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Vertebrate Eye Evolution

Chapter

Abstract

How transcriptional gene networks operate during development and how they have emerged during evolution are two fundamental and interconnected questions in the evo-devo field (Davidson in The regulatory genome: gene regulatory networks in development and evolution. Academic Press, Amsterdam, 2006; Carroll in Cell 134(1):25–36, 2008). In this chapter we discuss the origin of the vertebrate eye from a common ancestor and its gene regulatory network (GRN). In an attempt to shed light on the evolutionary history of the vertebrate eye, photoreceptive structures present in our chordate sister groups cephalochordates (lancelets) and urochordates (tunicates) will be examined. Additionally, we summarize the still fragmentary information on the specification of visual organs in these chordate groups.

Keywords

Vertebrate-eye evolution Visual organs Chambered-eyes Rhabdomeric photoreceptors Ciliary photoreceptors Pigment cell Amphioxus ocelli Ascidian ocelli 

Notes

Acknowledgments

This work was supported by grants BFU2011-22916, BFU2014-53765-P, and P11-CVI-7256 to JRMM.

References

  1. Abitua, P. B., Wagner, E., Navarrete, I. A., & Levine, M. (2012). Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature, 492(7427), 104–107.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Arendt, D. (2003). Evolution of eyes and photoreceptor cell types. International Journal of Developmental Biology, 47(7–8), 563–571.PubMedGoogle Scholar
  3. Arendt, D., Tessmar, K., de Campos-Baptista, M. I., Dorresteijn, A., & Wittbrodt, J. (2002). Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development, 129(5), 1143–1154.PubMedGoogle Scholar
  4. 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(5697), 869–871.PubMedCrossRefGoogle Scholar
  5. Arendt, D., & Wittbrodt, J. (2001). Reconstructing the eyes of Urbilateria. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 356, 1545–1563.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bailey, T. J., El-Hodiri, H., Zhang, L., Shah, R., Mathers, P. H., & Jamrich, M. (2004). Regulation of vertebrate eye development by Rx genes. International Journal of Developmental Biology, 48(8–9), 761–770.PubMedCrossRefGoogle Scholar
  7. Bharti, K., Liu, W., Csermely, T., Bertuzzi, S., & Arnheiter, H. (2008). Alternative promoter use in eye development: The complex role and regulation of the transcription factor MITF. Development, 135(6), 1169–1178.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Caracciolo, A., Gesualdo, I., Branno, M., Aniello, F., Di Lauro, R., & Palumbo, A. (1997). Specific cellular localization of tyrosinase mRNA during Ciona intestinalis larval development. Development, Growth & Differentiation, 39(4), 437–444.CrossRefGoogle Scholar
  9. Carroll, S. B. (2008). Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell, 134(1), 25–36.PubMedCrossRefGoogle Scholar
  10. Cole, A. G., & Meinertzhagen, I. A. (2004). The central nervous system of the ascidian larva: Mitotic history of cells forming the neural tube in late embryonic Ciona intestinalis. Developmental Biology, 271(2), 239–262.PubMedCrossRefGoogle Scholar
  11. D’Aniello, E., Pezzotti, M. R., Locascio, A., & Branno, M. (2011). Onecut is a direct neural-specific transcriptional activator of Rx in Ciona intestinalis. Developmental Biology, 355(2), 358–371.PubMedCrossRefGoogle Scholar
  12. D’Aniello, S., D’Aniello, E., Locascio, A., Memoli, A., Corrado, M., Russo, M. T., et al. (2006). The ascidian homolog of the vertebrate homeobox gene Rx is essential for ocellus development and function. Differentiation, 74(5), 222–234.PubMedCrossRefGoogle Scholar
  13. Danno, H., Michiue, T., Hitachi, K., Yukita, A., Ishiura, S., & Asashima, M. (2008). Molecular links among the causative genes for ocular malformation: Otx2 and Sox2 coregulate Rax expression. Proceedings of the National Academy of Sciences of the United States of America, 105(14), 5408–5413.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Darras, S., & Nishida, H. (2001). The BMP/CHORDIN antagonism controls sensory pigment cell specification and differentiation in the ascidian embryo. Developmental Biology, 236(2), 271–288.PubMedCrossRefGoogle Scholar
  15. Davidson, E. H. (2006). The regulatory genome: Gene regulatory networks in development and evolution. Amsterdam, The Netherlands: Academic Press.Google Scholar
  16. del Marmol, V., & Beermann, F. (1996). Tyrosinase and related proteins in mammalian pigmentation. FEBS Letters, 381(3), 165–168.PubMedCrossRefGoogle Scholar
  17. Dilly, P. N. (1961). Electron microscope observations on the submicroscopic organization of the ascidian tadpole. Nature (London), 191, 186–187.CrossRefGoogle Scholar
  18. Drivenes, O., Soviknes, A. M., Ebbesson, L. O., Fjose, A., Seo, H. C., & Helvik, J. V. (2003). Isolation and characterization of two teleost melanopsin genes and their differential expression within the inner retina and brain. Journal of Comparative Neurology, 456(1), 84–93.PubMedCrossRefGoogle Scholar
  19. Eagleson, G. W., & Harris, W. A. (1990). Mapping of the presumptive brain regions in the neural plate of Xenopus laevis. Journal of Neurobiology, 21(3), 427–440.PubMedCrossRefGoogle Scholar
  20. Eakin, R. (1968). Evolution of photoreceptors. New York: Appleton-Century-Crofts.CrossRefGoogle Scholar
  21. Eakin, R., & Kuda, A. (1971a). Ultrastructure of sensory receptors in ascidian tadpoles. Z. Zellforsch, 112, 287–312.PubMedCrossRefGoogle Scholar
  22. Eakin, R. M., & Kuda, A. (1971b). Ultrastructure of sensory receptors in Ascidian tadpoles. Z Zellforsch Mikrosk Anat, 112(3), 287–312.PubMedCrossRefGoogle Scholar
  23. Eakin, R. M., & Kuda, A. (1972). Glycogen in lens of tunicate tadpole (Chordata: Ascidiacea). Journal of Experimental Zoology, 180(2), 267–270.PubMedCrossRefGoogle Scholar
  24. Erclik, T., Hartenstein, V., Lipshitz, H. D., & McInnes, R. R. (2008). Conserved role of the Vsx genes supports a monophyletic origin for bilaterian visual systems. Current Biology, 18(17), 1278–1287.PubMedCrossRefGoogle Scholar
  25. Erclik, T., Hartenstein, V., McInnes, R. R., & Lipshitz, H. D. (2009). Eye evolution at high resolution: The neuron as a unit of homology. Developmental Biology, 332(1), 70–79.PubMedCrossRefGoogle Scholar
  26. Esposito, R., D’Aniello, S., Squarzoni, P., Pezzotti, M. R., Ristoratore, F., & Spagnuolo, A. (2012). New insights into the evolution of metazoan tyrosinase gene family. PLoS ONE, 7(4), e35731.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Esposito, R., Racioppi, C., Pezzotti, M. R., Branno, M., Locascio, A., Ristoratore, F., & Spagnuolo, A. (2015). The ascidian pigmented sensory organs: Structures and developmental programs. Genesis, 53(1), 15–33.PubMedCrossRefGoogle Scholar
  28. Estivill-Torrus, G., Vitalis, T., Fernandez-Llebrez, P., & Price, D. J. (2001). The transcription factor Pax6 is required for development of the diencephalic dorsal midline secretory radial glia that form the subcommissural organ. Mechanisms of Development, 109(2), 215–224.PubMedCrossRefGoogle Scholar
  29. Fernald, R. D. (2004). Evolving eyes. The International Journal of Developmental Biology, 48(8–9), 701–705.PubMedCrossRefGoogle Scholar
  30. Fernholm, B., & Holmberg, K. (1975). The eyes in three genera of hagfish (Eptatretus, Paramyxine and Myxine)—A case of degenerative evolution. Vision Research, 15(2), 253–259.PubMedCrossRefGoogle Scholar
  31. Forsell, J., Holmqvist, B., Helvik, J. V., & Ekstrom, P. (1997). Role of the pineal organ in the photoregulated hatching of the Atlantic halibut. The International Journal of Developmental Biology, 41(4), 591–595.PubMedGoogle Scholar
  32. Furukawa, T., Morrow, E. M., Li, T. S., Davis, F. C., & Cepko, C. L. (1999). Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nature Genetics, 23(4), 466–470.PubMedCrossRefGoogle Scholar
  33. Gehring, W. J., & Ikeo, K. (1999). Pax 6: Mastering eye morphogenesis and eye evolution. Trends in Genetics, 15(9), 371–377.PubMedCrossRefGoogle Scholar
  34. Giudetti, G., Giannaccini, M., Biasci, D., Mariotti, S., Degl’innocenti, A., Perrotta, M., et al. (2014). Characterization of the Rx1-dependent transcriptome during early retinal development. Developmental Dynamics, 243(10), 1352–1361.PubMedCrossRefGoogle Scholar
  35. Glardon, S., Holland, L. Z., Gehring, W. J., & Holland, N. D. (1998). Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): Insights into eye and photoreceptor evolution. Development, 125(14), 2701–2710.PubMedGoogle Scholar
  36. Gomez Mdel, P., Angueyra, J. M., & Nasi, E. (2009). Light-transduction in melanopsin-expressing photoreceptors of Amphioxus. Proceedings of the National Academy of Sciences of the United States of America, 106(22), 9081–9086.PubMedCrossRefGoogle Scholar
  37. Gorman, A. L., McReynolds, J. S., & Barnes, S. N. (1971). Photoreceptors in primitive chordates: Fine structure, hyperpolarizing receptor potentials, and evolution. Science, 172(3987), 1052–1054.PubMedCrossRefGoogle Scholar
  38. Halder, G., Callaerts, P., & Gehring, W. J. (1995). Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science, 267, 1788–1792.PubMedCrossRefGoogle Scholar
  39. Hattar, S., Liao, H. W., Takao, M., Berson, D. M., & Yau, K. W. (2002). Melanopsin-containing retinal ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science, 295(5557), 1065–1070.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Heimberg, A. M., Cowper-Sal-lari, R., Semon, M., Donoghue, P. C., & Peterson, K. J. (2010). microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proceedings of the National Academy of Sciences of the United States of America, 107(45), 19379–19383.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hill, R. E., Favor, J., Hogan, B. L. M., Ton, C. C. T., Saunders, G. F., Hanson, I. M., et al. (1991). Mouse small eye results from mutations in a paired-like homeobox containing gene. Nature, 354, 522–525.PubMedCrossRefGoogle Scholar
  42. Holland, N. D., & Chen, J. (2001). Origin and early evolution of the vertebrates: New insights from advances in molecular biology, anatomy, and palaeontology. BioEssays, 23(2), 142–151.PubMedCrossRefGoogle Scholar
  43. Holmberg, K. H. (1977). The visual system of vertebrates. In F. Crescitelli (Ed.), Handbook of sensory physiology (Vol. VII/5). Berlin: Springer.Google Scholar
  44. Hong, S. K., Kim, C. H., Yoo, K. W., Kim, H. S., Kudoh, T., Dawid, I. B., & Huh, T. L. (2002). Isolation and expression of a novel neuron-specific onecut homeobox gene in zebrafish. Mechanisms of Development, 112(1–2), 199–202.PubMedCrossRefGoogle Scholar
  45. Horie, T., Orii, H., & Nakagawa, M. (2005). Structure of ocellus photoreceptors in the ascidian Ciona intestinalis larva as revealed by an anti-arrestin antibody. Journal of Neurobiology, 65(3), 241–250.PubMedCrossRefGoogle Scholar
  46. Horie, T., Sakurai, D., Ohtsuki, H., Terakita, A., Shichida, Y., Usukura, J., et al. (2008). Pigmented and nonpigmented ocelli in the brain vesicle of the ascidian larva. Journal of Comparative Neurology, 509(1), 88–102.PubMedCrossRefGoogle Scholar
  47. Imai, K. S., Stolfi, A., Levine, M., & Satou, Y. (2009). Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system. Development, 136(2), 285–293.PubMedCrossRefGoogle Scholar
  48. Inada, K., Horie, T., Kusakabe, T., & Tsuda, M. (2003). Targeted knockdown of an opsin gene inhibits the swimming behaviour photoresponse of ascidian larvae. Neuroscience Letters, 347(3), 167–170.PubMedCrossRefGoogle Scholar
  49. Irvine, S. Q., Fonseca, V. C., Zompa, M. A., & Antony, R. (2008). Cis-regulatory organization of the Pax6 gene in the ascidian Ciona intestinalis. Developmental Biology, 317(2), 649–659.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Ivashkin, E., & Adameyko, I. (2013). Progenitors of the protochordate ocellus as an evolutionary origin of the neural crest. Evodevo, 4.Google Scholar
  51. Jiang, D., Tresser, J. W., Horie, T., Tsuda, M., & Smith, W. C. (2005). Pigmentation in the sensory organs of the ascidian larva is essential for normal behavior. The Journal of Experimental Biology, 208(Pt 3), 433–438.PubMedCrossRefGoogle Scholar
  52. Kajiwara, S., & Yoshida, M. (1985). Changes in behavior and ocellar structure during the larval life of solitary ascidians. Biological Bulletin, 169, 565–577.CrossRefGoogle Scholar
  53. Katoh, K., Omori, Y., Onishi, A., Sato, S., Kondo, M., & Furukawa, T. (2010). Blimp1 suppresses Chx10 expression in differentiating retinal photoreceptor precursors to ensure proper photoreceptor development. Journal of Neuroscience, 30(19), 6515–6526.PubMedCrossRefGoogle Scholar
  54. Kimura, A., Singh, D., Wawrousek, E. F., Kikuchi, M., Nakamura, M., & Shinohara, T. (2000). Both PCE-1/RX and OTX/CRX interactions are necessary for photoreceptor-specific gene expression. Journal of Biological Chemistry, 275(2), 1152–1160.PubMedCrossRefGoogle Scholar
  55. Kusakabe, T., & Tsuda, M. (2007). Photoreceptive systems in ascidians. Photochemistry and Photobiology, 83(2), 248–252.PubMedCrossRefGoogle Scholar
  56. Lacalli, T. C. (1996). Frontal eye circuitry, rostral sensory pathways and brain organization in amphioxus larvae: Evidence from 3D reconstructions. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 351(1337), 243–263.CrossRefGoogle Scholar
  57. Lacalli, T. C. (2001). New perspectives on the evolution of protochordate sensory and locomotory systems, and the origin of brains and heads. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 356(1414), 1565–1572.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lacalli, T. C. (2002). The dorsal compartment locomotory control system in amphioxus larvae. Journal of Morphology, 252(3), 227–237.PubMedCrossRefGoogle Scholar
  59. Lacalli, T. C. (2004). Sensory systems in amphioxus: A window on the ancestral chordate condition. Brain, Behavior and Evolution, 64(3), 148–162.PubMedCrossRefGoogle Scholar
  60. Lacalli, T. C., & Kelly, S. J. (2003). Ventral neurons in the anterior nerve cord of amphioxus larvae. I. An inventory of cell types and synaptic patterns. Journal of Morphology, 257(2), 190–211.PubMedCrossRefGoogle Scholar
  61. Lamb, T. D. (2013). Evolution of phototransduction, vertebrate photoreceptors and retina. Progress in Retinal and Eye Research, 36, 52–119.PubMedCrossRefGoogle Scholar
  62. Lamb, T. D., Collin, S. P., & Pugh, E. N, Jr. (2007). Evolution of the vertebrate eye: Opsins, photoreceptors, retina and eye cup. Nature Reviews Neuroscience, 8(12), 960–976.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Land, M. F., & Nilsson, D.-E. (2002). Animal eyes. Oxford; New York: Oxford University Press.Google Scholar
  64. Landry, C., Clotman, F., Hioki, T., Oda, H., Picard, J. J., Lemaigre, F. P., & Rousseau, G. G. (1997). HNF-6 is expressed in endoderm derivatives and nervous system of the mouse embryo and participates to the cross-regulatory network of liver-enriched transcription factors. Developmental Biology, 192(2), 247–257.PubMedCrossRefGoogle Scholar
  65. Leung, Y. F., Ma, P., Link, B. A., & Dowling, J. E. (2008). Factorial microarray analysis of zebrafish retinal development. Proceedings of the National Academy of Sciences of the United States of America, 105(35), 12909–12914.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Locket, N. A., & Jorgensen, J. M. (1998). The biology of hagfishes. In J. M. Jorgensen, J. P. Lomholt, R. E. Weber, & H. Weber (Eds.). London: Chapman and Hall.Google Scholar
  67. Mallatt, J., & Sullivan, J. (1998). 28S and 18S rDNA sequences support the monophyly of lampreys and hagfishes. Molecular Biology and Evolution, 15(12), 1706–1718.PubMedCrossRefGoogle Scholar
  68. Martinez-Morales, J. R., Dolez, V., Rodrigo, I., Zaccarini, R., Leconte, L., Bovolenta, P., & Saule, S. (2003). OTX2 activates the molecular network underlying retina pigment epithelium differentiation. Journal of Biological Chemistry, 278(24), 21721–21731.PubMedCrossRefGoogle Scholar
  69. Martinez-Morales, J. R., Rodrigo, I., & Bovolenta, P. (2004). Eye development: A view from the retina pigmented epithelium. BioEssays, 26(7), 766–777.PubMedCrossRefGoogle Scholar
  70. Matos-Cruz, V., Blasic, J., Nickle, B., Robinson, P. R., Hattar, S., & Halpern, M. E. (2011). Unexpected diversity and photoperiod dependence of the zebrafish melanopsin system. PLoS ONE, 6(9), e25111.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Melendez-Ferro, M., Perez-Costas, E., Gonzalez, M. J., Pombal, M. A., Anadon, R., & Rodicio, M. C. (2000). GABA-immunoreactive internuclear neurons in the ocular motor system of lampreys. Brain Research, 855(1), 150–157.PubMedCrossRefGoogle Scholar
  72. Miya, T., & Nishida, H. (2003). An Ets transcription factor, HrEts, is target of FGF signaling and involved in induction of notochord, mesenchyme, and brain in ascidian embryos. Developmental Biology, 261(1), 25–38.PubMedCrossRefGoogle Scholar
  73. Moret, F., Christiaen, L., Deyts, C., Blin, M., Joly, J. S., & Vernier, P. (2005). The dopamine-synthesizing cells in the swimming larva of the tunicate Ciona intestinalis are located only in the hypothalamus-related domain of the sensory vesicle. European Journal of Neuroscience, 21(11), 3043–3055.PubMedCrossRefGoogle Scholar
  74. Morris, S. C., & Caron, J. B. (2014). A primitive fish from the Cambrian of North America. Nature, 512(7515), 419–422.PubMedCrossRefGoogle Scholar
  75. Muranishi, Y., Terada, K., & Furukawa, T. (2012). An essential role for Rax in retina and neuroendocrine system development. Development, Growth & Differentiation, 54(3), 341–348.CrossRefGoogle Scholar
  76. Murisier, F., & Beermann, F. (2006). Genetics of pigment cells: Lessons from the tyrosinase gene family. Histology and Histopathology, 21(4–6), 567–578.PubMedGoogle Scholar
  77. Nguyen, D. N., Rohrbaugh, M., & Lai, Z. (2000). The Drosophila homolog of Onecut homeodomain proteins is a neural-specific transcriptional activator with a potential role in regulating neural differentiation. Mechanisms of Development, 97(1–2), 57–72.PubMedCrossRefGoogle Scholar
  78. Nguyen, M. T., & Arnheiter, H. (2000). Signaling and transcriptional regulation in early mammalian eye development: A link between FGF and MITF. Development, 127, 3581–3591.PubMedGoogle Scholar
  79. Nicol, D., & Meinertzhagen, I. A. (1991). Cell counts and maps in the larval central-nervous-system of the ascidian Ciona-intestinalis (L). Journal of Comparative Neurology, 309(4), 415–429.PubMedCrossRefGoogle Scholar
  80. Nishida, A., Furukawa, A., Koike, C., Tano, Y., Aizawa, S., Matsuo, I., & Furukawa, T. (2003). Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nature Neuroscience, 6(12), 1255–1263.PubMedCrossRefGoogle Scholar
  81. Nishida, H. (1987). Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Developmental Biology, 121(2), 526–541.PubMedCrossRefGoogle Scholar
  82. Ohtsuki, H. (1990). Statocyte and ocellar pigment cell in embryos and larvae of the ascidian, Styela-plicata (Lesueur). Development, Growth & Differentiation, 32(1), 85–90.CrossRefGoogle Scholar
  83. Ostholm, T., Brannas, E., & van Veen, T. (1987). ‘The pineal organ is the first differentiated light receptor in the embryonic salmon, Salmo salar L. Cell and Tissue Research, 249(3), 641–646.PubMedCrossRefGoogle Scholar
  84. Pezzotti, M. R., Locascio, A., Racioppi, C., Fucci, L., & Branno, M. (2014). Auto and cross regulatory elements control Onecut expression in the ascidian nervous system. Developmental Biology, 390(2), 273–287.PubMedCrossRefGoogle Scholar
  85. Pichaud, F., & Desplan, C. (2002). Pax genes and eye organogenesis. Current Opinion in Genetics & Development, 12(4), 430–434.CrossRefGoogle Scholar
  86. Quiring, R., Walldorf, U., Kloter, U., & Gehring, W. J. (1994). Homology of the eyeless gene of drosophila to the small eye gene in mice and aniridia in humans. Science, 265, 785–789.PubMedCrossRefGoogle Scholar
  87. Razy-Krajka, F., Brown, E. R., Horie, T., Callebert, J., Sasakura, Y., Joly, J. S., et al. (2012). Monoaminergic modulation of photoreception in ascidian: Evidence for a proto-hypothalamo-retinal territory. BMC Biology, 10, 45.PubMedPubMedCentralCrossRefGoogle Scholar
  88. Reichert, H., & Simeone, A. (2001). Developmental genetic evidence for a monophyletic origin of the bilaterian brain. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 356(1414), 1533–1544.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Rhode, B. (1991). Ultrastructure of prostomial photoreceptors in four marine polychaete species (Annelida). Journal of Morphology, 209, 177–188.CrossRefGoogle Scholar
  90. Rhode, B. (1992). Development and differentiation of the eye in Platynereis durilii (Annelida, Polychaeta). Journal of Morphology, 212, 71–85.CrossRefGoogle Scholar
  91. Riyahi, K., & Shimeld, S. M. (2007). Chordate betagamma-crystallins and the evolutionary developmental biology of the vertebrate lens. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 147(3), 347–357.CrossRefGoogle Scholar
  92. Ruiz, M. S., & Anadon, R. (1991). Some considerations on the fine structure of rhabdomeric photoreceptors in the amphioxus, Branchiostoma lanceolatum (Cephalochordata). Journal fur Hirnforschung, 32(2), 159–164.PubMedGoogle Scholar
  93. Sakurai, D., Goda, M., Kohmura, Y., Horie, T., Iwamoto, H., Ohtsuki, H., & Tsuda, M. (2004). The role of pigment cells in the brain of ascidian larva. Journal of Comparative Neurology, 475(1), 70–82.PubMedCrossRefGoogle Scholar
  94. Sapkota, D., Chintala, H., Wu, F. G., Fliesler, S. J., Hu, Z. H., & Mu, X. Q. (2014). Onecut1 and Onecut2 redundantly regulate early retinal cell fates during development. Proceedings of the National Academy of Sciences of the United States of America, 111(39), E4086–E4095.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Satir, P. (2000). A comment on the origin of the vertebrate eye. Anatomical Record, 261(6), 224–227.PubMedCrossRefGoogle Scholar
  96. Sato, S., Masuya, H., Numakunai, T., Satoh, N., Ikeo, K., Gojobori, T., et al. (1997). Ascidian tyrosinase gene: Its unique structure and expression in the developing brain. Developmental Dynamics: An Official Publication of the American Association of Anatomists, 208(3), 363–374.CrossRefGoogle Scholar
  97. Sato, S., & Yamamoto, H. (2001). Development of pigment cells in the brain of ascidian tadpole larvae: Insights into the origins of vertebrate pigment cells. Pigment Cell Research/Sponsored by the European Society for Pigment Cell Research and the International Pigment Cell Society, 14(6), 428–436.CrossRefGoogle Scholar
  98. Shimeld, S. M., Purkiss, A. G., Dirks, R. P., Bateman, O. A., Slingsby, C., & Lubsen, N. H. (2005). Urochordate betagamma-crystallin and the evolutionary origin of the vertebrate eye lens. Current Biology: CB, 15(18), 1684–1689.PubMedCrossRefGoogle Scholar
  99. Squarzoni, P., Parveen, F., Zanetti, L., Ristoratore, F., & Spagnuolo, A. (2011). FGF/MAPK/Ets signaling renders pigment cell precursors competent to respond to Wnt signal by directly controlling Ci-Tcf transcription. Development, 138(7), 1421–1432.PubMedCrossRefGoogle Scholar
  100. Stokes, M. D., & Holland, N. D. (1995). Ciliary hovering in larval lancelets (=Amphioxus). Biological Bulletin, 188(3), 231–233.CrossRefGoogle Scholar
  101. Suzuki, A., Endo, K., & Kitano, T. (2014). Phylogenetic positions of RH blood group-related genes in cyclostomes. Gene, 543(1), 22–27.PubMedCrossRefGoogle Scholar
  102. Taniguchi, K., & Nishida, H. (2004). Tracing cell fate in brain formation during embryogenesis of the ascidian Halocynthia roretzi. Development, Growth & Differentiation, 46(2), 163–180.CrossRefGoogle Scholar
  103. Toyoda, R., Kasai, A., Sato, S., Wada, S., Saiga, H., Ikeo, K., et al. (2004). Pigment cell lineage-specific expression activity of the ascidian tyrosinase-related gene. Gene, 332, 61–69.PubMedCrossRefGoogle Scholar
  104. Tsuda, M., Sakurai, D., & Goda, M. (2003a). Direct evidence for the role of pigment cells in the brain of ascidian larvae by laser ablation. Journal of Experimental Biology, 206(8), 1409–1417.PubMedCrossRefGoogle Scholar
  105. Tsuda, M., Sakurai, D., & Goda, M. (2003b). Direct evidence for the role of pigment cells in the brain of ascidian larvae by laser ablation. Journal of Experimental Biology, 206(Pt 8), 1409–1417.PubMedCrossRefGoogle Scholar
  106. Velarde, R. A., Sauer, C. D., Walden, K. K. O., Fahrbach, S. E., & Robertson, H. M. (2005). Pteropsin: A vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochemistry and Molecular Biology, 35(12), 1367–1377.PubMedCrossRefGoogle Scholar
  107. von Salvini-Plawen, L. (1982). On the polyphyletic origin of photoreceptors. In J. A. Westfall (Ed.), Visual cells in evolution. New York: Raven Press.Google Scholar
  108. Vopalensky, P., & Kozmik, Z. (2009). Eye evolution: Common use and independent recruitment of genetic components. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 364(1531), 2819–2832.PubMedPubMedCentralCrossRefGoogle Scholar
  109. Vopalensky, P., Pergner, J., Liegertova, M., Benito-Gutierrez, E., Arendt, D., & Kozmik, Z. (2012). Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye. Proceedings of the National Academy of Sciences of the United States of America, 109(38), 15383–15388.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wada, S., Toyoda, R., Yamamoto, H., & Saiga, H. (2002). Ascidian otx gene Hroth activates transcription of the brain-specific gene HrTRP. Developmental Dynamics: An Official Publication of the American Association of Anatomists, 225(1), 46–53.CrossRefGoogle Scholar
  111. Watanabe, T., & Yoshida, M. (1986). ‘Morphological and Histochemical-Studies on Joseph Cells of Amphioxus, Branchiostoma-Belcheri Gray. Experimental Biology, 46(2), 67–73.PubMedGoogle Scholar
  112. Wicht, H., & Lacalli, T. C. (2005). The nervous system of amphioxus: Structure, development, and evolutionary significance. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 83(1), 122–150.CrossRefGoogle Scholar
  113. Wickstead, J. H., & Bone, Q. (1959). Ecology of acraniate larvae. Nature, 184, 1849–1851.Google Scholar
  114. Williams, N. A., & Holland, P. W. H. (1996). Old head on young shoulders. Nature, 383(6600), 490.CrossRefGoogle Scholar
  115. Wu, F., Sapkota, D., Li, R., & Mu, X. (2012). Onecut 1 and Onecut 2 are potential regulators of mouse retinal development. Journal of Comparative Neurology, 520(5), 952–969.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Yajima, I., Endo, K., Sato, S., Toyoda, R., Wada, H., Shibahara, S., et al. (2003). Cloning and functional analysis of ascidian Mitf in vivo: Insights into the origin of vertebrate pigment cells. Mechanisms of Development, 120(12), 1489–1504.PubMedCrossRefGoogle Scholar
  117. Yoshida, K., & Saiga, H. (2011). Repression of Rx gene on the left side of the sensory vesicle by Nodal signaling is crucial for right-sided formation of the ocellus photoreceptor in the development of Ciona intestinalis. Developmental Biology, 354(1), 144–150.PubMedCrossRefGoogle Scholar
  118. Yoshida, R., Sakurai, D., Horie, T., Kawakami, I., Tsuda, M., & Kusakabe, T. (2004). Identification of neuron-specific promoters in Ciona intestinalis. Genesis, 39(2), 130–140.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA)SevilleSpain
  2. 2.Stazione Zoologica Anton DohrnNaplesItaly

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