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The Evolution of Invertebrate Photopigments and Photoreceptors

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Evolution of Visual and Non-visual Pigments

Part of the book series: Springer Series in Vision Research ((SSVR,volume 4))

Abstract

The advent of new tools in genetics, labeling, and imaging has led to a revolution in the ability to investigate the genetic and cellular evolution of invertebrate photoreceptor pigments and cells. All opsins, invertebrate and vertebrate, derive from a common ancestral G-protein-coupled receptor, whose descendants form four distinct groups (one of which, the “cnidops,” is strictly limited to invertebrates). Today’s invertebrate opsins associate with a bewildering assortment of G-proteins and often have unusual properties, including functional bistability and occasionally the capacity to act as photoisomerases for visual pigment chromophores. In this chapter, we review our state of knowledge of how invertebrate opsins—the proteins underlying all visual pigments—have evolved and become functionally specialized as well as how the photoreceptive cells in which they are housed have diversified from a common ancestor—or ancestors—early in animal evolution.

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References

  • Ali MA, editor. Photoreception and vision in invertebrates. New York: Plenum Press; 1984.

    Google Scholar 

  • Alvarez CE. On the origins of arrestin and rhodopsin. BMC Evol Biol. 2008;8:222.

    PubMed  PubMed Central  Google Scholar 

  • Angueyra JM, Pulido C, Malagón G, Nasi E, Gomez M. Melanopsin-expressing amphioxus photoreceptors transduce light via a phospholipase-C signaling cascade. PLoS One. 2012;7:e29813.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Applebury ML, Antoch MP, Baxter LC, Chun LLY, Falk JD, Farhangfar F, et al. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron. 2000;27:513–23.

    PubMed  CAS  Google Scholar 

  • Arendt D. Evolution of eyes and photoreceptor cell types. Int J Dev Biol. 2003;47:563–71.

    PubMed  Google Scholar 

  • Arendt D, Wittbrodt J. Reconstructing the eyes of Urbilateria. Philos Trans R Soc Lond B Biol Sci. 2001;356:1545–63.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science. 2004;306:869–71.

    PubMed  CAS  Google Scholar 

  • Arendt D, Hausen H, Purschke G. The “division of labour” model of eye evolution. Philos Trans R Soc Lond B Biol Sci. 2009;364:2809–17.

    PubMed  PubMed Central  Google Scholar 

  • Arikawa K, Scholten DGW, Kinoshita M, Stavenga DG. Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zoolog Sci. 1999a;16:17–24.

    Google Scholar 

  • Arikawa K, Mizuno S, Scholten DGW, Minoshita M, Seki T, Kitamoto J, Stavenga DG. An ultraviolet absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio. Vision Res. 1999b;39:1–8.

    PubMed  CAS  Google Scholar 

  • Arikawa K, Mizuno S, Kinoshita K. Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of the butterfly Papilio xuthus. J Neurosci. 2003;23:4527–32.

    PubMed  CAS  Google Scholar 

  • Autrum H, editor. Handbook of sensory physiology, v. 7, part 6A, Invertebrate photoreceptors. Berlin: Springer; 1979.

    Google Scholar 

  • Autrum H, editor. Handbook of sensory physiology, v. 7, part 6B, Invertebrate visual centers and behavior I. Berlin: Springer; 1981a.

    Google Scholar 

  • Autrum H, editor. Handbook of sensory physiology, v. 7, part 6C, Invertebrate visual centers and behavior II. Berlin: Springer; 1981b.

    Google Scholar 

  • Backfisch B, Rajan VBV, Fischer RM, Lohs C, Arboleda E, Tessmar-Raible K, et al. Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution. Proc Natl Acad Sci U S A. 2013;110:193–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bailes HJ, Lucas RJ. Human melanopsin forms a pigment maximally sensitive to blue light (λmax ≈ 479 nm) supporting activation of Gq/11 and Gi/o signaling cascades. Proc Biol Sci. 2013;280:20122987.

    PubMed  PubMed Central  Google Scholar 

  • Bellingham J, Morris AG, Hunt DM. The rhodopsin gene of the cuttlefish Sepia officinalis: sequence and spectral tuning. J Exp Biol. 1998;201:2299–306.

    PubMed  CAS  Google Scholar 

  • Bernard GD. Dark-processes following photoconversion of butterfly rhodopsins. Biophys Struct Mech. 1983;9:277–86.

    CAS  Google Scholar 

  • Briscoe AD. Functional diversification of Lepidopteran opsins following gene duplication. Mol Biol Evol. 2001;18:2270–9.

    PubMed  CAS  Google Scholar 

  • Briscoe AD. Homology modeling suggests a functional role for parallel amino acid substitutions between bee and butterfly red- and green-sensitive opsins. Mol Biol Evol. 2002;19:983–6.

    PubMed  CAS  Google Scholar 

  • Briscoe AD, Chittka L. The evolution of color vision in insects. Annu Rev Entomol. 2001;46:471–510.

    PubMed  CAS  Google Scholar 

  • Brown PK, Brown PS. Visual pigments of the octopus and cuttlefish. Nature. 1958;162:1288–90.

    Google Scholar 

  • Chintapalli VR, Wang J, Dow JA. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet. 2007;39:715–20.

    PubMed  CAS  Google Scholar 

  • Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, et al. The ecoresponsive genome of Daphnia pulex. Science. 2011;331:555–61.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cronin TW, Goldsmith TH. Quantum efficiency and photosensitivity of the rhodopsin-metarhodopsin conversion in crayfish photoreceptors. Photochem Photobiol. 1982;36: 447–54.

    PubMed  CAS  Google Scholar 

  • Cronin TW, Goldsmith TH. Dark regeneration of rhodopsin in crayfish photoreceptors. J Gen Physiol. 1984;84:63–81.

    PubMed  CAS  Google Scholar 

  • Cronin TW, Marshall NJ, Caldwell RL. The intrarhabdomal filters in the retinas of mantis shrimps. Vision Res. 1994;34:279–91.

    PubMed  CAS  Google Scholar 

  • Döring C, Gosda J, Tessmar-Raible K, Hausen H, Arendt D, Purschke G. Evolution of clitellate phaosomes from rhabdomeric photoreceptor cells of polychaetes—a study in the leech Helobdella robusta (Annelida, Sedentaria, Clitellata). Front Zool. 2013;10:52.

    PubMed  PubMed Central  Google Scholar 

  • Dorlöchter M, Klemeit M, Stieve H. Immunological demonstration of Gq-protein in Limulus photoreceptors. Vis Neurosci. 1997;14:287–92.

    PubMed  Google Scholar 

  • Eakin RM. Evolutionary significance of photoreceptors: in retrospect. Am Zool. 1979;19: 647–53.

    Google Scholar 

  • Eakin RM. Structure of invertebrate photoreceptors. In: Dartnall HJA (ed). Handbook of sensory physiology, v. 7, part 1. Berlin: Springer; 1972. p. 625-684.

    Google Scholar 

  • Fain GL, Hardie R, Laughlin SB. Phototransduction and the evolution of photoreceptors. Curr Biol. 2010;20:R114–124.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Feuda R, Hamilton SC, McInerney JO, Pisani D. Metazoan opsin evolution reveals a simple route to animal vision. Proc Natl Acad Sci U S A. 2012;109:18868–72.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Fredriksson R, Lagerström MC, Lundin L-G, Schiöth HB. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol. 2003;63:1256–72.

    PubMed  CAS  Google Scholar 

  • Frentiu FD, Bernard GD, Sison-Mangus MP, Van Zandt BA, Briscoe AD. Gene duplication is an evolutionary mechanism for expanding spectral diversity in the long-wavelength photopigments of butterflies. Mol Biol Evol. 2007;24:2016–28.

    PubMed  CAS  Google Scholar 

  • Friedrich M, Chen R, Daines B, Bao R, Caravas J, Rai PK, Zagmajster M, Peck SB. Phototransduction and clock gene expression in the troglobiont beetle Ptomaphagus hirtus of Mammoth cave. J Exp Biol. 2011;214:3532–41.

    PubMed  CAS  Google Scholar 

  • Goldsmith TH. Evolutionary tinkering with visual photoreception. Vis Neurosci. 2013;30:21–37.

    PubMed  Google Scholar 

  • Gomez M, Nasi E. Antagonists of the cGMP-gated conductance of vertebrate rods block the photocurrent in scallop ciliary photoreceptors. J Physiol. 1997;500:367–78.

    PubMed  PubMed Central  Google Scholar 

  • Gomez M, Nasi E. Light transduction in invertebrate hyperpolarizing photoreceptors: possible involvement of a Go-regulated guanylate cyclase. J Neurosci. 2000;20:5254–63.

    PubMed  CAS  Google Scholar 

  • Gomez M, Angueyra JM, Nasi E. Light-transduction in melanopsin-expressing photoreceptors of Amphioxus. Proc Natl Acad Sci U S A. 2009;106:9081–6.

    Google Scholar 

  • Gotow T, Nishi T, Kijima H. Single K+ channels closed by light and opened by cyclic GMP in molluscan extra-ocular photoreceptor cells. Brain Res. 1994;662:268–72.

    PubMed  CAS  Google Scholar 

  • Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, et al. The developmental transcriptome of Drosophila melanogaster. Nature. 2011;471:473–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hall MD, Hoon MA, Ryba NJ, Pottinger JD, Keen JN, Saibil HR, et al. Molecular cloning and primary structure of squid (Loligo forbesi) rhodopsin, a phospholipase C-directed G-protein-linked receptor. Biochem J. 1991;274:35–40.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hara T, Hara R. New photosensitive pigment found in the retina of the squid Ommastrephes. Nature. 1965;206:1331–4.

    PubMed  CAS  Google Scholar 

  • Hara T, Hara R. Regeneration of squid retinochrome. Nature. 1968;214:573–5.

    Google Scholar 

  • Hara T, Hara R. Cephalopod retinochrome. In: Dartnall HJA, editor. Handbook of sensory physiology, Photochemistry of vision, vol. VII, Part I. Berlin: Springer; 1972. p. 720–46.

    Google Scholar 

  • Hara T, Hara R. Distribution of rhodopsin and retinochrome in the squid retina. J Gen Physiol. 1976;67:791–805.

    PubMed  CAS  Google Scholar 

  • Hara-Nishimura I, Kondo M, Nishimura M, Hara R, Hara T. Cloning and nucleotide sequence of cDNA for rhodopsin of the squid Todarodes pacificus. FEBS Lett. 1993;317:5–11.

    PubMed  CAS  Google Scholar 

  • Hargrave PA, McDowell JH, Curtis DR, Wang JK, Juszczak E, Fong S-L, et al. The structure of bovine rhodopsin. Biophys Struct Mech. 1983;9:235–44.

    PubMed  CAS  Google Scholar 

  • Heath-Heckman EAC, Peyer SM, Whistler CA, Apicella MA, Goldman WE, McFall-Ngai MJ. Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-vibrio symbiosis. MBio. 2013; 4(2):e00167.

    Google Scholar 

  • Henze MJ, Dannenhauer K, Kohler M, Labhart T, Gesemann M. Opsin evolution and expression in arthropod compound eyes and ocelli: insights from the cricket Gryllus bimaculatus. BMC Evol Biol. 2012;12:163.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hering L, Henze MJ, Kohler M, Kelber A, Bleidorn C, Leschke M, et al. Opsins in Onychophora (velvet worms) suggest a single origin and subsequent diversification of visual pigments in arthropods. Mol Biol Evol. 2012;29:3451–8.

    Google Scholar 

  • Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, et al. G protein-coupled receptors in Anopheles gambiae. Science. 2002;298:176–8.

    PubMed  CAS  Google Scholar 

  • Holland LZ, Albalat R, Azumi K, Benito-Gutiérrez È, Blow MJ, Bronner-Fraser M, et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 2008;18:1100–11.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hubbard R, St. George RCC. The rhodopsin system of the squid. J Gen Physiol. 1958;41:501–28.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hunt DM, Wilkie SE, Bowmaker JK, Poopalasundaram S. Vision in the ultraviolet. Cell Mol Life Sci. 2001;58:1583–98.

    PubMed  CAS  Google Scholar 

  • Izutsu M, Zhou J, Sugiyama Y, Nishimura O, Aizu T, Toyoda A, et al. Genome features of “dark-fly”, a Drosophila line reared long-term in a dark environment. PLoS One. 2012;7:e33288.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jékely G, Colombelli J, Hausen H, Guy K, Stelzer E, Nédélec F, et al. Mechanism of phototaxis in marine zooplankton. Nature. 2008;456:395–9.

    PubMed  Google Scholar 

  • Kashiyama K, Seki T, Numata H, Goto SG. Molecular characterization of visual pigments in Branchiopoda and the evolution of opsins in Arthropoda. Mol Biol Evol. 2009;26:299–311.

    PubMed  CAS  Google Scholar 

  • Katagiri N, Terakita A, Schchida Y, Katagiri Y. Demonstration of a rhodopsin-retinochrome system in the stalk eye of a marine gastropod, Onchidium, by immunohistocytochemistry. J Comp Neurol. 2001;433:380–9.

    PubMed  CAS  Google Scholar 

  • Katti C, Kempler K, Porter ML, Legg A, Gonzalez R, Garcia-Rivera E, et al. Opsin co-expression in Limulus photoreceptors: differential regulation by light and a circadian clock. J Exp Biol. 2010;213:2589–601.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kistenpfennig, CR. Rhodopsin and cryptochrome—circadian photoreception in Drosophila. Ph.D. dissertation. Department of Neurobiology and Genetics, Julius-Maximilians-Universität Würzburg. 2012; 151 pp.

    Google Scholar 

  • Knox BE, Salcedo E, Mathiesz K, Schaefer J, Chou W-H, Chadwell LV, et al. Heterologous expression of Limulus rhodopsin. J Biol Chem. 2003;278:40493–502.

    PubMed  CAS  Google Scholar 

  • Kojima D, Terakita A, Ishikawa T, Tsukahara Y, Maeda A, Shichida Y. A Novel Go-mediated phototransduction cascade in scallop visual cells. J Biol Chem. 1997;272:22979–82.

    PubMed  CAS  Google Scholar 

  • Koyanagi M, Terakita A. Gq-coupled rhodopsin subfamily composed of invertebrate visual pigment and melanopsin. Photochem Photobiol. 2008;84:1024–30.

    PubMed  CAS  Google Scholar 

  • Koyanagi M, Terakita A, Kubokawa K, Shichida Y. Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis and all-trans retinals as their chromophores. FEBS Lett. 2002;531:525–8.

    PubMed  CAS  Google Scholar 

  • Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr Biol. 2005;15:1065–9.

    PubMed  CAS  Google Scholar 

  • Koyanagi M, Nagata T, Katoh K, Yamashita S, Tokunaga F. Molecular evolution of arthropod color vision deduced from multiple opsin genes of jumping spiders. J Mol Evol. 2008a;66: 130–7.

    PubMed  CAS  Google Scholar 

  • Koyanagi M, Takano KI, Tsukamoto H, Ohtsu K, Tokunaga F, Terakita A. Jellyfish vision starts with cAMP signaling initiated by opsin-G cascade. Proc Natl Acad Sci U S A. 2008b;105:15576–80.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Koyanagi M, Takada E, Nagata T, Tsukamoto H, Terakita A. Homologs of vertebrate Opn3 potentially serve as a light sensor in nonphotoreceptive tissue. Proc Natl Acad Sci U S A. 2013;110:4998–5003.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kozmik Z, Ruzickova J, Jonasova K, Matsumoto Y, Vopalensky P, Kozmikova I, et al. Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc Natl Acad Sci U S A. 2008;105:8989–93.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kusakabe T, Kusakabe R, Kawakami I, Satou Y, Satoh N, Tsuda M. Ci-opsin1, a vertebrate-type opsin gene, expressed in the larval ocellus of the ascidian Ciona intestinalis. FEBS Lett. 2001;506:69–72.

    PubMed  CAS  Google Scholar 

  • Leys SP, Cronin TW, Degnan BM, Marshall NJ. Spectral sensitivity in a sponge larva. J Comp Physiol A. 2002;188:199–202.

    Google Scholar 

  • Liu J, Ward A, Gao J, Dong Y, Nishio N, Inada H, et al. C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nat Neurosci. 2010;13: 715–22.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Martin VJ. Photoreceptors of cnidarians. Can J Zool. 2002;80:1703–22.

    CAS  Google Scholar 

  • Mason B, Schmale M, Gibbs P, Miller MW, Wang Q, Levay K, et al. Evidence for multiple phototransduction pathways in a reef-building coral. PLoS One. 2012;7(12):e50371.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mäthger LM, Roberts SB, Hanlon RT. Evidence for distributed light sensing in the skin of cuttlefish, Sepia officinalis. Biol Lett. 2010;6:600–3.

    PubMed  PubMed Central  Google Scholar 

  • Matsui W, Seidou M, Uchiyama I, Sekiya N, Yoshihara K, Kito Y. 4-Hydroxyretinal, a new visual pigment chromophore found in the bioluminescent squid, Watasenia scintillans. Biochim Biophys Acta. 1988;966:370–4.

    PubMed  CAS  Google Scholar 

  • Michinomae M, Masuda H, Seidou M, Kito Y. Structural basis for wavelength discrimination in the banked retina of the firefly squid Watasenia scintillans. J Exp Biol. 1994;193:1–12.

    PubMed  Google Scholar 

  • Montell C. Drosophila visual transduction. Trends Neurosci. 2012;35:356–63.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Morris A, Bowmaker JK, Hunt DM. The molecular basis of a spectral shift in the rhodopsins of two species of squid from different photic environments. Proc Biol Sci. 1993;254:233–40.

    PubMed  CAS  Google Scholar 

  • Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Stalleicken J, Dirks P, et al. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc Natl Acad Sci U S A. 2004;101:14294–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Murakami M, Kouyama T. Crystal structure of squid rhodopsin. Nature. 2008;453:363–7.

    PubMed  CAS  Google Scholar 

  • Musio C, Santillo S, Taddei-Ferretti C, Robles LJ, Vismara R, Barsanti L, et al. First identification and localization of a visual pigment in Hydra (Cnidaria Hydrozoa). J Comp Physiol A. 2001;187:79–81.

    PubMed  CAS  Google Scholar 

  • Nagata T, Koyanagi M, Tsukamoto H, Terakita A. Identification and characterization of a protostome homologue of peropsin from a jumping spider. J Comp Physiol A. 2010;196:51–9.

    CAS  Google Scholar 

  • Nathans J, Hogness DS. Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell. 1983;34:807–14.

    PubMed  CAS  Google Scholar 

  • Nilsson D-E. The evolution of eyes and visually guided behaviour. Philos Trans R Soc Lond B Biol Sci. 2009;364:2833–47.

    PubMed  PubMed Central  Google Scholar 

  • Nilsson D-E. Eye evolution and its functional basis. Vis Neurosci. 2013;30:5–20.

    PubMed  PubMed Central  Google Scholar 

  • Nobes C, Baverstock J, Saibil H. Activation of the GTP-binding protein Gq by rhodopsin in squid photoreceptors. Biochem J. 1992;287:545–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nordström K, Wallen R, Seymour J, Nilsson D-E. A simple visual system without neurons in jellyfish larvae. Proc Biol Sci. 2003;270:2349–54.

    PubMed  PubMed Central  Google Scholar 

  • O’Tousa JE, Baehr W, Martin RL, Hirsh J, Pak WL, Applebury ML. The Drosophila ninaE gene encodes an opsin. Cell. 1985;40:839–50.

    PubMed  Google Scholar 

  • Ooka S, Katow T, Yaguchi S, Yaguchi J, Katow H. Spatiotemporal expression pattern of an encephalopsin orthologue of the sea urchin Hemicentrotus pulcherrimus during early development, and its potential role in larval vertical migration. Dev Growth Differ. 2010;52:195–207.

    PubMed  CAS  Google Scholar 

  • Ovchinnikov YA, Abdulaev NG, Feigina MY, Artamonov ID, Zdotarev AS, Miroshnikov AI, et al. The complete amino acid sequence of visual rhodopsin. Bioorg Khim. 1982;8:1011–4.

    CAS  Google Scholar 

  • Ovchinnikov Y, Abdulaev N, Zolotarev A, Artamonov I, Bespalov I, Dergachev A, et al. Octopus opsin amino acid sequence deduced from cDNA. FEBS Lett. 1988;232:69–72.

    PubMed  CAS  Google Scholar 

  • Ozaki K, Terakita A, Hara R, Hara T. Rhodopsin and retinochrome in the retina of a marine gastropod, Conomulex luhuanus. Vision Res. 1986;26:691–705.

    PubMed  CAS  Google Scholar 

  • Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, et al. Crystal structure of rhodopsin: A G protein-coupled receptor. Science. 2000;289:739–45.

    PubMed  CAS  Google Scholar 

  • Partch CL, Sancar A. Photochemistry and photobiology of cryptochrome blue-light photopigments: the search for a photocycle. Photochem Photobiol. 2005;81:1291–304.

    PubMed  CAS  Google Scholar 

  • Passamaneck YJ, Martindale MQ. Evidence for a phototransduction cascade in an early brachiopod embryo. Integr Comp Biol. 2013;53:17–26.

    PubMed  CAS  Google Scholar 

  • Passamaneck YJ, Furchheim N, Hejnol A, Martindale MQ, Lüter C. Ciliary photoreceptors in the cerebral eyes of a protostome larva. Evodevo. 2011;2:6.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pepe IM, Cugnoli C. Isolation and characterization of a water-soluble photopigment from honeybee compound eye. Vision Res. 1980;20:97–102.

    PubMed  CAS  Google Scholar 

  • Pichaud F, Briscoe A, Desplan C. Evolution of color vision. Curr Opin Neurobiol. 1999;9:622–7.

    PubMed  CAS  Google Scholar 

  • Plachetzki DC, Degnan BM, Oakley TH. The origins of novel protein interactions during animal opsin evolution. PLoS One. 2007;2(10):e1054.

    PubMed  PubMed Central  Google Scholar 

  • Plachetzki DC, Fong CR, Oakley TH. The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway. Proc R Soc B. 2010;277:1963–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Plachetzki DC, Fong CR, Oakley TH. Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biol. 2012;10:17.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Porter ML, Cronin TW, McClellan DA, Crandall KA. Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins. Mol Biol Evol. 2007;24:253–68.

    PubMed  CAS  Google Scholar 

  • Porter ML, Bok M, Robinson PR, Cronin TW. Molecular diversity of visual pigments in Stomatopoda (Crustacea). Vis Neurosci. 2009;26:255–66.

    PubMed  Google Scholar 

  • Porter ML, Blasic JR, Bok MJ, Cameron EG, Pringle T, Cronin TW, et al. Shedding new light on opsin evolution. Proc Biol Sci. 2012;297:3–14.

    Google Scholar 

  • Porter ML, Speiser DI, Zaharoff AK, Caldwell RL, Cronin TW, Oakley TH. The evolution of complexity in the visual systems of stomatopods: Insights from transcriptomics. Integr Comp Biol. 2013;53:39–49.

    PubMed  CAS  Google Scholar 

  • Raible F, Tessmar-Raible K, Arboleda E, Kaller T, Bork P, Arendt D, et al. Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. Dev Biol. 2006;300:461–75.

    PubMed  CAS  Google Scholar 

  • Rajkumar P, Rollmann SM, Cook TA, Layne JE. Molecular evidence for color discrimination in the Atlantic sand fiddler crab, Uca pugilator. J Exp Biol. 2010;213:4240–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ramirez MD, Speiser DI, Pankey MS, Oakley TH. Understanding the dermal light sense in the context of integrative photoreceptor cell biology. Vis Neurosci. 2011;28:265–79.

    PubMed  Google Scholar 

  • Rivera AS, Pankey MS, Plachetzki DC, Villacorta C, Syme AE, Serb JM, Omilian AR, Oakley TH. Gene duplication and the origins of morphological complexity in pancrustacean eyes, a genomic approach. BMC Evol Biol. 2010;10:123.

    PubMed  PubMed Central  Google Scholar 

  • Rivera AS, Ozturk N, Fahey B, Plachetzki DC, Degnan BM, Sancar A, Oakley TH. Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin. J Exp Biol. 2012;215:1278–86.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sakamoto K, Hisatomi O, Tokunaga F, Eguchi E. Two opsins from the compound eye of the crab Hemigrapsus sanguineus. J Exp Biol. 1996;199:441–50.

    PubMed  CAS  Google Scholar 

  • Salcedo E, Huber A, Henrich S, Chadwell LV, Chou W-H, Paulsen R, Britt SG. Blue- and green-absorbing visual pigments of Drosophila: Ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsins. J Neurosci. 1999;19:10716–26.

    PubMed  CAS  Google Scholar 

  • Salcedo E, Zheng L, Phistry M, Bagg EE, Britt SG. Molecular basis for ultraviolet vision in invertebrates. J Neurosci. 2003;23:10873–6.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Salcedo E, Farrell DM, Zheng L, Phistry M, Bagg EE, Britt SG. The green-absorbing Drosophila Rh6 visual pigment contains a blue-shifting amino acid substitution that is conserved in vertebrates. J Biol Chem. 2009;284:5717–22.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Salvini-Plawen LV, Mayr E. On the evolution of photoreceptors and eyes. In: Hecht MK, Steere WC, Wallace B, editors. Evolutionary biology, vol. 10. New York: Plenum; 1972. p. 207–63.

    Google Scholar 

  • Santillo S, Orlando P, De Petrocellis L, Cristino L, Guglielmotti V, Musio C. Evolving visual pigments: hints from the opsin-based proteins in a phylogenetically old “eyeless” invertebrate. Biosystems. 2006;86:3–17.

    PubMed  CAS  Google Scholar 

  • Satoh AK, Ready DF. Arrestin1 mediates light-dependent rhodopsin endocytosis and cell survival. Curr Biol. 2005;15:1722–33.

    PubMed  CAS  Google Scholar 

  • Sauman I, Briscoe AD, Zhu H, Shi D, Froy O, Stalleicken J, et al. Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron. 2005;46:457–67.

    PubMed  CAS  Google Scholar 

  • Schnitzler CE, Pang K, Powers ML, Reitzel AM, Ryan FJ, Simmons D, et al. Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biol. 2012;10:107.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Schwemer J. Renewal of visual pigment in photoreceptors of the blowfly. J Comp Physiol A. 1984;154:535–54.

    CAS  Google Scholar 

  • Schwemer J, Pepe IM, Paulsen R, Cugnoli C. Light-induced trans-cis isomerization of retinal by a protein from honeybee retina. J Comp Physiol A. 1984;154:549–54.

    CAS  Google Scholar 

  • Seidou M, Sugahara M, Uchiyama K, Hiraki H, Hamanaka T, Michinomae M, et al. On the three visual pigments in the retina of the firefly squid Watasenia scintillans. J Comp Physiol A. 1990;166:769–73.

    Google Scholar 

  • Seki T. Metaretinochrome in membranes as an effective donor of 11-cis retinal for the synthesis of squid rhodopsin. J Gen Physiol. 1984;84:49–62.

    PubMed  CAS  Google Scholar 

  • Serb JM, Porath-Krause AJ, Pairett AN. Uncovering a gene duplication in photoreceptive protein, opsin, in scallops (Bivalvia: Pectinidae). Integr Comp Biol. 2013;53:68–77.

    PubMed  CAS  Google Scholar 

  • Smith WC, Goldsmith TH. The role of retinal photoisomerase in the visual cycle of the honeybee. J Gen Physiol. 1991a;97:143–65.

    PubMed  CAS  Google Scholar 

  • Smith WC, Goldsmith TH. Cellular localization of retinal photoisomerase in the compound eye of the honeybee (Apis mellifera). Vis Neurosci. 1991b;7:237–49.

    PubMed  CAS  Google Scholar 

  • Smith WC, Freidman MA, Goldsmith TH. Retinoids in the lateral eye of Limulus: evidence for a retinal photoisomerase. Vis Neurosci. 1992;8:329–36.

    PubMed  CAS  Google Scholar 

  • Smith WC, Price DA, Greenberg RM, Batelle B-A. Opsins from the lateral eyes and ocelli of the horseshoe crab, Limulus polyphemus. Proc Natl Acad Sci U S A. 1993;90:6150–4.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Smith WC, Greenberg RM, Calman BG, Hendrix MM, Hutchinson L, Donoso LA, Battelle B-A. Isolation and expression of an arrestin cDNA from the horseshoe crab lateral eye. J Neurochem. 1995;64:1–13.

    PubMed  CAS  Google Scholar 

  • Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, et al. The genome of the sea urchin Strongylocentrotus purpuratus. Science. 2006;314:941–52.

    PubMed  Google Scholar 

  • Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashina T, et al. The Trichoplax genome and the nature of placozoans. Nature. 2008;454:955–60.

    PubMed  CAS  Google Scholar 

  • Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, et al. The cry b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell. 1998;95:681–92.

    PubMed  CAS  Google Scholar 

  • Stavenga DG. On visual pigment templates and the spectral shape of invertebrate rhodopsins and metarhodopsins. J Comp Physiol A. 2010;196:869–78.

    CAS  Google Scholar 

  • Su CY, Luo DG, Terakita A, Shichida Y, Liao HW, Kazmi MA, et al. Parietal-eye phototransduction components and their potential evolutionary implications. Science. 2006;311:1617–21.

    PubMed  CAS  Google Scholar 

  • Suga H, Schmid V, Gehring WJ. Evolution and functional diversity of jellyfish opsins. Curr Biol. 2008;18:51–5.

    PubMed  CAS  Google Scholar 

  • Suzuki T, Narito K, Yoshihara K, Nagai K, Kito Y. Phosphatidyl inositol-phospholipase C in squid photoreceptor membrane is activated by stable metarhodopsin via GTP-binding protein, Gq. Vision Res. 1995;35:1011–7.

    PubMed  CAS  Google Scholar 

  • Takeuchi T, Kawashima T, Koyanagi R, Gyoja F, Tanaka M, Ikuta T, et al. Draft genome of the pearl oyster Pinctada fucata: A platform for understanding bivalve biology. DNA Res. 2012;19:117–30.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Terakita A. The opsins. Genome Biol. 2005;6:213.

    PubMed  PubMed Central  Google Scholar 

  • Terakita A, Hara R, Hara T. Retinal-binding protein as a shuttle for retinal in the rhodopsin-retinochrome system of the squid visual cells. Vision Res. 1989;29:639–52.

    PubMed  CAS  Google Scholar 

  • Terakita A, Yamashita T, Shichida Y. Highly conserved glutamic acid in the extracellular IV-V loop in rhodopsins acts as the counterion in retinochrome, a member of the rhodopsin family. Proc Natl Acad Sci U S A. 2000;97:14263–7.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Terakita A, Tsukamoto H, Koyanagi M, Sugahara M, Yamashita T, Shichida Y. Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin. J Neurochem. 2008;105:883–90.

    PubMed  CAS  Google Scholar 

  • Tong D, Rozas NS, Oakley TH, Mitchell J, Colley NJ, McFall-Ngai MJ. Evidence for light perception in a bioluminescent organ. Proc Natl Acad Sci U S A. 2009;106:9836–41.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Townson SM, Chang BSW, Salcedo E, Chadwell LV, Pierce NE, Britt SG. Honeybee blue- and ultraviolet-sensitive opsins: cloning, heterologous expression in Drosophila, and physiological characterization. J Neurosci. 1998;18:2412–22.

    PubMed  CAS  Google Scholar 

  • Tsukamoto H, Terakita A. Diversity and functional properties of bistable pigments. Photochem Photobiol Sci. 2010;9:1435–43.

    PubMed  CAS  Google Scholar 

  • Ullrich-Lüter E, Dupont S, Arboleda E, Hausen H, Arnone MI. Unique system of photoreceptors in sea urchin tube feet. Proc Natl Acad Sci U S A. 2011;108:8367–72.

    PubMed  PubMed Central  Google Scholar 

  • Vanfleteren JR. A monophyletic line of evolution: Ciliary induced photoreceptor membranes. In: Westfall JA, editor. Visual cells in evolution. New York: Raven; 1982. p. 107–36.

    Google Scholar 

  • Vanfleteren JR, Coomans A. Photoreceptor evolution and phylogeny. J Zool Syst Evol Res. 1976;14:157–69.

    Google Scholar 

  • Velarde RA, Sauer CD, Walden KKO, Fahrbach SE, Robertson HM. Pteropsin: a vertebrate like non-visual opsin expressed in the honey bee brain. Insect Biochem Mol Biol. 2005;35: 1367–77.

    PubMed  CAS  Google Scholar 

  • Vopalensky P, Pergner J, Liegertova M, Benito-Gutierrez E, Arendt D, Kozmik Z. Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate retina. Proc Natl Acad Sci U S A. 2012;38:15383–8.

    Google Scholar 

  • Wakakuwa M, Terakita A, Koyanagi M, Stavenga DG, Shichida Y, Arikawa K. Evolution and mechanism of spectral tuning of blue-absorbing visual pigments in butterflies. PLoS One. 2010;5:e15015.

    PubMed  PubMed Central  Google Scholar 

  • Wald G, Hubbard R. Visual pigment of a decapod crustacean: the lobster. Nature. 1957;180:278–80.

    PubMed  CAS  Google Scholar 

  • Wang X, Wang T, Jiao Y, von Lintig J, Montell C. Requirement for an enzymatic visual cycle in Drosophila. Curr Biol. 2010;20:93–102.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Warrant E, Nilsson D-E. Invertebrate vision. Cambridge: Cambridge University Press; 2006.

    Google Scholar 

  • Westfall JA, Kinnamon JC. A second sensory-motor-interneuron with neurosecretory granules in Hydra. J Neurocytol. 1978;7:365–79.

    PubMed  CAS  Google Scholar 

  • Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN. Light-avoidance-mediating photoreceptors tile the Drosophila larva body wall. Nature. 2010;468:921–6.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yau K-W, Hardie RC. Phototransduction motifs and variations. Cell. 2009;139:246–64.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yoshida R, Kusakabe T, Kamatani M, Daitoh M, Tsuda M. Central nervous system-specific expression of G protein alpha subunits in the ascidian Ciona intestinalis. Zoolog Sci. 2002;19:1079–88.

    PubMed  CAS  Google Scholar 

  • Zhan S, Merlin C, Boore JL, Reppert SM. The Monarch butterfly genome yields insights into long-distance migration. Cell. 2011;147:1171–85.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature. 2012;490:49–54.

    PubMed  CAS  Google Scholar 

  • Zhukovsky EA, Robinson PR, Oprian DD. Transducin activation by rhodopsin without a covalent bond to 11-cis-retinal chromophore. Science. 1991;252:558–60.

    Google Scholar 

  • Zuker CS, Cowman AF, Rubin GM. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell. 1985;40:851–8.

    PubMed  CAS  Google Scholar 

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Cronin, T.W., Porter, M.L. (2014). The Evolution of Invertebrate Photopigments and Photoreceptors. In: Hunt, D., Hankins, M., Collin, S., Marshall, N. (eds) Evolution of Visual and Non-visual Pigments. Springer Series in Vision Research, vol 4. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-4355-1_4

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