1932

Abstract

Learning how complex traits like eyes originate is fundamental for understanding evolution. In this review, we first sketch historical perspectives on trait origins and argue that new technologies afford key new insights. Next, we articulate four open questions about trait origins. To address them, we define a research program to break complex traits into component parts and to study the individual evolutionary histories of those parts. By doing so, we can learn when the parts came together and perhaps understand why they stayed together. We apply this approach to five structural innovations critical for complex eyes and review the history of the parts of each of those innovations. Eyes evolved within animals by tinkering: creating new functional associations between genes that usually originated far earlier. Multiple genes used in eyes today had ancestral roles in stress responses. We hypothesize that photo-oxidative stress had a role in eye origins by increasing the chance that those genes were expressed together in places on animals where light was abundant.

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2015-12-04
2024-03-28
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Literature Cited

  1. Albalat R. 2012. Evolution of the genetic machinery of the visual cycle: a novelty of the vertebrate eye?. Mol. Biol. Evol. 29:1461–69 [Google Scholar]
  2. Alexandrou MA, Swartz BA, Matzke NJ, Oakley TH. 2013. Genome duplication and multiple evolutionary origins of complex migratory behavior in Salmonidae. Mol. Phylogenetics Evol. 69:3514–23 [Google Scholar]
  3. Arendt D. 2003. Evolution of eyes and photoreceptor cell types. Int. J. Dev. Biol. 47:563–71 [Google Scholar]
  4. Arendt D, Hausen H, Purschke G. 2009. The “division of labour” model of eye evolution. Philos. Trans. R. Soc. B. 364:2809–17 [Google Scholar]
  5. Asano M, Ito M. 1955. Biochemical studies on the octopus II pigments of the integument and ink sack of octopus. Tohoku J. Agric. Res. 6:147–58 [Google Scholar]
  6. Avelar GM, Schumacher RI, Zaini PA, Leonard G, Richards TA, Gomes SL. 2014. A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr. Biol. 24:111234–40 [Google Scholar]
  7. Bernan V, Filpula D, Herber W, Bibb M, Katz E. 1985. The nucleotide sequence of the tyrosinase gene from Streptomyces antibioticus and characterization of the gene product. Gene 37:101–10 [Google Scholar]
  8. Björn LO. 2007. Photobiology: The Science of Life and Light New York: Springer
  9. Björn LO. 2015. Photoactive proteins. Photobiology LO Björn 139–50 New York: Springer [Google Scholar]
  10. Blevins E, Johnsen S. 2004. Spatial vision in the echinoid genus Echinometra. J. Exp. Biol. 207:4249–53 [Google Scholar]
  11. Borovansky J, Riley PA. 2011. Melanins and Melanosomes: Biosynthesis, Biogenesis, Physiological and Pathological Functions Weinheim, Ger: Wiley
  12. Brown KT, Wiesel TN. 1959. Intraretinal recording with micropipette electrodes in the intact cat eye. J. Physiol. 149:537–62 [Google Scholar]
  13. Butenandt A. 1959. Wirkstoffe des Insektenreiches. Naturwissenschaften 46:461–71 [Google Scholar]
  14. Butenandt A, Schafer W, Neubert G. 1967. Constitution of ommines. Monatshefte Chemie 98:946–55 [Google Scholar]
  15. Carosa E, Kozmik Z, Rall JE, Piatigorsky J. 2002. Structure and expression of the scallop Ω-crystallin gene: evidence for convergent evolution of promoter sequences. J. Biol. Chem. 277:1656–64 [Google Scholar]
  16. Carvalho-Santos Z, Azimzadeh J, Pereira-Leal JB, Bettencourt-Dias M. 2011. Tracing the origins of centrioles, cilia, and flagella. J. Cell Biol. 194:2165–75 [Google Scholar]
  17. Chiou SH. 1988. A novel crystallin from octopus lens. FEBS Lett. 241:1–2261–64 [Google Scholar]
  18. Cunningham CW, Omland KE, Oakley TH. 1998. Reconstructing ancestral character states: a critical reappraisal. Trends Ecol. Evol. 13:9361–66 [Google Scholar]
  19. Darwin C. 1859. On the Origins of Species by Means of Natural Selection. London: Murray
  20. de Queiroz A. 1999. Do image-forming eyes promote evolutionary diversification?. Evolution 53:61654–64 [Google Scholar]
  21. DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK. 2007. β-Arrestins and cell signaling. Annu. Rev. Physiol. 69:1483–510 [Google Scholar]
  22. d'Ischia M, Wakamatsu K, Napolitano A, Briganti S, Garcia-Borron J-C. et al. 2013. Melanins and melanogenesis: methods, standards, protocols. Pigment Cell Melanoma Res. 26:616–33 [Google Scholar]
  23. Dubin RA, Wawrousek EF, Piatigorsky J. 1989. Expression of the murine αB-crystallin gene is not restricted to the lens. Mol. Cell. Biol. 9:31083–91 [Google Scholar]
  24. Eakin RM. 1965. Evolution of photoreceptors. Cold Spring Harbor Symp. Quant. Biol. 30:363–70 [Google Scholar]
  25. Eakin RM. 1979. Evolutionary significance of photoreceptors: in retrospect. Am. Zool. 19:2647–53 [Google Scholar]
  26. Esposito R, D'Aniello S, Squarzoni P, Pezzotti MR, Ristoratore F, Spagnuolo A. 2012. New insights into the evolution of metazoan tyrosinase gene family. PLOS ONE 7:e35731 [Google Scholar]
  27. Feuda R, Hamilton SC, McInerney JO, Pisani D. 2012. Metazoan opsin evolution reveals a simple route to animal vision. PNAS 109:4618868–72 [Google Scholar]
  28. Feuda R, Rota-Stabelli O, Oakley TH, Pisani D. 2014. The comb jelly opsins and the origins of animal phototransduction. Genome Biol. Evol. 6:1964–71 [Google Scholar]
  29. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:41531–45 [Google Scholar]
  30. Ganfornina MD, Sánchez D. 1999. Generation of evolutionary novelty by functional shift. Bioessays 21:5432–39 [Google Scholar]
  31. Gomez Mdel P, Espinosa L, Ramirez N, Nasi E. 2011. Arrestin in ciliary invertebrate photoreceptors: molecular identification and functional analysis in vivo. J. Neurosci. 31:51811–19 [Google Scholar]
  32. Granit R. 1941. Isolation of colour-sensitive elements in a mammalian retina. Acta Physiol. Scand. 2:93–109 [Google Scholar]
  33. Hara-Nishimura I, Matsumoto T, Mori H, Nishimura M, Hara R, Hara T. 1990. Cloning and nucleotide sequence of cDNA for retinochrome, retinal photoisomerase from the squid retina. FEBS Lett. 271:1–2106–10 [Google Scholar]
  34. Hardie RC. 2001. Phototransduction in Drosophila melanogaster. J. Exp. Biol. 204:Pt 203403–9 [Google Scholar]
  35. Hardie RC, Franze K. 2012. Photomechanical responses in Drosophila photoreceptors. Science 338:6104260–63 [Google Scholar]
  36. Heintzen C. 2012. Plant and fungal photopigments. WIREs Membr. Transp. Signal. 1:411–32 [Google Scholar]
  37. Hering L, Mayer G. 2014. Analysis of the opsin repertoire in the tardigrade Hypsibius dujardini provides insights into the evolution of opsin genes in panarthropoda. Genome Biol. Evol. 6:92380–91 [Google Scholar]
  38. Herranz S, Rodríguez JM, Bussink H-J, Sánchez-Ferrero JC, Arst HN Jr. et al. 2005. Arrestin-related proteins mediate pH signaling in fungi. PNAS 102:3412141–46 [Google Scholar]
  39. Hisatomi O, Tokunaga F. 2002. Molecular evolution of proteins involved in vertebrate phototransduction. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 133:4509–22 [Google Scholar]
  40. Ho SYW, Phillips MJ, Cooper A, Drummond AJ. 2005. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol. Biol. Evol. 22:71561–68 [Google Scholar]
  41. Hurst DT. 1980. An Introduction to the Chemistry and Biochemistry of Pyrimidines, Purines, and Pteridines New York: Wiley
  42. Ingolia TD, Craig EA. 1982. Four small Drosophila heat shock proteins are related to each other and to mammalian α-crystallin. PNAS 79:72360–64 [Google Scholar]
  43. Jablonski D. 1993. The tropics as a source of evolutionary novelty through geological time. Nature 364:6433142–44 [Google Scholar]
  44. Jablonski D. 2005. Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution. J. Exp. Zool. B Mol. Dev. Evol. 304:6504–19 [Google Scholar]
  45. Jékely G. 2010. Origin and early evolution of neural circuits for the control of ciliary locomotion. Proc. R. Soc. B 278:1707914–22 [Google Scholar]
  46. Jékely G, Arendt D. 2006. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 28:2191–98 [Google Scholar]
  47. Jékely G, Colombelli J, Hausen H, Guy K, Stelzer E. et al. 2008. Mechanism of phototaxis in marine zooplankton. Nature 456:395–99 [Google Scholar]
  48. Johnson J-LF, Leroux MR. 2010. cAMP and cGMP signaling: Sensory systems with prokaryotic roots adopted by eukaryotic cilia. Trends Cell Biol. 20:8435–44 [Google Scholar]
  49. Katagiri N, Terakita A, Shichida Y, Katagiri Y. 2001. Demonstration of a rhodopsin-retinochrome system in the stalk eye of a marine gastropod, onchidium, by immunohistochemistry. J. Comp. Neurol. 433:3380–89 [Google Scholar]
  50. Kayal E, Roure B, Philippe H, Collins AG, Lavrov DV. 2013. Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol. Biol. 13:5 [Google Scholar]
  51. Kim J, Suh H, Kim S, Kim K, Ahn C, Yim J. 2006. Identification and characteristics of the structural gene for the Drosophila eye colour mutant sepia, encoding PDA synthase, a member of the Omega class glutathione S-transferases. Biochem. J. 398:451–60 [Google Scholar]
  52. Klemenz R, Fröhli E, Steiger RH, Schäfer R, Aoyama A. 1991. αB-Crystallin is a small heat shock protein. PNAS 88:93652–56 [Google Scholar]
  53. Kojima D, Terakita A, Ishikawa T, Tsukahara Y, Maeda A, Shichida Y. 1997. A novel Go-mediated phototransduction cascade in scallop visual cells. J. Biol. Chem. 272:3722979–82 [Google Scholar]
  54. Koyanagi M, Takano K, Tsukamoto H, Ohtsu K, Tokunaga F, Terakita A. 2008. Jellyfish vision starts with cAMP signaling mediated by opsin-Gs cascade. PNAS 105:4015576–80 [Google Scholar]
  55. Krauss U, Minh BQ, Losi A, Gärtner W, Eggert T. et al. 2009. Distribution and phylogeny of light-oxygen-voltage-blue-light-signaling proteins in the three kingdoms of life. J. Bacteriol. 191:237234–42 [Google Scholar]
  56. Kronforst MR, Barsh GS, Kopp A, Mallet J, Monteiro A. et al. 2012. Unraveling the thread of nature's tapestry: the genetics of diversity and convergence in animal pigmentation. Pigment Cell Melanoma Res. 25:4411–33 [Google Scholar]
  57. Kusakabe TG, Takimoto N, Jin M, Tsuda M. 2009. Evolution and the origin of the visual retinoid cycle in vertebrates. Philos. Trans. R. Soc. B 364:2897–910 [Google Scholar]
  58. Lamb TD, Pugh EN Jr. 2004. Dark adaptation and the retinoid cycle of vision. Prog. Retin. Eye Res. 23:307–80 [Google Scholar]
  59. Land MF. 2000. Eyes with mirror optics. J. Opt. A Pure Appl. Opt. 2:R44–50 [Google Scholar]
  60. Land MF. 2012. The evolution of lenses. Ophthalmic Physiol. Opt. 32:6449–60 [Google Scholar]
  61. Land MF, Fernald RD. 1992. The evolution of eyes. Annu. Rev. Neurosci. 15:1–29 [Google Scholar]
  62. Land MF, Nilsson D-E. 2012. Animal Eyes Oxford, UK: Oxford Univ. Press
  63. Larusso ND, Ruttenberg BE, Singh AK, Oakley TH. 2008. Type II opsins: evolutionary origin by internal domain duplication?. J. Mol. Evol. 66:5417–23 [Google Scholar]
  64. Lindgren AR, Pankey MS, Hochberg FG, Oakley TH. 2012. A multi-gene phylogeny of Cephalopoda supports convergent morphological evolution in association with multiple habitat shifts in the marine environment. BMC Evol. Biol. 12:129 [Google Scholar]
  65. Linzen B. 1974. The tryptophan → ommochrome pathway in insects. Advances in Insect Physiology 10 JE Treherne 117–246 New York: Academic [Google Scholar]
  66. Mackin KA, Roy RA, Theobald DL. 2014. An empirical test of convergent evolution in rhodopsins. Mol. Biol. Evol. 31:185–95 [Google Scholar]
  67. Marazzi B, Ané C, Simon MF, Delgado-Salinas A, Luckow M, Sanderson MJ. 2012. Locating evolutionary precursors on a phylogenetic tree. Evolution 66:123918–30 [Google Scholar]
  68. Marmor MF, Martin LJ. 1978. 100 years of the visual cycle. Surv. Ophthalmol. 22:279–85 [Google Scholar]
  69. Mason B, Schmale M, Gibbs P, Miller MW, Wang Q. et al. 2012. Evidence for multiple phototransduction pathways in a reef-building coral. PLOS ONE 7:12e50371 [Google Scholar]
  70. Mayeenuddin LH, Mitchell J. 2003. Squid visual arrestin: cDNA cloning and calcium-dependent phosphorylation by rhodopsin kinase (SQRK). J. Neurochem. 85:592–600 [Google Scholar]
  71. Mayr E. 1963. Animal Species and Evolution. Cambridge, MA: Harvard Univ. Press
  72. McGraw KJ, Safran RJ, Wakamatsu K. 2005. How feather colour reflects its melanin content. Funct. Ecol. 19:5816–21 [Google Scholar]
  73. McGreal RS, Kantorow WL, Chauss DC, Wei J, Brennan LA, Kantorow M. 2012. αB-crystallin/sHSP protects cytochrome c and mitochondrial function against oxidative stress in lens and retinal cells. Biochim. Biophys. Acta 18207921–30
  74. Mohamed AK, Burr C, Burr AHJ. 2007. Unique two-photoreceptor scanning eye of the nematode Mermis nigrescens. Biol. Bull. 212:206–21 [Google Scholar]
  75. Montell C. 1999. Visual transduction in Drosophila. Annu. Rev. Cell Dev. Biol. 15:231–68 [Google Scholar]
  76. Muller GB, Wagner GP. 1991. Novelty in evolution: restructuring the concept. Annu. Rev. Ecol. Syst. 22:1229–56 [Google Scholar]
  77. Nakagawa M, Orii H, Yoshida N, Jojima E, Horie T. et al. 2002. Ascidian arrestin (Ci-arr), the origin of the visual and nonvisual arrestins of vertebrate. Eur. J. Biochem. 269:5112–18 [Google Scholar]
  78. Nijhout HF. 1997. Ommochrome pigmentation of the linea and rosa seasonal forms of Precis coenia (Lepidoptera: Nymphalidae). Arch. Insect Biochem. Physiol. 36:215–22 [Google Scholar]
  79. Nilsson D-E. 2009. The evolution of eyes and visually guided behaviour. Philos. Trans. R. Soc. Lond. B 364:15312833–47 [Google Scholar]
  80. Nilsson D-E. 2013. Eye evolution and its functional basis. Vis. Neurosci. 30:1–25–20 [Google Scholar]
  81. Nilsson D-E, Pelger S. 1994. A pessimistic estimate of the time required for an eye to evolve. Proc. R. Soc. B 256:134553–58 [Google Scholar]
  82. Nordström K, Larsson TA, Larhammar D. 2004. Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications. Genomics 83:5852–72 [Google Scholar]
  83. Nordström K, Wallén, Seymour J, Nilsson D. 2003. A simple visual system without neurons in jellyfish larvae. Proc. R. Soc. B 270:15312349–54 [Google Scholar]
  84. Ntefidou M, Iseki M, Watanabe M, Lebert M, Häder D-P. 2003. Photoactivated adenylyl cyclase controls phototaxis in the flagellate Euglena gracilis. Plant Physiol. 133:41517–21 [Google Scholar]
  85. Oakley TH, Cunningham CW. 2002. Molecular phylogenetic evidence for the independent evolutionary origin of an arthropod compound eye. PNAS 99:31426–30 [Google Scholar]
  86. Oakley TH, Pankey MS. 2008. Opening the “black box”: the genetic and biochemical basis of eye evolution. Evol. Educ. Outreach 1:4390–402 [Google Scholar]
  87. Oakley TH, Plachetzki DC, Rivera AS. 2007. Furcation, field-splitting, and the evolutionary origins of novelty in arthropod photoreceptors. Arthropod Struct. Dev. 36:4386–400 [Google Scholar]
  88. Ohno S. 1970. Evolution by Gene Duplication. New York: Springer
  89. Ozaki K, Terakita A, Hara R, Hara T. 1987. Isolation and characterization of a retinal-binding protein from the squid retina. Vis. Res. 27:1057–70 [Google Scholar]
  90. Piatigorsky J. 2007. Gene Sharing and Evolution: The Diversity of Protein Functions. Cambridge, MA: Harvard Univ. Press [Google Scholar]
  91. Plachetzki DC, Degnan BM, Oakley TH. 2007. The origins of novel protein interactions during animal opsin evolution. PLOS ONE 2:10e1054 [Google Scholar]
  92. Plachetzki DC, Fong CR, Oakley TH. 2010. The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway. Proc. R. Soc. B 277:16901963–69 [Google Scholar]
  93. Plachetzki DC, Oakley TH. 2007. Key transitions during the evolution of animal phototransduction: novelty, “tree-thinking,” co-option, and co-duplication. Integr. Comp. Biol. 47:759–69 [Google Scholar]
  94. Poliakov E, Gubin AN, Stearn O, Li Y, Campos MM. et al. 2012. Origin and evolution of retinoid isomerization machinery in vertebrate visual cycle: hint from jawless vertebrates. PLOS ONE 7:11e49975 [Google Scholar]
  95. Porcar M, Bel Y, Socha R, Němec V, Ferré J. 1996. Identification of pteridines in the firebug, Pyrrhocoris apterus (L.) (Heteroptera, Pyrrhocoridae) by high-performance liquid chromatography. J. Chromatogr. A 724:1–2193–97 [Google Scholar]
  96. Porter ML, Blasic JR, Bok MJ, Cameron EG, Pringle T. et al. 2012. Shedding new light on opsin evolution. Proc. R. Soc. B 279:17263–14 [Google Scholar]
  97. Porter ML, Crandall KA. 2003. Lost along the way: the significance of evolution in reverse. Trends Ecol. Evol. 18:10541–47 [Google Scholar]
  98. Porter ML, Speiser DI, Zaharoff AK, Caldwell RL, Cronin TW, Oakley TH. 2013. The evolution of complexity in the visual systems of stomatopods: insights from transcriptomics. Integr. Comp. Biol. 53:139–49 [Google Scholar]
  99. Ramirez MD, Speiser DI, Pankey MS, Oakley TH. 2011. Understanding the dermal light sense in the context of integrative photoreceptor cell biology. Vis. Neurosci. 28:265–79 [Google Scholar]
  100. Randel N, Asadulina A, Bezares-Calderón LA, Verasztó C, Williams EA. et al. 2014. Neuronal connectome of a sensory-motor circuit for visual navigation. eLife 3:e02730 [Google Scholar]
  101. Rivera AS, Ozturk N, Fahey B, Plachetzki DC, Degnan BM. et al. 2012. Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin. J. Exp. Biol. 215:Pt 81278–86 [Google Scholar]
  102. Ruxton GD, Sherratt TN, Speed MP. 2004. Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals, and Mimicry 249 Oxford, UK: Oxford Univ. Press
  103. Ryall RL, Howells AJ. 1974. Ommochrome biosynthetic pathway of Drosophila melanogaster—variations in levels of enzyme activities and intermediates during adult development. Insect Biochem. 4:47–61 [Google Scholar]
  104. Saranak J, Foster KW. 1997. Rhodopsin guides fungal phototaxis. Nature 387:6632465–66 [Google Scholar]
  105. Satir P, Christensen ST. 2007. Overview of structure and function of mammalian cilia. Annu. Rev. Physiol. 69:377–400 [Google Scholar]
  106. Sebé-Pedrós A, Burkhardt P, Sánchez-Pons N, Fairclough SR, Lang BF. et al. 2013. Insights into the origin of metazoan filopodia and microvilli. Mol. Biol. Evol. 30:92013–23 [Google Scholar]
  107. Serb JM, Oakley TH. 2005. Hierarchical phylogenetics as a quantitative analytical framework for evolutionary developmental biology. Bioessays 27:111158–66 [Google Scholar]
  108. Shen D, Jiang M, Hao W, Tao L, Salazar M, Fong HK. 1994. A human opsin-related gene that encodes a retinaldehyde-binding protein. Biochemistry 33:4413117–25 [Google Scholar]
  109. Speiser DI, DeMartini DG, Oakley TH. 2014a. The shell-eyes of the chiton Acanthopleura granulata (Mollusca, Polyplacophora) use pheomelanin as a screening pigment. J. Nat. Hist. 48:2899–911 [Google Scholar]
  110. Speiser DI, Eernisse DJ, Johnsen S. 2011. A chiton uses aragonite lenses to form images. Curr. Biol. 21:665–70 [Google Scholar]
  111. Speiser DI, Lampe RI, Lovdahl VR, Carrillo-Zazueta B, Rivera AS, Oakley TH. 2013. Evasion of predators contributes to the maintenance of male eyes in sexually dimorphic Euphilomedes ostracods (Crustacea). Integr. Comp. Biol. 53:178–88 [Google Scholar]
  112. Speiser DI, Pankey M, Zaharoff AK, Battelle BA, Bracken-Grissom HD. et al. 2014b. Using phylogenetically-informed annotation (PIA) to search for light-interacting genes in transcriptomes from non-model organisms. BMC Bioinform. 15:1350 [Google Scholar]
  113. Spudich JL, Yang CS, Jung KH, Spudich EN. 2000. Retinylidene proteins: structures and functions from archaea to humans. Annu. Rev. Cell Dev. Biol. 16:365–92 [Google Scholar]
  114. Suga H, Koyanagi M, Hoshiyama D, Ono K, Iwabe N. et al. 1999. Extensive gene duplication in the early evolution of animals before the parazoan-eumetazoan split demonstrated by G proteins and protein tyrosine kinases from sponge and hydra. J. Mol. Evol. 48:646–53 [Google Scholar]
  115. Suga H, Schmid V, Gehring WJ. 2008. Evolution and functional diversity of jellyfish opsins. Curr. Biol. 18:151–55 [Google Scholar]
  116. Sugumaran M. 2002. Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Melanoma Res. 15:2–9 [Google Scholar]
  117. Takeuchi K, Satoul Y, Yamamoto H, Satoh N. 2005. A genome-wide survey of genes for enzymes involved in pigment synthesis in an ascidian, Ciona intestinalis. Zool. Sci. 22:723–34 [Google Scholar]
  118. Tan D-X, Hardeland R, Manchester LC, Paredes SD, Korkmaz A. et al. 2010. The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness. Biol. Rev. Camb. Philos. Soc. 85:3607–23 [Google Scholar]
  119. Terakita A, Hara R, Hara T. 1989. Retinal-binding protein as a shuttle for retinal in the rhodopsin-retinochrome system of the squid visual cells. Vis. Res. 29:639–52 [Google Scholar]
  120. Tomarev SI, Piatigorsky J. 1996. Lens crystallins of invertebrates. Eur. J. Biochem. 235:3449–65 [Google Scholar]
  121. True JR, Carroll SB. 2002. Gene co-option in physiological and morphological evolution. Annu. Rev. Cell Dev. Biol. 18:53–80 [Google Scholar]
  122. Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM. 2001. Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292:55242066–69 [Google Scholar]
  123. Ullrich-Lueter EM, Dupont S, Arboleda E, Hausen H, Arnone MI. 2011. Unique system of photoreceptors in sea urchin tube feet. PNAS 108:8367–72 [Google Scholar]
  124. Venkatachalam K, Montell C. 2007. TRP channels. Annu. Rev. Biochem. 76:387–417 [Google Scholar]
  125. Viscontini M, Hummel W, Fischer A. 1970. Pigmente von Nereiden (Annelida, Polychaeten). 1., Vorläufige Mitteilung. Isolierung von Pterindimeren aus den Augen von Platynereis dumerilii (Audouin & Milne Edwards) 1833. Helvetica Chima Acta 53:1207–9 [Google Scholar]
  126. von Salvini-Plawen L, Mayr E. 1977. On the evolution of photoreceptors and eyes. Evolutionary Biology MK Hecht, WC Steere, B Wallace 207–63 Boston: Springer [Google Scholar]
  127. Vopalensky P, Kozmik Z. 2009. Eye evolution: common use and independent recruitment of genetic components. Philos. Trans. R. Soc. B 364:2819–32 [Google Scholar]
  128. Wald G. 1968. Molecular basis of visual excitation. Science 162:3850230–39 [Google Scholar]
  129. Wang H, Yang B, Hao G, Feng Y, Chen H. et al. 2011. Biochemical characterization of the tetrahydrobiopterin synthesis pathway in the oleaginous fungus Mortierella alpina. Microbiology 157:3059–70 [Google Scholar]
  130. Wang X, Wang T, Jiao Y, von Lintig J, Montell C. 2010. Requirement for an enzymatic visual cycle in Drosophila. Curr. Biol. 20:93–102 [Google Scholar]
  131. Wang X, Wang T, Ni JD, von Lintig J, Montell C. 2012. The Drosophila visual cycle and de novo chromophore synthesis depends on rdhB. J. Neurosci. 32:3485–91 [Google Scholar]
  132. Watt WB. 1967. Pteridine biosynthesis in the butterfly Colias eurytheme. J. Biol. Chem. 242:565–72 [Google Scholar]
  133. Wittkopp PJ, Beldade P. 2009. Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Semin. Cell Dev. Biol. 20:65–71 [Google Scholar]
  134. Wittkopp PJ, Carroll SB, Kopp A. 2003. Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet. 19:495–504 [Google Scholar]
  135. Wogulis M, Chew ER, Donohoue PD, Wilson DK. 2008. Identification of formyl kynurenine formamidase and kynurenine aminotransferase from Saccharomyces cerevisiae using crystallographic, bioinformatic and biochemical evidence. Biochemistry 47:1608–21 [Google Scholar]
  136. Ziegler I. 1961. Genetic aspects of ommochrome and pterin pigments. Adv. Genet. 10:349–403 [Google Scholar]
  137. Ziegler I. 2003. The pteridine pathway in zebrafish: regulation and specification during the determination of neural crest cell-fate. Pigment Cell Melanoma Res. 16:172–82 [Google Scholar]
  138. Zinovieva RD, Tomarev SI, Piatigorsky J. 1993. Aldehyde dehydrogenase-derived Ω-crystallins of squid and octopus. Specialization for lens expression. J. Biol. Chem. 268:1511449–55 [Google Scholar]
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