunz, Y.W. (1987). Ultraviolet receptors, tetrachromatic colour vision and retinal mosaics in the brown trout (Salmo trutta): Age-dependent changes. Vision Research 27, 2101–2108.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. & Loew, E.R. (2007). Vision in fish. In The Senses: A Comprehensive Reference, eds. Kaneko, A. & Masland, R.H.Oxford: Elsevier.Google Scholar
Braekevelt, C.R. (1984). Retinal fine structure in the european eel Anguilla anguilla. II. Photoreceptors of the glass eel stage. Anatomischer Anzeiger 157, 233–243.Google ScholarPubMed
Braekevelt, C.R. (1985). Retinal fine structure in the European eel Anguilla anguilla. IV. Photoreceptors of the yellow eel stage. Anatomischer Anzeiger 158, 23–32.Google ScholarPubMed
Braekevelt, C.R. (1988a). Retinal fine structure in the European eel Anguilla anguilla. VI. Photoreceptors of the sexually immature silver eel stage. Anatomischer Anzeiger 166, 23–31.Google ScholarPubMed
Braekevelt, C.R. (1988b). Retinal fine structure in the European eel Anguilla anguilla. VIII. Photoreceptors of the sexually mature silver eel stage. Anatomischer Anzeiger 167, 1–10.Google ScholarPubMed
Bridges, C.D.B. (1972). The rhodopsin-porphyropsin visual system. In Photochemistry of Vision, ed. Dartnall, H.J.A., pp. 417–480. Berlin: Springer.CrossRefGoogle Scholar
Byzov, A.L., Damjanovic, I., Utina, I.A., Mickovic, B., Gacic, Z. & Andjus, R.K. (1998). Electrophysiological and spectral properties of second-order retinal neurons in the eel. Comparative Biochemistry and Physiology A 121, 197–208.CrossRefGoogle Scholar
Carleton, K.L. & Kocher, T.D. (2001). Cone opsin genes of African cichlid fishes: Tuning spectral sensitivity by differential gene expression. Molecular Biology and Evolution 18, 1540–1550.CrossRefGoogle ScholarPubMed
Carlisle, D.B. & Denton, E.J. (1959). On the metamorphosis of the visual pigments of Anguilla anguilla (L.). Journal of the Marine Biological Association UK 38, 97–102.CrossRefGoogle Scholar
Chinen, A., Hamaoka, T., Yamada, Y. & Kawamura, S. (2003). Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163, 663–675.CrossRefGoogle ScholarPubMed
Chinen, A., Matsumoto, Y. & Kawamura, S. (2005). Reconstitution of ancestral green visual pigments of zebrafish and molecular mechanism of their spectral differentiation. Molecular Biology and Evolution 22, 1001–1010.CrossRefGoogle ScholarPubMed
Damjanovic, I., Byzov, A.L., Bowmaker, J.K., Gacic, Z., Utina, I.A., Maximova, E.M., Mickovic, B. & Andjus, R.K. (2005). Photopic vision in eels: Evidence of colour discrimination. Annual NY Academy of Science 1048, 69–84.CrossRefGoogle Scholar
Douglas, R.H. (2001). The ecology of teleost fish visual pigments: A good example of sensory adaptation to the environment? In Ecology of Sensing, eds. Barth, F.G. & Schmid, A., pp. 215–235. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Gordon, J., Shapley, R.M. & Kaplan, E. (1978). The eel retina. Receptor classes and spectral mechanisms. Journal of General Physiology 71, 123–138.CrossRefGoogle ScholarPubMed
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G. & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509–528.CrossRefGoogle ScholarPubMed
Hárosi, F.I. (1994). An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34, 1359–1367.CrossRefGoogle ScholarPubMed
Hawryshyn, C.W., Arnold, M.G., Chaisson, D.J. & Martin, P.C. (1989). The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri). Visual Neuroscience 2, 247–254.CrossRefGoogle ScholarPubMed
Hess, M., Melzer, R.R. & Smola, U. (1998). The photoreceptors of Muraena helena and Ariosoma balearicum: A comparison of multiple bank retinae in anguilliform eels (Teleostei). Zoologischer Anzeiger 237, 127–137.Google Scholar
Hope, A.J., Partridge, J.C. & Hayes, P.K. (1998). Switch in rod opsin gene expression in the European eel, Anguilla anguilla (L.). Proceedings of the Royal Society B: Biological Sciences 265, 869–874.CrossRefGoogle ScholarPubMed
Liebman, P.A. & Entine, G. (1964). Sensitive low-light-level microspectrophotometer: Detection of photosensitive pigments of retinal cones. Journal of the Optical Society of America A 54, 1451–1459.CrossRefGoogle ScholarPubMed
Lyall, A.H. (1957). Cone arrangement in teleost retinae. Quarterly Journal of Microscopical Science 98, 189–201.Google Scholar
Lythgoe, J.N. (1979). The Ecology of Vision. Oxford: Oxford University Press.Google Scholar
Mollon, J.D., Bowmaker, J.K. & Jacobs, G.H. (1984). Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proceedings of the Royal Society B: Biological Sciences 222, 373–399.Google Scholar
Omura, Y., Tsuzuki, K., Sugiura, M., Uematsu, K. & Tsukamoto, K. (2003). Rod cells proliferate in the eel retina throughout life. Fish Science 69, 924–928.CrossRefGoogle Scholar
Omura, Y., Uematsu, K., Tachiki, H., Furukawa, K. & Satoh, H. (1997). Cone cells appear also in the retina of eel larvae. Fish Science 63, 1052–1053.CrossRefGoogle Scholar
Parry, J.W.L. & Bowmaker, J.K. (2000). Visual pigment reconstitution in intact goldfish retina using synthetic retinaldehyde isomers. Vision Research 40, 2241–2247.CrossRefGoogle ScholarPubMed
Parry, J.W.L., Carleton, K.L., Spady, T., Carboo, A., Hunt, D.M. & Bowmaker, J.K. (2005). Mix and match color vision: Tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Current Biology 15, 1734–1739.CrossRefGoogle ScholarPubMed
Partridge, J.C. & Cummings, M.E. (1999). Adaptations of visual pigments to the aquatic environment. In Adaptive Mechanisms in the Ecology of Vision, eds. Archer, S.N., Djamgoz, M.B.A, Loew, E.R., Partridge, J.C. & Valerga, S., pp. 251–283. Dordrecht: Kluwer.CrossRefGoogle Scholar
Spady, T.C., Parry, J.W.L., Robinson, P.R., Hunt, D.M., Bowmaker, J.K. & Carleton, K.L. (2006). Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Molecular Biology and Evolution 23, 1538–1547.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
Tesch, F.W. (1977). The Eel. London: Chapman and Hall.CrossRefGoogle Scholar
Whitmore, A.V. & Bowmaker, J.K. (1989). Seasonal variation in cone sensitivity and short-wave absorbing visual pigments in the rudd, Scardinius erythrophthalmus. Journal of Comparative Physiology A 166, 103–115.CrossRefGoogle Scholar
Wood, P. & Partridge, J.C. (1993). Opsin substitution induced in retinal rods of the eel (Anguilla anguilla (L.)): A model for G-protein-linked receptors. Proceedings of the Royal Society B: Biological Sciences 254, 227–232.Google Scholar
Wood, P., Partridge, J.C. & de Grip, W.J. (1992). Rod visual pigment changes in the elver of the eel Anguilla anguilla (L.) measured by microspectrophotometry. Journal of Fish Biology 41, 601–611.CrossRefGoogle Scholar
Yokoyama, S. (2000). Molecular evolution of vertebrate visual pigments. Progress in Retina Eye Research 19, 385–419.CrossRefGoogle ScholarPubMed