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Evolutionary tinkering with visual photoreception

Published online by Cambridge University Press:  06 March 2012

TIMOTHY H. GOLDSMITH*
Affiliation:
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut
*
*Address correspondence and reprint requests to: Timothy H. Goldsmith, Department of Molecular, Cellular, and Developmental Biology, Yale University, PO Box 208103, New Haven, CT 06520-8103. E-mail: [email protected]

Abstract

Eyes have evolved many times, and arthropods and vertebrates share transcription factors for early development. Moreover, the photochemistry of vision in all eyes employs an opsin and the isomerization of a retinoid from the 11-cis to the all-trans configuration. The opsins, however, have associated with several different G proteins, initiating hyperpolarizing and depolarizing conductance changes at the photoreceptor membrane. Beyond these obvious instances of homology, much of the evolutionary story is one of tinkering, producing a great variety of morphological forms and variation within functional themes. This outcome poses a central issue in the convergence of evolutionary and developmental biology: what are the heritable features in the later stages of development that give natural selection traction in altering phenotypic outcomes? This paper discusses some results of evolutionary tinkering where this question arises and, in some cases, where the reasons for particular outcomes and the role of adaptation may not be understood. Phenotypic features include: the exploitation of microvilli in rhabdomeric photoreceptors for detecting the plane of polarized light; different instances of retinoid in the visual pigment; examples of the many uses of accessory pigments in tuning the spectral sensitivity of photoreceptors; selection of opsins in tuning sensitivity in aquatic environments; employing either reflection or refraction in the optics of compound eyes; the multiple ways of constructing images in compound eyes; and the various ways of regenerating 11-cis retinals to maintain visual sensitivity. Evolution is an irreversible process, but tinkering may recover some lost functions, albeit by new mutational routes. There is both elegance and intellectual coherence to the natural processes that produce such variety and functional complexity. But marginalizing the teaching of evolution in public education is a continuing social and political problem that contributes to the reckless capacity of humans to alter the planet without trying to understand how nature works.

Type
Perspective
Copyright
Copyright © Cambridge University Press 2012

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References

Abmad, S.T., Natochin, M., Barren, B., Artemyev, N.O. & O’Tousa, J.E. (2006). Heterologous expression of bovine rhodopsin in Drosophila photoreceptor cells. Investigative Ophthmology and Visual Science 47, 37223728.Google Scholar
Amemiya, T. (1975). Electron microscopic and cytochemical study on paraboloid glycogen of the accessory cone of the chick retina. Histochemistry 43, 185192.CrossRefGoogle Scholar
Arendt, D. (2003). Evolution of eyes and photoreceptor cell types. The International Journal of Developmental Biology 47, 563571.Google ScholarPubMed
Berkman, M.B. & Plutzer, E. (2011). Defeating creationism in the courtroom, but not in the classroom. Science 331, 404405.CrossRefGoogle Scholar
Bernard, G.D. (1983). Bleaching of rhabdoms in eyes of intact butterflies. Science 219, 6971.CrossRefGoogle ScholarPubMed
Bernstein, P.S., Law, W.C. & Rando, R.R. (1987). Biochemical characterization of the retinoid isomerase system of the eye. The Journal of Biological Chemistry 262, 1684816857.CrossRefGoogle ScholarPubMed
Bhagavatula, P., Claudianos, C., Ibbotson, M. & Srinivasan, M. (2009). Edge detection in landing budgerigars (Melopsittacus undulatus). PLoS One 4, e7301.CrossRefGoogle ScholarPubMed
Bowmaker, J.K., Heath, L.A., Wilkie, S.E. & Hunt, D.M. (1997). Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Research 37, 21832194.CrossRefGoogle ScholarPubMed
Braitenberg, V. (1967). Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Experimental Brain Research 3, 271298.CrossRefGoogle ScholarPubMed
Briscoe, A.D. & Chittka, L. (2001). The evolution of color vision in insects. Annual Review of Entomology 46, 471510.CrossRefGoogle ScholarPubMed
Britt, L.L., Loew, E.R. & McFarland, W.N. (2001). Visual pigments in the early life stages of Pacific Northwest marine fishes. The Journal of Experimental Biology 204, 25812587.CrossRefGoogle ScholarPubMed
Bruno, M.S., Barnes, S.N. & Goldsmith, T.H. (1977). The visual pigment and visual cycle of the lobster, Homarus. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 120, 123142.CrossRefGoogle Scholar
Butcher, E. (1938). The structure of the retina of Fundulus heteroclitus and the regions of the retina associated with the different chromatophoric responses. The Journal of Experimental Zoology 79, 275297.CrossRefGoogle Scholar
Campenhausen, M.V. & Kirschfeld, K. (1998). Spectral sensitivity of the accessory optic system of the pigeon. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 183, 16.CrossRefGoogle Scholar
Carleton, K.L., Spady, T.C., Streelman, J.T., Kidd, M.R., McFarland, W.N. & Loew, E.R. (2008). Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biology 6, 22.CrossRefGoogle ScholarPubMed
Cheadle, S.W. & Zeki, S. (2011). Masking within and across visual dimensions: Psychophysical evidence for perceptual segregation of color and motion. Visual Neuroscience 28, 445451.CrossRefGoogle ScholarPubMed
Collin, S.P., Davies, W.L., Hart, N.S. & Hunt, D.S. (2009). The evolution of early vertebrate photoreceptors. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 29252940.CrossRefGoogle ScholarPubMed
Cronin, T.W., Caldwell, R.L. & Marshall, J. (2001). Tunable colour vision in a mantis shrimp. Nature 411, 547548.CrossRefGoogle Scholar
Cronin, T.W. & Goldsmith, T.H. (1984). Dark regeneration of rhodopsin in crayfish photoreceptors. The Journal of General Physiology 84, 6381.CrossRefGoogle ScholarPubMed
Cronin, T.W., Jarvilehto, M., Weckstrom, M. & Lall, A.B. (2000). Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae). Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 186, 112.CrossRefGoogle ScholarPubMed
Cummins, D.R. & Goldsmith, T.H. (1981). Cellular identification of the violet receptor in the crayfish eye. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 142, 199202.CrossRefGoogle Scholar
Cuthill, I.C., Partridge, J.C., Bennett, A.T.D., Church, S.C., Hart, N.S. & Hunt, S. (2000). Ultraviolet vision in birds. Advances in the Study of Behavior 29, 159214.CrossRefGoogle Scholar
Darwin, C. (1859). On the Origin of Species by Means of Natural Selection. London: John Murray. Facsimile of the First Edition, Harvard University Press, Cambridge, (1964).Google Scholar
Daumer, K. (1956). Reizmetrische Untersuchung des Farbensehens der Bienen. Zeitschrift für vegleichende Physiologie 38, 413478.CrossRefGoogle Scholar
Eguchi, E. (1965). Rhabdom structure and receptor potentials in single crayfish retinular cells. Journal of Cellular and Comparative Physiology 66, 411430.CrossRefGoogle ScholarPubMed
Exner, S. (1891). The Physiology of the Compound Eyes of Insects and Crustaceans. Translated and annotated by R.C. Hardie, Springer-Verlag, Berlin (1989).Google Scholar
Fang, M., Li, J., Wai, S.M., Kwong, W.H., Kung, L.S. & Yew, D.T. (2005). Retinal twin cones or retinal double cones in fish: Misnomer or different morphological forms? The International Journal of Neuroscience 115, 981987.CrossRefGoogle ScholarPubMed
Flamarique, I.N. & Hárosi, F.I. (2002). Visual pigments and dichroism of anchovy cones: A model system for polarization detection. Visiual Neuroscience 19, 467473.CrossRefGoogle Scholar
Flamarique, I.N., Hawryshyn, C.W. & Hárosi, F.I. (1998). Double-cone internal reflection as a basis for polarization detection in fish. Journal of the Optical Society of America. A, Optics, Image Science, and Vision 15, 349358.CrossRefGoogle Scholar
Frederiksen, R., Crouch, R.K., Nickle, B., Chakrabarti, K.S., Oprian, D., Koutalos, Y., Boyer, N.P. & Cornwall, M.C. (2012). Increased rate of pigment regeneration and dark adaptation in rod photoreceptors containing 11-cis 4-OH rhodopsin. (submitted for publication).Google Scholar
Frentiu, F.D., Bernard, G.D., Sison-Mangus, M.P., Brower, A.V.Z. & Briscoe, A.D. (2007). Gene duplication is an evolutionary mechanism for expanding spectral diversity in the long-wavelength photopigments of butterflies. Molecular Biology and Evolution 24, 20162028.CrossRefGoogle ScholarPubMed
Fukushi, T. (1994). Colour perception of single and mixed monochromatic lights in the blowfly Lucilia cuprina. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 175, 1522.Google Scholar
Gärtner, W., Ullrich, D. & Vogt, K. (1991). Quantum yield of CHAPSO-solubilized rhodopsin and 3-hydroxyretinal containing bovine opsin. Photochemistry and Photobiology 54, 10471055.CrossRefGoogle ScholarPubMed
Goldsmith, T.H. (1975). The polarization sensitivity-dichroic absorption paradox in arthropod photoreceptors. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R., pp. 392409. Berlin, Germany: Springer-Verlag.CrossRefGoogle Scholar
Goldsmith, T.H. (2006). What birds see. Scientific American 295, 6975.CrossRefGoogle ScholarPubMed
Goldsmith, T.H. & Butler, B.K. (2005). Color vision of the budgerigar. (Melopsittacus undulatus): Hue matches, tetrachromacy, and intensity discrimination. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 191, 933951.CrossRefGoogle ScholarPubMed
Goldsmith, T.H., Collins, J.S. & Licht, S. (1984). The cone oil droplets of avian retinas. Vision Research 24, 16611671.CrossRefGoogle ScholarPubMed
Goldsmith, T.H. & Warner, L.T. (1964). Vitamin A in the vision of insects. The Journal of General Physiology 47, 433441.CrossRefGoogle ScholarPubMed
Goldsmith, T.H. & Wehner, R. (1977). Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. The Journal of General Physiology 70, 453490.CrossRefGoogle ScholarPubMed
Halder, G., Callaerts, P. & Gehring, W.J. (1995). Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 17881792.CrossRefGoogle ScholarPubMed
Hara, T. & Hara, R. (1973). Isomerization of retinal catalyzed by retinochrome in the light. Nature 242, 3943.Google Scholar
Hara, T. & Hara, R. (1976). Distribution of rhodopsin and retinochrome in the squid retina. The Journal of General Physiology 67, 791805.CrossRefGoogle ScholarPubMed
Hardie, R.C. (1984). Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 154, 157165.CrossRefGoogle Scholar
Hardie, R.C. (1986). The photoreceptor array in the dipteran retina. Trends in Neurosciences 9, 419423.CrossRefGoogle Scholar
Hawryshyn, C.W. & Bolger, A.E. (1990). Spatial orientation of trout to partially polarized light. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 167, 691697.Google Scholar
Hofstee, C.A. (1996). The Ca2+ homeostasis of the photoreceptor cell of Drosophila studied with the pupil mechanism. Thesis, University of Gronigen. Cited in Stavenga and Hardie (2011).Google Scholar
Hope, A.J., Partridge, J.C., Dulai, K.S. & Hunt, D.M. (1997). Mechanisms of wavelength tuning in the rod opsins of deep-sea fishes. Proceedings of the Royal Society of London. Series B, Biological Sciences 264, 155163.CrossRefGoogle ScholarPubMed
Horváth, G., Clarkson, E.N.K. & Pix, W. (1997). Survey of modern counterparts of schizochroal trilobite eyes: Structural and functional similarities and differences. Historical Biology 12, 229263.CrossRefGoogle Scholar
Jacob, F. (1977). Evolution and tinkering. Science 196, 11611166.CrossRefGoogle ScholarPubMed
Jacobs, G.H. (2009). Evolution of colour vision in mammals. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 29572967.CrossRefGoogle ScholarPubMed
Kamermans, M. & Hawryshyn, C. (2011). Teliost polarization vision: How it might work and what it might be good for. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 366, 742756.CrossRefGoogle ScholarPubMed
Kirschfeld, K. (1967). Die Projektion der optische Umvelt auf das Raster der Rhabdomere im Komplexauge von Musca. Experimental Brain Research 3, 248270.CrossRefGoogle Scholar
Labhart, T. (1980). Specialized photoreceptors at the dorsal rim of the honeybee’s compound eye: Polarizational and angular sensitivity. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 141, 1930.CrossRefGoogle Scholar
Lee, M.S.Y., Jago, J.B., Garcia-Bellido, D.C., Edgecombe, G.D., Gehling, J.G. & Paterson, J.R. (2011). Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia. Nature 474, 631634.CrossRefGoogle ScholarPubMed
Liebman, P.A. & Granda, A.M. (1975). Super dense carotenoid spectra resolved in single cone oil droplets. Nature 253, 370372.CrossRefGoogle ScholarPubMed
Livingstone, M.S. &, Hubel, D.H. (1987) Psychophysical evidence for separate channels for the perception of form, color, movement and depth. The Journal of Neuroscience 7, 34163468.CrossRefGoogle ScholarPubMed
Loew, E.R. & Lythgoe, J.N. (1978). The ecology of cone pigments in teleost fishes. Vision Research 18, 715722.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. (1985). Cell coupling in double cones of the fish retina. Proceedings of the Royal Society of London. Series B, Biological Sciences 226, 211215.Google Scholar
Mata, N.L., Radu, R.A., Clemmons, R.S. & Travis, G.H. (2002). Isomerization and oxidation of vitamin A in cone-dominant retinas: A novel pathway for visual-pigment regeneration in daylight. Neuron 36, 6980.CrossRefGoogle ScholarPubMed
Matsui, S., Seidou, M., Uchiyama, I., Sekiya, N., Hiraki, K., Yoshihara, K. & Kito, Y. (1988). 4-Hydroxyretinal, a new visual pigment chromophore found in the bioluminescent squid, Watasenia scintillans. Biochimica et Biophysica Acta 966, 370374.CrossRefGoogle ScholarPubMed
Miller, J.L. & Korenbrot, J.I. (1993). Phototransduction and adaptation in rods, single cones, and twin cones of the striped bass retina: A comparative study. Visual Neuroscience 10, 653667.CrossRefGoogle ScholarPubMed
Moody, M.F. & Parriss, J.R. (1961). The discrimination of polarized light by Octopus: A behavioral and morphological study. Zeitschrift für vergleichende Physiologie 44, 268291.CrossRefGoogle Scholar
Mote, M.I. (1974). Polarization sensitivity: A phenomenon independent of stimulus intensity or state of adaptation in retinular cells of the crabs Carcinus and Callinectes. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 90, 389403.Google Scholar
Mussi, M., Haimberger, T.J. & Hawryshyn, C.W. (2005). Behavioural discrimination of polarized light in the damselfish Chromis viridis (family Pomacentridae). The Journal of Experimental Biology 208, 30373046.CrossRefGoogle ScholarPubMed
Nathans, J., Piantanida, R.I., Eddy, R.L., Shows, T.B. & Hogness, D.S. (1986). Molecular genetics of inherited variation in human color vision. Science 232, 203210.CrossRefGoogle ScholarPubMed
Neumeyer, C. (1992). Tetrachromatic color vision in goldfish: Evidence from color mixture experiments. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 171, 639649.Google Scholar
Nilsson, D.-E. (1988). A new type of imaging optics in compound eyes. Nature 332, 7678.CrossRefGoogle Scholar
Nilsson, D.-E. (2009). The evolution of eyes and visually guided behavior. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 28332847.CrossRefGoogle Scholar
Oberhauser, V., Voolstra, O., Bangert, A., von Lintig, J. & Vogt, K. (2008). NinaB combines carotenoid oxygenase and retinoid isomerase activity in a single polypeptide. Proceedings of the National Academy of Sciences of the United States of America 105, 1900019005.CrossRefGoogle Scholar
Ödeen, A. & Håstad, O. (2003). Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Molecular Biology and Evolution 20, 855861.CrossRefGoogle ScholarPubMed
Osorio, D. (1986). Ultraviolet sensitivity and spectral opponency in the locust. The Journal of Experimental Biology 122, 193208.CrossRefGoogle Scholar
Ozaki, K., Terakita, A., Hara, R. & Hara, T. (1986). Rhodopsin and retinochrome in the retina of a marine gastropod, Conomulex luhuanus. Vision Research 26, 691705.CrossRefGoogle ScholarPubMed
Pignatelli, V., Champ, C., Marshall, J. & Vorobyev, M. (2010). Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus. Biology Letters 6, 537539.CrossRefGoogle ScholarPubMed
Porter, M.L., Blasic, J.R., Bok, M.J., Cameron, E.G., Pringle, T., Cronin, T.W. & Robinson, P.R. (2012). Sheding new light on opsin evolution. Proceedings of the Royal Society of London. Series B, Biological Sciences 279, 314.Google Scholar
Qiu, X. & Arikawa, K. (2003). Polymorphism of red receptors: Sensitivity spectra of proximal photoreceptors in the small white butterfly Pieris rapae crucivora. The Journal of Experimental Biology 206, 27872793.CrossRefGoogle ScholarPubMed
Robinson, J., Schmitt, E.A., Hárosi, F.I., Reece, R.J. & Dowling, J.E. (1993). Zebrafish ultraviolet visual pigment: Absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the United States of America 90, 60096012.CrossRefGoogle ScholarPubMed
Schaerer, S. & Neumeyer, C. (1996). Motion detection in goldfish investigated with the optomotor response is ‘color blind’. Vision Research 36, 40254034.CrossRefGoogle ScholarPubMed
Schwemer, J. (1984). Renewal of visual pigment in photoreceptors of the blowfly. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 154, 535547.CrossRefGoogle Scholar
Schwemer, J., Pepe, I.M., Paulsen, R. & Cugnoli, C. (1984). Light-induced trans‑cis isomerization of retinal by a protein from honeybee retina. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 154, 549554.CrossRefGoogle Scholar
Seki, T. & Vogt, K. (1998). Evolutionary aspects of the diversity of visual pigment chromophores in the class Insecta. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 119, 5364.CrossRefGoogle Scholar
Shaw, S.R. (1969). Sense-cell structure and interspecies comparisons of polarized-light absorption in arthropod compound eyes. Vision Research 9, 10311040.CrossRefGoogle ScholarPubMed
Shimazaki, Y. & Eguchi, E. (1995). Light-dependent metabolic pathway of 3-hydroxyretinoids in the eye of the butterfly, Papilio xuthus. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 176, 661671.CrossRefGoogle Scholar
Smith, W.C., Freidman, M.A. & Goldsmith, T.H. (1992). Retinoids in the lateral eye of Limulus: Evidence for a retinal photoisomerase. Visual Neuroscience 8, 329336.CrossRefGoogle ScholarPubMed
Smith, W.C. & Goldsmith, T.H. (1990). Phyletic aspects of the distribution of 3-hydroxyretinal in the class Insecta. Journal of Molecular Evolution 30, 7284.CrossRefGoogle ScholarPubMed
Smith, W.C. & Goldsmith, T.H. (1991 a). The role of retinal photoisomerase in the visual cycle of the honeybee. The Journal of General Physiology 97, 143165.CrossRefGoogle ScholarPubMed
Smith, W.C. & Goldsmith, T.H. (1991 b). Cellular localization of retinal photoisomerase in the compound eye of the honeybee (Apis mellifera). Visual Neuroscience 7, 237249.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, 15381547.CrossRefGoogle ScholarPubMed
Srivastava, R. & Goldsmith, T.H. (1997). On the mechanism of isomerization of ocular retinoids by the crayfish Procambarus clarkii. The Journal of Experimental Biology 200, 625631.CrossRefGoogle ScholarPubMed
Srivastava, R., Lau, D. & Goldsmith, T.H. (1996). Formation and storage of 11- cis retinol in the eyes of lobster (Homarus) and crayfish (Procambarus). Visual Neuroscience 13, 215222.CrossRefGoogle ScholarPubMed
Stavenga, D.G. & Hardie, R.C. (2011). Metarhodopsin control by arrestin, light-filtering screening pigments, and visual pigment turnover in invertebrate microvillar photoreceptors. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 197, 227241.CrossRefGoogle ScholarPubMed
Townson, S.M., Chang, B.S.W., Salcedo, E., Chadwell, L.V., Pierce, N.E. & Britt, S.G. (1998). Honeybee blue- and ultraviolet-sensitive opsins: Cloning, heterologous expression in Drosophila, and physiological characterization. The Journal of Neuroscience 18, 24122422.CrossRefGoogle ScholarPubMed
Vogt, K. (1980). Die Spiegeloptik des Flusskrebsauges. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 135, 119.CrossRefGoogle Scholar
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. Bloomfield Hills, MI: Cranbrook Institute of Science. Reprinted 1963, New York: Hafner Publishing Company.Google Scholar
Wehner, R. & Bernard, G.D. (1993). Photoreceptor twist: A solution to the false-color problem. Proceedings of the National Academy of Sciences of the United States of America 90, 41324135.CrossRefGoogle Scholar
Yau, K.-W. & Hardie, R.C. (2009). Phototransduction motifs and variations. Cell 139, 246264.CrossRefGoogle ScholarPubMed
Yokoyama, S. & Radlwimmer, F.B. (2001). The molecular genetics of red and green color vision in vertebrates. Genetics 158, 16971710.CrossRefGoogle ScholarPubMed