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Understanding the dermal light sense in the context of integrative photoreceptor cell biology

Published online by Cambridge University Press:  08 July 2011

M. DESMOND RAMIREZ ,
DANIEL I. SPEISER ,
M. SABRINA PANKEY  and
TODD H. OAKLEY
M. DESMOND RAMIREZ
Affiliation:
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California
DANIEL I. SPEISER
Affiliation:
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California
M. SABRINA PANKEY
Affiliation:
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California
TODD H. OAKLEY*
Affiliation:
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California
*
*Address correspondence and reprint requests to: Todd H. Oakley, Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106. E-mail: [email protected]
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Abstract

While the concept of a dermal light sense has existed for over a century, little progress has been made in our understanding of the mechanisms underlying dispersed photoreception and the evolutionary histories of dispersed photoreceptor cells. These cells historically have been difficult to locate and positively identify, but modern molecular techniques, integrated with existing behavioral, morphological, and physiological data, will make cell identification easier and allow us to address questions of mechanism and evolution. With this in mind, we propose a new classification scheme for all photoreceptor cell types based on two axes, cell distribution (aggregated vs. dispersed) and position within neural networks (first order vs. high order). All photoreceptor cells fall within one of four quadrants created by these axes: aggregated/high order, dispersed/high order, aggregated/first order, or dispersed/first order. This new method of organization will help researchers make objective comparisons between different photoreceptor cell types. Using integrative data from four major phyla (Mollusca, Cnidaria, Echinodermata, and Arthropoda), we also provide evidence for three hypotheses for dispersed photoreceptor cell function and evolution. First, aside from echinoderms, we find that animals often use dispersed photoreceptor cells for tasks that do not require spatial vision. Second, although there are both echinoderm and arthropod exceptions, we find that dispersed photoreceptor cells generally lack morphological specializations that either enhance light gathering or aid in the collection of directional information about light. Third, we find that dispersed photoreceptor cells have evolved a number of times in Metazoa and that most dispersed photoreceptor cells have likely evolved through the co-option of existing phototransduction cascades. Our new classification scheme, combined with modern investigative techniques, will help us address these hypotheses in great detail and generate new hypothesis regarding the function and evolution of dispersed photoreceptor cells.

Keywords

Extraocular photoreceptorsNon-visual photoreceptionEvolutionPhototransductionInvertebrates
Type
Evolution and eye design
Information
Visual Neuroscience , Volume 28 , Issue 4 , July 2011 , pp. 265 - 279
Copyright
Copyright © Cambridge University Press 2011

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References

Adler, K. (1976). Extraocular photoreception in amphibians. Photochemistry and Photobiology 23, 275–298.CrossRefGoogle ScholarPubMed
Aizenberg, J., Tkachenko, A., Weiner, S., Addadi, L. & Hendler, G. (2001). Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412, 819–822.CrossRefGoogle ScholarPubMed
Arendt, D. (2003). Evolution of eyes and photoreceptor cell types. International Journal of Developmental Biology 47, 563–572.Google ScholarPubMed
Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A.W. & Wittbrodt, J. (2004). Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306, 869–871.CrossRefGoogle Scholar
Arendt, D. & Wittbrodt, J. (2001). Reconstructing the eyes of Urbilateria. Philosophical Transactions of the Royal Society B: Biological Sciences 356, 1545–1563.CrossRefGoogle ScholarPubMed
Arey, L. & Crozier, W. (1919). The sensory responses of Chiton. Journal of Experimental Zoology 29, 157–260.CrossRefGoogle Scholar
Arikawa, K. & Aoki, K. (1982). Response characteristics and occurrence of extraocular photoreceptors on lepidopteran genitalia. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 148, 483–489.CrossRefGoogle Scholar
Arikawa, K., Eguchi, E., Yoshida, A. & Aoki, K. (1980). Multiple extraocular photoreceptive areas on genitalia of butterfly Papilio xuthus. Nature 288, 700–702.CrossRefGoogle Scholar
Arikawa, K. & Miyako-Shimazaki, Y. (1996). Combination of physiological and anatomical methods for studying extraocular photoreceptors on the genitalia of the butterfly, Papilio xuthus. Journal of Neuroscience Methods 69, 75–82.CrossRefGoogle ScholarPubMed
Arikawa, K., Suyama, D. & Fujii, T. (1997). Hindsight by genitalia: Photo-guided copulation in butterflies. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 180, 295–299.CrossRefGoogle Scholar
Arikawa, K. & Takagi, N. (2001). Genital photoreceptors have crucial role in oviposition in Japanese yellow swallowtail butterfly, Papilio xuthus. Zoological Science 18, 175–179.CrossRefGoogle Scholar
Arvanitaki, A. & Chalazonitis, N. (1961). Excitatory and inhibitory processes initiated by light and infra-red radiations in single identifiable nerve cells. In Nervous Inhibition, ed. Florey, E. New York: Pergamon Press, 194–231.Google Scholar
Bagnara, J. & Obika, M. (1967). Light sensitivity of melanophores in neural crest explants. Experimentia 23, 155–157.CrossRefGoogle ScholarPubMed
Barber, V. & Wright, D. (1969). The fine structure of the eye and optic tentacle of the mollusc Cardium edule. Journal of Ultrastructure Research 26, 515–528.CrossRefGoogle ScholarPubMed
Bellingham, J., Morris, A. & Hunt, D. (1998). The rhodopsin gene of the cuttlefish Sepia officinalis: Sequence and spectral tuning. The Journal of Experimental Biology 201, 2299–2306.CrossRefGoogle ScholarPubMed
Blevins, E. & Johnsen, S. (2004). Spatial vision in the echinoid genus Echinometra. Journal of Experimental Biology 207, 4249–4253.CrossRefGoogle ScholarPubMed
Bolwig, N. (1946). Senses and sense organs of the anterior end of the house fly larvae. Dansk Naturhist for Kobenhavn Vidensk Meddel 109, 81–217.Google Scholar
Boyle, P. (1969). Rhabdomeric ocellus in a chiton. Nature 222, 895–896.CrossRefGoogle Scholar
Boyle, P. (1972). The aesthetes of chitons. Marine and Freshwater Behaviour and Physiology 1, 171–184.CrossRefGoogle Scholar
Brown, P. & Brown, P. (1958). Visual pigments of the octopus and cuttlefish. Nature 182, 1288–1290.CrossRefGoogle ScholarPubMed
Burke, R., Angerer, L., Elphick, M., Humphrey, G., Yaguchi, S., Kiyama, T., Liang, S., Mu, X., Agca, C. & Klein, W. (2006). A genomic view of the sea urchin nervous system. Developmental Biology 300, 434–460.CrossRefGoogle ScholarPubMed
Cashmore, A.R., Jarillo, J.A., Wu, Y. & Liu, D. (1999). Cryptochromes: Blue light receptors for plants and animals. Science 284, 760–765.CrossRefGoogle ScholarPubMed
Chono, K., Fujito, Y. & Ito, E. (2002). Non-ocular dermal photoreception in the pond snail Lymnaea stagnalis. Brain Research 951, 107–112.CrossRefGoogle ScholarPubMed
Chrachri, A. & Nelson, L. (2005). Whole-cell recording of light-evoked photoreceptor responses in a slice preparation of the cuttlefish retina. Visual Neuroscience 22, 359–370.CrossRefGoogle Scholar
Clark, E.D. & Kimeldorf, D.J. (1971). Behavioral reactions of the sea anemone, Anthopleura xanthogrammica, to ultraviolet and visible radiations. Radiation Research 45, 166–175.CrossRefGoogle ScholarPubMed
Cobb, J. & Hendler, G. (1990). Neurophysiological characterization of the photoreceptor system in a brittlestar, Ophiocoma wendtii (Echinodermata, Ophiuroidea). Comparative Biochemistry and Physiology A: Physiology 97, 329–333.CrossRefGoogle Scholar
Cobb, J. & Moore, A. (1986). Comparative studies on receptor structure in the brittlestar Ophiura ophiura. Journal of Neurocytology 15, 97–108.CrossRefGoogle ScholarPubMed
Cobb, C. & Williamson, R. (1998 a). Electrophysiology and innervation of the photosensitive epistellar body in the lesser octopus Eledone cirrhosa. The Biological Bulletin 195, 78–87.CrossRefGoogle ScholarPubMed
Cobb, C. & Williamson, R. (1998 b). Electrophysiology of extraocular photoreceptors in the squid Loligo forbesi (Cephalopoda: Loliginidae). Journal of Molluscan Studies 64, 111–117.CrossRefGoogle Scholar
Cobb, C.S., Williamson, R. & Pope, S.K. (1995). The responses of the epistellar photoreceptors to light and their effect on circadian rhythms in the lesser octopus, Eledone cirrhosa. Marine and Freshwater Behaviour and Physiology 26, 59–69.CrossRefGoogle Scholar
Cook, A. (1975). The withdrawal response of a freshwater snail (Lymnaea stagnalis L.). Journal of Experimental Biology 62, 783–796.CrossRefGoogle Scholar
Cowles, R. (1910). Stimuli produced by light and by contact with solid walls as factors in the behavior of ophiuroids. Journal of Experimental Biology 9, 387–416.Google Scholar
Crisp, M. (1972). Photoreceptive function of an epithelial receptor in Nassarius reticulatus [Gastropoda, Prosobranchia]. Journal of the Marine Biological Association of the United Kingdom 52, 437–442.CrossRefGoogle Scholar
Diggle, P. (2003). Statistical Analysis of Spatial Point Patterns. Arnold, London.Google Scholar
Dilly, P. & Wolken, J. (1973). Studies on the receptors in Ciona intestinalis. IV. The ocellus in the adult. Micron 4, 11–29.Google Scholar
Dörjes, J. (1968). Die Acoela (Turbellaria) der deutschen Nordseeküste und ein neues System der Ordnung. Zeitschrift fuer Zoologische Systematik und Evolutionsforschung 6, 56–452.CrossRefGoogle Scholar
Duivenboden, Y. (1982). Non-ocular photoreceptors and photo-orientation in the pond snail Lymnaea stagnalis (L.). Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 149, 363–368.CrossRefGoogle Scholar
Eakin, R. (1961). Photoreceptors in the amphibian frontal organ. Proceedings of the National Academy of Sciences 47, 1084–1088.CrossRefGoogle ScholarPubMed
Eakin, R. (1968). Evolution of photoreceptors. In Evolutionary Biology, Vol 2, eds. Dobzhansky, T., Hecht, M., and Steere, W., pp. 194–242. Appleton-Century-Crofts: New York.CrossRefGoogle Scholar
Eakin, R. (1972). Structure in invertebrate photoreceptors. In Handbook of Sensory Physiology, Vol. 7, ed. Dartnell, H.J., pp. 635–684. New York: Springer New York.Google Scholar
Eakin, R. & Brandenburger, J. (1967). Differentiation in eye of a pulmonate snail Helix aspersa. Journal of Ultrastructure Research 18, 391–421.CrossRefGoogle ScholarPubMed
Eakin, R. & Westfall, J.A. (1962). Fine structure of photoreceptors in Amphioxus. Journal of Ultrastructure Research 6, 531–539.CrossRefGoogle ScholarPubMed
Edwards, S., Charlie, N., Milfort, M., Brown, B., Gravlin, C., Knecht, J. & Miller, K. (2008). A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biology 6, 1715–1729.CrossRefGoogle ScholarPubMed
Fu, Y. & Yau, K.W. (2007). Phototransduction in mouse rods and cones. Pflügers Archiv: European Journal of Physiology 454, 805–819.CrossRefGoogle ScholarPubMed
Gabel, C.V., Gabel, H., Pavlichin, D., Kao, A., Clark, D.A. & Samuel, A.D.T. (2007). Neural circuits mediate electrosensory behavior in Caenorhabditis elegans. Journal of Neuroscience 27, 7586–7596.CrossRefGoogle ScholarPubMed
Gomez, M.P. & Nasi, E. (2000). Light Transduction in Invertebrate Hyperpolarizing Photoreceptors: Possible Involvement of a Go-Regulated Guanylate Cyclase. Journal of Neuroscience 20, 5254–5263.CrossRefGoogle ScholarPubMed
Gotow, T. (1975). Morphology and function of the photoexcitable neurones in the central ganglia of Onchidium verruculatum. Journal of Comparative Physiology A: Neuroethology 99, 139–152.CrossRefGoogle Scholar
Gotow, T. & Nishi, T. (2002). Light-dependent K channels in the mollusc Onchidium simple photoreceptors are opened by cGMP. Journal of General Physiology 120 (4): 581–597. doi:10.1085/jgp.20028619.CrossRefGoogle ScholarPubMed
Gotow, T. & Nishi, T. (2008). Simple photoreceptors in some invertebrates: Physiological properties of a new photosensory modality. Brain Research 1225, 3–16.CrossRefGoogle ScholarPubMed
Grancher, J. (1920). Note on the photic sensitivity of the chitons. The American Naturalist 54, 376–380.Google Scholar
Grueber, W., Jan, L. & Jan, Y. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867–2878.CrossRefGoogle ScholarPubMed
Hara, T. & Hara, R. (1980). Retinochrome and rhodopsin in the extraocular photoreceptor of the squid, Todarodes. The Journal of General Physiology 75, 1.CrossRefGoogle ScholarPubMed
Hardie, R. & Raghu, P. (2001). Visual Transduction in Drosophila. Nature. 413, 186–193.CrossRefGoogle ScholarPubMed
Hattar, S., Lucas, R.J., Mrosovsky, N., Thompson, S., Douglas, R., Hankins, M.W., Lem, J., Biel, M., Hofmann, F. & Foster, R.G. (2003). Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 75–81.CrossRefGoogle ScholarPubMed
Haug, G. (1933). Die Lichtreaktionen der Hydren (Chlorohydra viridissima und Pelmatohydra oligactis). Zeitschrift für Vergleichende Physiologie 19, 354–355.CrossRefGoogle Scholar
Heath, H. (1904). The larval eye of chitons. Proceedings of the Academy of Natural Sciences of Philadelphia 56, 257–259.Google Scholar
Hecht, S. (1919). Sensory equilibrium and dark adaptation in Mya arenaria. The Journal of General Physiology 1, 545–558.CrossRefGoogle ScholarPubMed
Hegemann, P. (2008). Algal sensory photoreceptors. Annual Review of Plant Biology 59, 167–189.CrossRefGoogle ScholarPubMed
Hendler, G. (1984). Brittlestar color-change and phototaxis (Echinodermata: Ophiuroidea: Ophiocomidae). Marine Ecology 5, 379–401.CrossRefGoogle Scholar
Hendler, G. & Byrne, M. (1987). Fine structure of the dorsal arm plate of Ophiocoma wendtii: Evidence for a photoreceptor system (Echinodermata, Ophiuroidea). Zoomorphology 107, 261–272.CrossRefGoogle Scholar
Hisano, N., Tateda, H. & Kuwabara, M. (1972 a). An electrophysiological study of the photo-excitative neurones of Onchidium verruculatum in situ. Journal of Experimental Biology 57, 661–671.CrossRefGoogle ScholarPubMed
Hisano, N., Tateda, H. & Kuwabara, M. (1972 b). Photosensitive neurones in the marine pulmonate mollusc Onchidium verruculatum. Journal of Experimental Biology 57, 651.CrossRefGoogle ScholarPubMed
Howard, L. (2008). Drosophilidae compound eye edit. Photo. http://commons.wikimedia.org/wiki/File:Drosophilidae_compound_eye_edit1.jpg.Google Scholar
Hyman, L. (1951). The Invertebrates: Acanthocephala, Aschelminthes, and Entoprocta, the Pseudocoelomate Bilateria, Vol. 3. McGraw-Hill, New York: London.Google Scholar
Hyman, L. (1967). The Invertebrates. Vol. VI. Mollusca I. Aplacophora, Polyplacophora, Monoplacophora, Gastropoda. The Coelomate Bilateria. McGraw-Hill, New York: London.Google Scholar
Jekely, G. (2009). Evolution of phototaxis. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 2795–2808.CrossRefGoogle ScholarPubMed
Johnsen, S. (1997). Identification and localization of a possible rhodopsin in the echinoderms Asterias forbesi (Asteroidea) and Ophioderma brevispinum (Ophiuroidea). The Biological Bulletin 193, 97–105.CrossRefGoogle ScholarPubMed
Kennedy, D. (1960). Neural photoreception in a lamellibranch mollusc. Journal of General Physiology 44, 277–299.CrossRefGoogle Scholar
Kennedy, D. (1963). Physiology of photoreceptor neurons in the abdominal nerve cord of the crayfish. The Journal of General Physiology 46, 551.CrossRefGoogle ScholarPubMed
Kojima, D., Terakita, A. & Ishikawa, T. (1997). A novel Go-mediated phototransduction cascade in scallop visual cells. Journal of Biological Chemistry 272, 22979–22982.CrossRefGoogle ScholarPubMed
Koyanagi, M., Kubokawa, K. & Tsukamoto, H. (2005). Cephalochordate melanopsin: Evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Current Biology 15, 1065–1069.CrossRefGoogle ScholarPubMed
Koyanagi, M., Takano, K., Tsukamoto, H. & Ohtsu, K. (2008). Jellyfish vision starts with cAMP signaling mediated by opsin-Gs cascade. Proceedings of the National Academy of Sciences 105, 15576–15580.CrossRefGoogle ScholarPubMed
Koyanagi, M., Terakita, A., Kubokawa, K. & Shichida, Y. (2002). Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis-and all-trans-retinals as their chromophores. FEBS Letters 531, 525–528.CrossRefGoogle ScholarPubMed
Kozmik, Z., Ruzickova, J. & Jonasova, K. (2008). Assembly of the cnidarian camera-type eye from vertebrate-like components. Proceedings of the National Academy of Sciences 105, 8989–8993.CrossRefGoogle ScholarPubMed
Kusakabe, T., Kusakabe, R., Kawakami, I., Satou, Y., Satoh, N. & Tsuda, M. (2001). Ci-opsin1, a vertebrate-type opsin gene, expressed in the larval ocellus of the ascidian Ciona intestinalis. FEBS Letters 506, 69–72.CrossRefGoogle ScholarPubMed
Kusakabe, T. & Tsuda, M. (2007). Photoreceptive systems in ascidians. Photochemistry and Photobiology 83, 248–252.CrossRefGoogle ScholarPubMed
Lacalli, T. (2004). Sensory systems in amphioxus: A window on the ancestral chordate condition. Brain Behavior and Evolution 64, 148–162.CrossRefGoogle ScholarPubMed
Land, M.F. & Nilsson, D.-E. (2002). Animal Eyes. Oxford University Press Oxford; Toronto.Google Scholar
Lesser, M.P., Carleton, K.L., Bottger, S.A., Barry, T.M. & Walker, C.W. (2011). Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6. Proceedings of the Royal Society B: Biological Sciences. doi:10.1098/rspb.2011.0336.CrossRefGoogle ScholarPubMed
Light, V. (1930). Photoreceptors in Mya arenaria, with special reference to their distribution, structure, and function. Journal of Morphology 49, 1–43.CrossRefGoogle Scholar
Liu, J., Ward, A., Gao, J., Dong, Y., Nishio, N., Inada, H., Kang, L., Yu, Y., Ma, D., Xu, T., Mori, I., Xie, Z. & Xu, X.Z. (2010). C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nature Neuroscience 13, 715–722.CrossRefGoogle Scholar
Lukowiak, K. & Jacklet, J. (1972). Habituation and dishabituation: Interactions between peripheral and central nervous systems in Aplysia. Science 178, 1306–1308.CrossRefGoogle ScholarPubMed
Mano, H. & Fukada, Y. (2007). A median third eye: Pineal gland retraces evolution of vertebrate photoreceptive organs. Photochemistry and Photobiology 83, 11–18.CrossRefGoogle ScholarPubMed
Marks, P. (1976). Nervous control of light responses in the sea anemone, Calamactis praelongus. Journal of Experimental Biology 65, 85–96.CrossRefGoogle ScholarPubMed
Martin, V. (2002). Photoreceptors of cnidarians. Canadian Journal of Zoology 80, 1703–1722.CrossRefGoogle Scholar
Mathger, L.M., Roberts, S.B. & Hanlon, R.T. (2010). Evidence for distributed light sensing in the skin of cuttlefish, Sepia officinalis. Biology Letters 6, 600–603.CrossRefGoogle ScholarPubMed
Mauro, A. (1977). Extra-ocular photoreceptors in cephalopods. Symposium of the Zoological Society of London 38, 287–308.Google Scholar
Millott, N. (1968). The dermal light sense. Symposia of the Zoological Society of London 23, 1–36.Google Scholar
Millott, N. (1975). The photosensitivity of echinoids. Advances in Marine Biology 13, 1–52.Google Scholar
Milne, L. & Milne, M. (1956). Invertebrate photoreceptors. In Radiation Biology, Vol. 3. ed. Hollaender, A. McGraw-Hill New York 621–692.Google Scholar
Miyako, Y., Arikawa, K. & Eguchi, E. (1993). Ultrastructure of the extraocular photoreceptor in the genitalia of a butterfly, Papilio xuthus. The Journal of Comparative Neurology 327, 458–468.CrossRefGoogle ScholarPubMed
Morton, J. (1960). The responses and orientation of the bivalve Lasaea rubra Montagu. Journal of the Marine Biological Association of the United Kingdom 39, 5–26.CrossRefGoogle Scholar
Mrabet, Y. (2008). Drosophila XY sex-chromosomes. Drawing. http://commons.wikimedia.org/wiki/File:Drosophila_XY_sex-determination.svg.Google Scholar
Nasi, E. & Del Pilar Gomez, M. (2009). Melanopsin-mediated light-sensing in amphioxus: A glimpse of the microvillar photoreceptor lineage within the deuterostomia. Communicative and Integrative Biology 2, 441–443.CrossRefGoogle ScholarPubMed
Nilsson, D. (1994). Eyes as optical alarm systems in fan worms and ark clams. Philosophical Transactions: Biological Sciences 346, 195–212.Google Scholar
Nilsson, D. (2009). The evolution of eyes and visually guided behaviour. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 2833–2847.CrossRefGoogle ScholarPubMed
Nishioka, R., Hagadorn, I. & Bern, H. (1962). Ultrastructure of the epistellar body of the octopus. Cell and Tissue Research 57, 406–421.Google ScholarPubMed
Nishioka, R., Yasumasu, I., Packard, A., Bern, H. & Young, J. (1966). Nature of vesicles associated with the nervous system of cephalopods. Cell and Tissue Research 75, 301–316.Google ScholarPubMed
Nordstrom, K., Wallen, R., Seymour, J. & Nilsson, D. (2003). A simple visual system without neurons in jellyfish larvae. Proceedings of the Royal Society B: Biological Sciences 270, 2349–2354.CrossRefGoogle ScholarPubMed
North, W.J. (1957). Sensitivity to light in the sea anemone Metridium senile (L.). The Journal of General Physiology 40, 715–733.CrossRefGoogle ScholarPubMed
North, W. & Pantin, C. (1958). Sensitivity to light in the sea-anemone Metridium senile (L): Adaptation and action spectra. Proceedings of the Royal Society of London 148, 385–396.Google Scholar
Ooka, S., Katow, T., Yaguchi, S., Yaguchi, J. & Katow, H. (2010). Spatiotemporal expression pattern of an encephalopsin orthologue of the sea urchin Hemicentrotus pulcherrimus during early development, and its potential role in larval vertical migration. Development, Growth & Differentiation 52, 195–207.CrossRefGoogle ScholarPubMed
Oshima, N. (2001). Direct reception of light by chromatophores of lower vertebrates. Pigment Cell Research 14, 312–319.CrossRefGoogle ScholarPubMed
Packard, A. & Brancato, D. (1993). Some responses of Octopus chro-matophores to light. Journal of Physiology 459, 429.Google Scholar
Panda, S., Sato, T., Castrucci, A., Rollag, M., Degrip, W., Hogenesch, J., Provencio, I. & Kay, S. (2002). Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298, 2213–2216.CrossRefGoogle ScholarPubMed
Pankey, S., Sunada, H., Horikoshi, T. & Sakakibara, M. (2010). Cyclic nucleotide-gated channels are involved in phototransduction of dermal photoreceptors in Lymnaea stagnalis. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 180, 1205–1211.CrossRefGoogle ScholarPubMed
Passano, L. & Mccullough, C. (1962). The light response and the rhythmic potentials of Hydra. Proceedings of the National Academy of Sciences of the United States of America 48, 1376–1382.CrossRefGoogle ScholarPubMed
Pearse, V.B. (1974). Modification of sea anemone behavior by symbiotic zooxanthellae: Expansion and contraction. Biological Bulletin 147, 641–651.CrossRefGoogle ScholarPubMed
Plachetzki, D.C., Fong, C.R. & Oakley, T.H. (2010). The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway. Proceedings of the Royal Society B: Biological Sciences 277, 1963–1969.CrossRefGoogle ScholarPubMed
Plachetzki, D.C., Degnan, BM. & Oakley, TH. (2007). The Origins of Novel Protein Interactions during Animal Opsin Evolution. PLoS ONE 2(10): e1054. doi:10.1371/journal.pone.0001054.CrossRefGoogle ScholarPubMed
Provencio, I., Rodriguez, I. & Jiang, G. (2000). A novel human opsin in the inner retina. Journal of Neuroscience 20, 600–605.CrossRefGoogle ScholarPubMed
Raible, F., Tessmar-Raible, K., Arboleda, E., Kaller, T., Bork, P., Arendt, D. & Arnone, M. (2006). Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. Developmental Biology 300, 461–475.CrossRefGoogle ScholarPubMed
Richter, S., Loesel, R., Purschke, G., Schmidt-Rhaesa, A., Scholtz, G., Stach, T., Vogt, L., Wanninger, A., Brenneis, G., Doering, C., Faller, S., Fritsch, M., Grobe, P., Heuer, C.M., Kaul, S., Moller, O.S., Mueller, C.H.G., Rieger, V., Rothe, B.H., Stegner, M.E.J. & Harzsch, S. (2010). Invertebrate neurophylogeny: Suggested terms and definitions for a neuroanatomical glossary. Frontiers in Zoology 7, 29.CrossRefGoogle ScholarPubMed
Röhlich, P., Aros, B. & Viragh, S. (1970). Fine structure of photoreceptor cells in the earthworm, Lumbricus terrestris. Cell and Tissue Research 104, 345–357.Google ScholarPubMed
Rubin, E.B., Shemesh, Y., Cohen, M., Elgavish, S., Robertson, H.M. & Bloch, G. (2006). Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Research 16, 1352–1365.CrossRefGoogle ScholarPubMed
Ruiz, M. & Anadon, R. (1991). Some considerations on the fine structure of rhabdomeric photoreceptors in the amphioxus, Branchiostoma lanceolatum (Cephalochordata). Journal für Hirnforschung 32, 159–164.Google ScholarPubMed
Rushforth, N., Burnett, A. & Maynard, R. (1963). Behavior in hydra: Contraction responses of Hydra pirardi to mechanical and light stimuli. Science 139, 760–761.CrossRefGoogle Scholar
Sakakibara, M., Aritaka, T., Iizuka, A., Suzuki, H., Horikoshi, T. & Lukowiak, K. (2005). Electrophysiological responses to light of neurons in the eye and statocyst of Lymnaea stagnalis. Journal of Neurophysiology 93, 493–507.CrossRefGoogle ScholarPubMed
Salvini-Plawen, L. & Mayr, E. (1977). On the evolution of photoreceptors and eyes. Evolutionary Biology 10, 207–253.Google Scholar
Sawyer, S., Dowse, H. & Shick, J. (1994). Neurophysiological correlates of the behavioral response to light in the sea anemone Anthopleura elegantissima. Biological Bulletin 186, 195–201.CrossRefGoogle ScholarPubMed
Shick, J. & Dykens, J.A. (1984). Photobiology of the symbiotic sea anemone Anthopleura elegantissima: Photosynthesis, respiration, and behavior under intertidal conditions. The Biological Bulletin 166, 608–619.CrossRefGoogle Scholar
Siddiqui, I. & Viglierchio, D. (1970). Ultrastructure of photoreceptors in the marine nematode Deontostoma californicum. Journal of Ultrastructure Research 32, 558–571.CrossRefGoogle ScholarPubMed
Singla, C. (1974). Ocelli of hydromedusae. Cell and Tissue Research 149, 413–429.CrossRefGoogle ScholarPubMed
Speiser, D.I., Eernisse, D.J. & Johnsen, S. (2011). A chiton uses aragonite lenses to form images. Current Biology 21, 665–670.CrossRefGoogle ScholarPubMed
Steven, D. (1963). The dermal light sense. Biological Reviews 38, 204–240.CrossRefGoogle ScholarPubMed
Stoll, C. (1972). Sensory systems involved in shadow response of Lymnaea stagnalis (L) as studied with use of habituation phenomena. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen Series C: Biological and Medical Sciences 75, 342–351.Google Scholar
Stoll, C. (1976). Extraocular photoreception in Lymnaea Stagnalis L. In Neurobiology of Invertebrates, Gastropoda Brain. ed. Salánki, J. Akadémiai Kiadó, location: Budapest pp 487–495Google Scholar
Su, C., Luo, D., Terakita, A., Shichida, Y., Liao, H., Kazmi, M., Sakmar, T. & Yau, K. (2006). Parietal-eye phototransduction components and their potential evolutionary implications. Science 311, 1617–1621.CrossRefGoogle ScholarPubMed
Suga, H., Schmid, V. & Gehring, W. (2008). Evolution and functional diversity of jellyfish opsins. Current Biology 18, 51–55.CrossRefGoogle ScholarPubMed
Tardent, P. & Frei, E. (1969). Reaction patterns of dark and light adapted Hydra to light stimuli. Cellular and Molecular Life Sciences 25, 265–267.CrossRefGoogle ScholarPubMed
Tarttelin, E., Bellingham, J., Hankins, M., Foster, R. & Lucas, R.J. (2003). Neuropsin (Opn5): A novel opsin identified in mammalian neural tissue. FEBS Letters 554, 410–416.CrossRefGoogle ScholarPubMed
Tong, D., Rozas, N., Oakley, T., Mitchell, J., Colley, N.J. & Mc Fall-Ngai, M.J. (2009). Evidence for light perception in a bioluminescent organ. Proceedings of the National Academy of Sciences 106, 9836–9841.CrossRefGoogle Scholar
Ullrich-Lüter, E.M. Dupont, S., Arboleda, E., Hausen, H., Arnone, MI. (2011). Unique system of photoreceptors in sea urchin tube feet. Proceedings of the National Academy of Sciences of the United States of America, 10.1073/pnas.1018495108.CrossRefGoogle ScholarPubMed
Ward, A., Liu, J., Feng, Z. & Xu, X. (2008). Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nature Neuroscience 11, 916–922.CrossRefGoogle ScholarPubMed
Watson, G. & Hessinger, D. (1989). Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243, 1589–1591.CrossRefGoogle Scholar
Watson, G. & Hessinger, D. (1994). Evidence for calcium channels involved in regulating nematocyst discharge. Comparative Biochemistry and Physiology 107, 473–481.CrossRefGoogle ScholarPubMed
Wiederhold, M. JR, , E.M. & Bell, A. (1973). Photoreceptor spike responses in the hardshell clam, Mercenaria mercenaria. Journal of General Physiology 61, 24–55.CrossRefGoogle ScholarPubMed
Wilkens, L. & Larimer, J. (1972). The CNS photoreceptor of crayfish: Morphology and synaptic activity. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 80, 389–407.CrossRefGoogle Scholar
Woodley, J. (1982). Photosensitivity in Diadema antillarum: Does it show scototaxis? In Echinoderms, Proceedings of the International Conference, Tampa Bay. ed. Lawrence, J.M., pp. 61: CRC Press A.A. Balkema, Rotterdam.Google Scholar
Xiang, Y., Yuan, Q., Vogt, N., Looger, L.L., Jan, L.Y. & Jan, Y.N. (2010). Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468, 921–926.CrossRefGoogle ScholarPubMed
Yamasu, T. & Yoshida, M. (1973). Electron microscopy on the photoreceptors of the anthomedusae and a scyphomedusa. Publications. Seto Marine Biological Laboratory, Kyoto University 20, 757–778.CrossRefGoogle Scholar
Yanase, T. & Sakamoto, S. (1965). Fine structure of the visual cells of the dorsal eye in molluscan Onchidium verruculatum. Zoological Magazine 74, 238–242.Google Scholar
Yerramilli, D. & Johnsen, S. (2010). Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). Journal of Experimental Biology 213, 249–255.CrossRefGoogle ScholarPubMed
Yoshida, M. (1979). Extraocular photoreception. In Handbook of Sensory Physiology, vol. 7, ed. Autrum, H., pp. 581–640. Berlin: Springer.Google Scholar
Zylstra, U. (1971). Distribution and ultrastructure of epidermal sensory cells in the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Netherlands Journal of Zoology 22, 283–298.CrossRefGoogle Scholar