From comparison of the eyes of lampreys and jawed vertebrates, it is clear that a 'vertebrate-style' camera eye was already present in the last common ancestor of these taxa, around 500 million years ago (Mya).
Numerous features of hagfish eyes are far simpler than those of vertebrate eyes, and Lamb and colleagues' interpretation is that the eyes of extant hagfish are likely to be similar to the eyes possessed by our own ancestors, some 530 Mya. The authors suggest that this 'eye' did not exhibit image-forming capabilities, and that its function was instead non-visual (possibly circadian).
Comparison of photoreceptor ultrastructure across extant taxa that diverged from our own line at progessively more distant times in the past demonstrates what appears to be a series of fine gradations in cellular characteristics. This finding is consistent with a gradual evolution of improvements in photoreceptor function between 550 and 500 Mya.
Dendrograms of opsin genes indicate that three major classes of opsin (rhabdomeric, 'photoisomerase' and ciliary) were present in the bilateral ancestors of protostomes and deuterostomes, around 600 Mya. They also illuminate the major features of the subsequent evolution of visual and non-visual opsins.
The development of gross eye morphology and retinal microcircuitry provide clues to the evolution of the vertebrate retina. The results are consistent with the notion that a primitive retina (similar to that of hagfish) contained ciliary photoreceptors connected directly to projection neurons, and that subsequently retinal bipolar cells evolved and became inserted between the photoreceptors and the projection neurons.
By integrating these findings, Lamb and colleagues propose a scenario for a long sequence of small evolutionary steps that led (some 500 Mya) to the emergence of the vertebrate camera-style eye. The authors think that this sequence satisfies Darwin's prescription for overcoming “the difficulty of believing that a perfect and complex eye could be formed by natural selection”, and they suggest a number of explicit tests of such a scenario.
Charles Darwin appreciated the conceptual difficulty in accepting that an organ as wonderful as the vertebrate eye could have evolved through natural selection. He reasoned that if appropriate gradations could be found that were useful to the animal and were inherited, then the apparent difficulty would be overcome. Here, we review a wide range of findings that capture glimpses of the gradations that appear to have occurred during eye evolution, and provide a scenario for the unseen steps that have led to the emergence of the vertebrate eye.
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Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life 186 (John Murray, London, 1859).
Conway Morris, S. The Cambrian “explosion”: slow-fuse or megatonnage? Proc. Natl Acad. Sci. USA 97, 4426–4429 (2000).
Conway Morris, S. Evolution: bringing molecules into the fold. Cell 100, 1–11 (2000). This paper provides an illuminating analysis of the conflicts between the classical (paleontological and morphological) approaches to understanding evolution and the more recent molecular approaches.
Conway Morris, S. Darwin's dilemma: the realities of the Cambrian 'explosion'. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1069–1083 (2006).
Dawkins, R. & Krebs, J. R. Arms races between and within species. Proc. R. Soc. Lond. B Biol. Sci. 205, 489–511 (1979).
Gehring, W. J. Historical perspective on the development and evolution of eyes and photoreceptors. Int. J. Dev. Biol. 48, 707–717 (2004).
Fernald, R. D. in Evolution of Nervous Systems: A Comprehensive Reference. Vol. 2: Non-Mammalian Vertebrates (eds Kaas, J. H. & Bullock, T. H.) 335–348 (Elsevier, Amsterdam, 2007).
Arendt, D. & Wittbrodt, J. Reconstructing the eyes of Urbilateria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1545–1563 (2001).
Arendt, D. Evolution of eyes and photoreceptor cell types. Int. J. Dev. Biol. 47, 563–571 (2003). This paper, along with reference 8, lays the cellular and molecular foundations for identifying homologous types of visual cell across bilateral animals.
Land, M. F. & Nilsson, D.-E. Animal Eyes (Oxford Univ. Press, New York, 2002).
Janvier, P. Early Vertebrates (Oxford Univ. Press, Oxford, UK, 1996).
Xian-Guang, H., Aldridge, R. J., Siveter, D. J., Siveter, D. J. & Xiang-Hong, F. New evidence on the anatomy and phylogeny of the earliest vertebrates. Proc. R. Soc. Lond. B Biol. Sci. 269, 1865–1869 (2002).
Shu, D. G. et al. Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature 421, 526–529 (2003).
Gradstein, F. M., Ogg, J. G. & Smith, A. G. A Geologic Time Scale 2004 (Cambridge Univ. Press, Cambridge, UK, 2005).
Gess, R. W., Coates, M. I. & Rubidge, B. S. A lamprey from the Devonian period of South Africa. Nature 443, 981–984 (2006).
Janvier, P. Palaeontology: modern look for ancient lamprey. Nature 443, 921–924 (2006).
Benton, M. J. & Donoghue, P. C. J. Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26–53 (2007).
Donoghue, P. C. & Benton, M. J. Rocks and clocks: calibrating the tree of life using fossils and molecules. Trends Ecol. Evol. 22, 424–431 (2007).
Welch, J. J., Fontanillas, E. & Bromham, L. Molecular dates for the “Cambrian explosion”: the influence of prior assumptions. Syst. Biol. 54, 672–678 (2005).
Welch, J. J. & Bromham, L. Molecular dating when rates vary. Trends Ecol. Evol. 20, 320–327 (2005).
Thomas, J. A., Welch, J. J., Woolfit, M. & Bromham, L. There is no universal molecular clock for invertebrates, but rate variation does not scale with body size. Proc. Natl Acad. Sci. USA 103, 7366–7371 (2006).
Suga, H. et al. 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, 646–653 (1999).
Ohno, S. Evolution by Gene Duplication (Allen & Unwin, London, 1970).
Holland, P. W. H., García-Fernández, J. M., Williams, N. A. & Sidow, A. Gene duplications and the origins of vertebrate development. Development (Suppl.) 125–133 (1994).
Sidow, A. Gen(om)e duplications in the evolution of early vertebrates. Curr. Opin. Genet. Dev. 6, 715–722 (1996). This paper provides a summary of the evidence for, and the role of, early genome duplications in vertebrate evolution.
Furlong, R. F. & Holland, P. W. H. Were vertebrates octoploid? Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 531–544 (2002).
Lundin, L. G., Larhammar, D. & Hallböök, F. Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates. J. Struct. Funct. Genomics 3, 53–63 (2003).
Fredriksson, R., Lagerström, M. C., Lundin, L. G. & Schiöth, H. B. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63, 1256–1272 (2003).
Nordström, K., Larsson, T. A. & Larhammar, D. Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications. Genomics 83, 852–872 (2004). This paper summarizes the blocks of human phototransduction genes that are likely to have arisen from genome duplications in early vertebrate evolution.
Escriva, H., Manzon, L., Youson, J. & Laudet, V. Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol. Biol. Evol. 19, 1440–1450 (2002).
Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, 1700–1708 (2005).
Panopoulou, G. & Poustka, A. J. Timing and mechanism of ancient vertebrate genome duplications — the adventure of a hypothesis. Trends Genet. 21, 559–567 (2005).
Gerhart, J. Evolution of the organizer and the chordate body plan. Int. J. Dev. Biol. 45, 133–153 (2001).
Yu, J. K. et al. Axial patterning in cephalochordates and the evolution of the organizer. Nature 445, 613–617 (2007).
Holland, L. Z. & Holland, N. D. A revised fate map for amphioxus and the evolution of axial patterning in chordates. Integr. Comp. Biol. 47, 360–372 (2007).
Holmberg, K. in Handbook of Sensory Physiology, Vol. VII/5, The visual system of vertebrates (ed. Crescitelli, F.) 47–66 (Springer, Berlin, 1977). This paper provides an excellent summary of the ultrastructure of hagfish and lamprey eyes, providing a basis for comparison with jawed vertebrates.
Fritzsch, B. & Collin, S. P. Dendritic distribution of two populations of ganglion cells and the retinopetal fibers in the retina of the silver lamprey (Ichthyomyzon unicuspis). Vis. Neurosci. 4, 533–545 (1990).
Collin, S. P. et al. Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr. Biol. 13, R864–R865 (2003). This study presents the discovery in lampreys of five retinal opsins that are homologous to the four classes of cone opsin and rhodopsin in vertebrates.
Locket, N. A. & Jorgensen, J. M. in The Biology of Hagfishes (eds Jorgensen, J. M., Lomholt, J. P., Weber, R. E. & Malte, H.) 541–556 (Chapman and Hall, London, 1998). This paper provides the most comprehensive description of the eyes of hagfish.
Fernholm, B. & Holmberg, K. The eyes in three genera of hagfish (Eptatretus, Paramyxine and Myxine) — a case of degenerative evolution. Vision Res. 15, 253–259 (1975).
Kobayashi, H. On the photo-perceptive function in the eye of the hagfish, Myxine garmani Jordan et Snyder. J. Natl Fish. Univ. 13, 67–83 (1964).
Holmberg, K. The hagfish retina: fine structure of retinal cells in Myxine glutinosa, L., with special reference to receptor and epithelial cells. Z. Zellforsch. Mikrosk. Anat. 111, 519–538 (1970).
Holmberg, K. The hagfish retina: electron microscopic study comparing receptor and epithelial cells in Pacific hagfish, Polistotrema stouti, with those in Atlantic hagfish, Myxine glutinosa. Z. Zellforsch. Mikrosk. Anat. 121, 249–269 (1971).
Kusunoki, T. & Amemiya, F. Retinal projections in the hagfish, Eptatretus burgeri. Brain Res. 262, 295–298 (1983).
Wicht, H. & Northcutt, R. G. Retinofugal and retinopetal projections in the Pacific hagfish, Eptatretus stouti (Myxinoidea). Brain Behav. Evol. 36, 315–328 (1990).
Hattar, S. et al. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J. Comp. Neurol. 497, 326–349 (2006).
Vigh, B. et al. The pineal organ as a folded retina: immunocytochemical localization of opsins. Biol. Cell 90, 653–659 (1998).
Ekström, P. & Meissl, H. Evolution of photosensory pineal organs in new light: the fate of neuroendocrine photoreceptors. Philos. Trans. R. Soc. Lond. B Biol. 358, 1679–1700 (2003).
Newth, D. R. & Ross, D. M. On the reaction to light of Myxine glutinosa L. J. Exp. Biol. 32, 4–21 (1955).
Dickson, D. H. & Collard, T. R. Retinal development in the lamprey (Petromyzon marinus L.): pre-metamorphic ammocoete eye. Am. J. Anat. 154, 321–336 (1979).
Rubinson, K. & Cain, H. Neural differentiation in the retina of the larval sea lamprey (Petromyzon marinus). Vis. Neurosci. 3, 241–248 (1989).
Rubinson, K. The developing visual system and metamorphosis in the lamprey. J. Neurobiol. 21, 1123–1135 (1990).
Meyer-Rochow, V. B. & Stewart, D. Review of larval and postlarval eye ultrastructure in the lamprey (Cyclostomata) with special emphasis on Geotria australis (Gray). Microsc. Res. Tech. 35, 431–444 (1996).
Rapaport, D. H. in Retinal Development (eds Sernagor, E., Eglen, S., Harris, W. & Wong, R.) 30–58 (Cambridge Univ. Press, Cambridge, UK, 2006).
Dickson, D. H., Graves, D. A. & Moyles, M. R. Corneal splitting in the developing lamprey Petromyzon marinus L. eye. Am. J. Anat. 165, 83–98 (1982).
Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006). This paper presents a molecular–genetic analysis that reverses the earlier view that cephalochordates are closer to our own ancestors than are tunicates.
Dilly, N. Studies on the receptors in the cerebral vesicle of the ascidian tadpole. 2. The ocellus. Q. J. Microsc. Sci. 105, 13–20 (1964).
Eakin, R. M. & Kuda, A. Ultrastructure of sensory receptors in ascidian tadpoles. Z. Zellforsch. Mikrosk. Anat. 112, 287–312 (1971).
Barnes, S. N. Fine structure of the photoreceptor and cerebral ganglion of the tadpole larva of Amaroucium constellatum (Verril) (subphylum: Urochordata; class: Ascidiacea). Z. Zellforsch Mikrosk. Anat. 117, 1–16 (1971).
Gorman, A. L. F., McReynolds, J. S. & Barnes, S. N. Photoreceptors in primitive chordates: fine structure, hyperpolarizing receptor potentials, and evolution. Science 172, 1052–1054 (1971).
Kusakabe, T. et al. Ci-opsin1, a vertebrate-type opsin gene, expressed in the larval ocellus of the ascidian Ciona intestinalis. FEBS Lett. 506, 69–72 (2001).
Tsuda, M. et al. Origin of the vertebrate visual cycle: II. Visual cycle proteins are localized in whole brain including photoreceptor cells of a primitive chordate. Vis. Res. 43, 3045–3053 (2003).
D'Aniello, S. et al. The ascidian homolog of the vertebrate homeobox gene Rx is essential for ocellus development and function. Differentiation 74, 222–234 (2006).
Sato, S. & Yamamoto, H. Development of pigment cells in the brain of ascidian tadpole larvae: insights into the origins of vertebrate pigment cells. Pigment Cell Res. 14, 428–436 (2001).
Takimoto, N., Kusakabe, T., Horie, T., Miyamoto, Y. & Tsuda, M. Origin of the vertebrate visual cycle: III. Distinct distribution of RPE65 and β-carotene 15,15′-monooxygenase homologues in Ciona intestinalis. Photochem. Photobiol. 82, 1468–1474 (2006). This study is the third in a series of investigations into the origin of the isomerohydrolase (RPE65) enzyme in an early chordate organism.
Lacalli, T. C. Frontal eye circuitry, rostral sensory pathways and brain organization in amphioxus larvae: evidence from 3D reconstructions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 243–263 (1996).
Lacalli, T. C. Sensory systems in amphioxus: a window on the ancestral chordate condition. Brain Behav. Evol. 64, 148–162 (2004). This paper provides a summary of the rhabdomeric and ciliary photoreceptor organs in the primitive chordate amphioxus.
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. 531, 525–528 (2002).
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. 15, 1065–1069 (2005). This paper provides an examination of the homologue of rhabdomeric-like vertebrate opsin, melanopsin, which is found in the primitive chordate amphioxus, and of the link between invertebrates and vertebrates.
Schubert, M., Escriva, H., Xavier-Neto, J. & Laudet, V. Amphioxus and tunicates as evolutionary model systems. Trends Ecol. Evol. 21, 269–277 (2006).
Beaster-Jones, L., Horton, A. C., Gibson-Brown, J. J., Holland, N. D. & Holland, L. Z. The amphioxus T-box gene, AmphiTbx15/18/22, illuminates the origins of chordate segmentation. Evol. Dev. 8, 119–129 (2006).
Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W. & Wittbrodt, J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306, 869–871 (2004). This study presents the discovery that an invertebrate (protostome) species possessed ciliary photoreceptors expressing a ciliary opsin, in addition to rhabdomeric photoreceptors expressing a rhabdomeric opsin.
Yokoyama, S. Molecular evolution of vertebrate visual pigments. Prog. Retin. Eye Res. 19, 385–419 (2000).
Nasi, E., del Pilar Gomez, M. & Payne, R. in Molecular Mechanisms of Visual Transduction (eds Stavenga, D. G., de Grip, W. J. & Pugh, E. N. J.) 389–448 (Elsevier, Amsterdam, 2000).
Velarde, R. A., Sauer, C. D., Walden, K. K. O., Fahrbach, S. E. & Robertson, H. M. Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochem. Mol. Biol. 35, 1367–1377 (2005).
Arendt, D., Tessmar, K., de Campos-Baptista, M. I. M., Dorresteijn, A. & Wittbrodt, J. Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 129, 1143–1154 (2002).
Imai, J. H. & Meinertzhagen, I. A. Neurons of the ascidian larval nervous system in Ciona intestinalis: I. Central nervous system. J. Comp. Neurol. 501, 316–334 (2007).
Pu, G. A. & Dowling, J. E. Anatomical and physiological characteristics of pineal photoreceptor cell in the larval lamprey, Petromyzon marinus. J. Neurophysiol. 46, 1018–1038 (1981).
Samejima, M., Tamotsu, S., Watanabe, K. & Morita, Y. Photoreceptor cells and neural elements with long axonal processes in the pineal organ of the lamprey, Lampetra japonica, identified by use of the horseradish peroxidase method. Cell Tissue Res. 258, 219–224 (1989).
Govardovskii, V. I. & Lychakov, D. V. Visual cells and visual pigments of the lamprey, Lampetra fluviatilis. J. Comp. Physiol. A 154, 279–286 (1984).
Collin, S. P., Potter, I. C. & Braekevelt, C. R. The ocular morphology of the southern hemisphere lamprey Geotria australis Gray, with special reference to optical specialisations and the characterisation and phylogeny of photoreceptor types. Brain Behav. Evol. 54, 96–118 (1999).
Collin, S. P. & Potter, I. C. The ocular morphology of the southern hemisphere lamprey Mordacia mordax Richardson with special reference to a single class of photoreceptor and a retinal tapetum. Brain Behav. Evol. 55, 120–138 (2000).
Collin, S. P., Hart, N. S., Shand, J. & Potter, I. C. Morphology and spectral absorption characteristics of retinal photoreceptors in the southern hemisphere lamprey (Geotria australis). Vis. Neurosci. 20, 119–30 (2003).
Collin, S. P., Hart, N. S., Wallace, K. M., Shand, J. & Potter, I. C. Vision in the southern hemisphere lamprey Mordacia mordax: spatial distribution, spectral absorption characteristics, and optical sensitivity of a single class of retinal photoreceptor. Vis. Neurosci. 21, 765–773 (2004).
Collin, S. P. & Trezise, A. E. The origins of colour vision in vertebrates. Clin. Exp. Optom. 87, 217–23 (2004).
Holmberg, K. & Öhman, P. Fine structure of retinal synaptic organelles in lamprey and hagfish photoreceptors. Vision Res. 16, 237–239 (1976).
Vollrath, L., Meyer, A. & Buschmann, F. Ribbon synapses of the mammalian retina contain two types of synaptic bodies — ribbons and spheres. J. Neurocytol. 18, 115–120 (1989).
Wagner, H.-J. Presynaptic bodies (“ribbons”): from ultrastructural observations to molecular perspectives. Cell Tissue Res. 287, 435–446 (1997).
Davies, W. L. et al. Functional characterization, tuning, and regulation of visual pigment gene expression in an anadromous lamprey. FASEB J. 21, 2713–2724 (2007).
Hisatomi, O. & Tokunaga, F. Molecular evolution of proteins involved in vertebrate phototransduction. Comp. Biochem. Physiol. Biochem. Mol. Biol. 133, 509–522 (2002).
Shichida, Y. & Yamashita, T. Diversity of visual pigments from the viewpoint of G protein activation — comparison with other G protein-coupled receptors. Photochem. Photobiol. Sci. 2, 1237–1246 (2003).
Terakita, A. The opsins. Genome Biol. 6, 213 (2005).
Okano, T., Kojima, D., Fukada, Y., Shichida, Y. & Yoshizawa, T. Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc. Natl Acad. Sci. USA 89, 5932–5936 (1992).
Kuwayama, S., Imai, H., Hirano, T., Terakita, A. & Shichida, Y. Conserved proline residue at position 189 in cone visual pigments as a determinant of molecular properties different from rhodopsins. Biochemistry 41, 15245–15252 (2002).
Terakita, A. et al. Counterion displacement in the molecular evolution of the rhodopsin family. Nature Struct. Mol. Biol. 11, 284–289 (2004).
Imai, H. et al. Molecular properties of rod and cone visual pigments from purified chicken cone pigments to mouse rhodopsin in situ. Photochem. Photobiol. Sci. 4, 667–674 (2005). This paper provides an excellent summary of the molecular properties that distinguish cone opsins from rhodopsin.
Kuwayama, S., Imai, H., Morizumi, T. & Shichida, Y. Amino acid residues responsible for the meta-III decay rates in rod and cone visual pigments. Biochemistry 44, 2208–2215 (2005).
Okano, T., Yoshizawa, T. & Fukada, Y. Pinopsin is a chicken pineal photoreceptive molecule. Nature 372, 94–97 (1994).
Sun, H., Gilbert, D. J., Copeland, N. G., Jenkins, N. A. & Nathans, J. Peropsin, a novel visual pigment-like protein located in the apical microvilli of the retinal pigment epithelium. Proc. Natl Acad. Sci. USA 94, 9893–9898 (1997).
Koyanagi, M. et al. Bistable UV pigment in the lamprey pineal. Proc. Natl Acad. Sci. USA 101, 6687–6691 (2004).
Su, C. Y. et al. Parietal-eye phototransduction components and their potential evolutionary implications. Science 311, 1617–1621 (2006).
Carleton, K. L., Spady, T. C. & Cote, R. H. Rod and cone opsin families differ in spectral tuning domains but not signal transducing domains as judged by saturated evolutionary trace analysis. J. Mol. Evol. 61, 75–89 (2005).
Fu, Y. B. et al. Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proc. Natl Acad. Sci. USA 102, 10339–10344 (2005).
Chaurasia, S. S. et al. Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J. Neurochem. 92, 158–170 (2005).
Kumbalasiri, T. & Provencio, I. Melanopsin and other novel mammalian opsins. Exp. Eye Res. 81, 368–375 (2005).
Yan, E. C. Y. et al. Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl Acad. Sci. USA 100, 9262–9267 (2003).
Wang, Z., Asenjo, A. B. & Oprian, D. D. Identification of the Cl−-binding site in the human red and green color vision pigments. Biochemistry 32, 2125–2130 (1993).
Hunt, D. M. et al. in Vision Down Under 2007 (Cairns, Australia, 2007).
von Baer, K. E. Über Entwickelungsgeschichte der Thiere (Bei den Gebrüdern Bornträger, Königsburg, 1828).
Haeckel, E. H. Natürliche Schöpfungsgeschichte (1868).
Valleix, S. et al. Homozygous nonsense mutation in the FOXE3 gene as a cause of congenital primary aphakia in humans. Am. J. Hum. Genet. 79, 358–364 (2006).
England, S. J., Blanchard, G. B., Mahadevan, L. & Adams, R. J. A dynamic fate map of the forebrain shows how vertebrate eyes form and explains two causes of cyclopia. Development 133, 4613–4617 (2006). By following the trajectories of individual identified cells, the authors of this study were able to track the morphological development of the zebrafish eye. This paper contains some excellent animations.
Assheton, R. On the development of the optic nerve of vertebrates, and the choroidal fissure of embryonic life. Q. J. Microsc. Sci. 34, 84–104 (1892).
Reichenbach, A. & Robinson, S. R. Phylogenetic constraints on retinal organisation and development. Prog. Retin. Eye Res. 15, 139–171 (1995). This paper provides an excellent review of vertebrate eye evolution and development that, when first published, was far ahead of its time.
Vigh, B. et al. Nonvisual photoreceptors of the deep brain, pineal organs and retina. Histol. Histopathol. 17, 555–590 (2002).
Klein, D. C. Evolution of the vertebrate pineal gland: the AANAT hypothesis. Chronobiol. Int. 23, 5–20 (2006).
Mano, H. & Fukada, Y. A median third eye: pineal gland retraces evolution of vertebrate photoreceptive organs. Photochem. Photobiol. 83, 11–18 (2007).
Turner, D. L. & Cepko, C. L. A common progenitor for neurons and glia persists in rat retina late in development. Nature 328, 131–136 (1987).
Holt, C. E., Bertsch, T. W., Ellis, H. M. & Harris, W. A. Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1, 15–26 (1988).
Wetts, R. & Fraser, S. E. Multipotent precursors can give rise to all major cell types of the frog retina. Science 239, 1142–1145 (1988).
Livesey, F. J. & Cepko, C. L. Vertebrate neural cell-fate determination: lessons from the retina. Nature Rev. Neurosci. 2, 109–118 (2001).
Blackshaw, S. et al. Genomic analysis of mouse retinal development. PLoS Biol. 2, 1411–1431 (2004).
Poggi, L., Vitorino, M., Masai, I. & Harris, W. A. Influences on neural lineage and mode of division in the zebrafish retina in vivo. J. Cell Biol. 171, 991–999 (2005).
Cayouette, M., Poggi, L. & Harris, W. A. Lineage in the vertebrate retina. Trends Neurosci. 29, 563–570 (2006).
Sernagor, E., Eglen, S., Harris, B. & Wong, R. Retinal Development (Cambridge Univ. Press, Cambridge, UK, 2006).
Johnson, P. T., Williams, R. R., Cusato, K. & Reese, B. E. Rods and cones project to the inner plexiform layer during development. J. Comp. Neurol. 414, 1–12 (1999).
Reese, B. E. Developmental plasticity of photoreceptors. Prog. Brain Res. 144, 3–19 (2004). Along with reference 126, this paper presents evidence that, during mammalian retinal development, connections form from photoreceptors directly to the IPL, before subsequently being retracted — an important phenomenon that is widely overlooked.
Dávid, C., Frank, C. L., Lukáts, A., Szél, A. & Vígh, B. Cerebrospinal fluid contacting neurons in the reduced brain ventricular system of the Atlantic hagfish, Myxine glutinosa. Acta Biol. Hung. 54, 35–44 (2003).
García-Fernández, J. M. & Foster, R. G. Immunocytochemical identification of photoreceptor proteins in hypothalamic cerebrospinal fluid contacting neurons of the larval lamprey (Petromyzon marinus). Cell Tissue Res. 275, 319–326 (1994).
Mariani, A. P. Biplexiform cells: ganglion cells of the primate retina that contact photoreceptors. Science 216, 1134–1136 (1982).
Straznicky, C. & Gabriel, R. Synapses of biplexiform ganglion cells in the outer plexiform layer of the retina in Xenopus laevis. J. Brain Res. 36, 135–141 (1995).
Rio, J. P., Vesselkin, N. P., Repérant, J., Kenigfest, N. B. & Versaux-Botteri, C. Lamprey ganglion cells contact photoreceptor cells. Neurosci. Lett. 250, 103–106 (1998).
Pushchin, I. I. & Kondrashev, S. L. Biplexiform ganglion cells in the retina of the perciform fish Pholidapus dybowskii revealed by HRP labeling from the optic nerve and optic tectum. Vision Res. 43, 1117–1133 (2003).
Nilsson, D.-E. & Pelger, S. A pessimistic estimate of the time required for an eye to evolve. Proc. Biol. Sci. 256, 53–58 (1994).
Delarbre, C., Gallut, C., Barriel, V., Janvier, P. & Gachelin, G. Complete mitochondrial DNA of the hagfish, Eptatretus burgeri: the comparative analysis of mitochondrial DNA sequences strongly supports the cyclostome monophyly. Mol. Phylogenet. Evol. 22, 184–192 (2002).
Takezaki, N., Figueroa, F., Zaleska-Rutczynska, Z. & Klein, J. Molecular phylogeny of early vertebrates: monophyly of the Agnathans as revealed by sequences of 35 genes. Mol. Biol. Evol. 20, 287–292 (2003).
Blair, J. E. & Hedges, S. B. Molecular phylogeny and divergence times of deuterostome animals. Mol. Biol. Evol. 22, 2275–2284 (2005).
Kuraku, S. & Kuratani, S. Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zool. Sci. 23, 1053–1064 (2006).
Bourlat, S. J. et al. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444, 85–88 (2006).
Janvier, P. Evolutionary biology: born-again hagfishes. Nature 446, 622–623 (2007).
Janvier, P. in Major Transitions in Vertebrate Evolution (eds Anderson, J. S. & Sues, H.-D.) 57–121 (Indiana Univ. Press, Bloomington, USA, 2007).
Ota, K. G., Kuraku, S. & Kuratani, S. Hagfish embryology with reference to the evolution of the neural crest. Nature 446, 672–675 (2007). This study presented a remarkable breakthrough in the investigation of hagfish embryology that provided unequivocal evidence for neural crest cells.
Wagner, H. J., Frohlich, E., Negishi, K. & Collin, S. P. The eyes of deep-sea fish II. Functional morphology of the retina. Prog. Retin. Eye Res. 17, 637–685 (1998).
Janvier, P. Vertebrate characters and the Cambrian vertebrates. C. R. Palevol 2, 523–531 (2003).
Wicht, H. & Northcutt, R. G. Ontogeny of the head of the Pacific hagfish (Eptatretus stouti, Myxinoidea): development of the lateral line system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 349, 119–134 (1995).
Miyata, T. & Suga, H. Divergence pattern of animal gene families and relationship with the Cambrian explosion. Bioessays 23, 1018–1027 (2001).
Nakashima, Y. et al. Origin of the vertebrate visual cycle: genes encoding retinal photoisomerase and two putative visual cycle proteins are expressed in whole brain of a primitive chordate. J. Comp. Neurol. 460, 180–190 (2003).
Kojima, D. et al. Novel Go-mediated phototransduction cascade in scallop visual cells. J. Biol. Chem. 272, 22979–22982 (1997).
Walls, G. L. The Vertebrate Eye and its Adaptive Radiation (Hafner, New York, 1942).
Vigh, B., Vigh-Teichmann, I., Röhlich, P. & Oksche, A. Cerebrospinal fluid-contacting neurons, sensory pinealocytes and Landolts clubs of the retina as revealed by means of an electron-microscopic immunoreaction against opsin. Cell Tissue Res. 233, 539–548 (1983).
McCauley, D. W. & Bronner-Fraser, M. Conservation of Pax gene expression in ectodermal placodes of the lamprey. Gene 287, 129–139 (2002).
Fritzsch, B., Sonntag, R., Dubuc, R., Ohta, Y. & Grillner, S. Organization of the six motor nuclei innervating the ocular muscles in lamprey. J. Comp. Neurol. 294, 491–506 (1990).
Bullock, T. H., Moore, J. K. & Fields, R. D. Evolution of myelin sheaths: both lamprey and hagfish lack myelin. Neurosci. Lett. 48, 145–148 (1984).
Kolb, H. & Famiglietti, E. V. Rod and cone pathways in inner plexiform layer of cat retina. Science 186, 47–49 (1974).
Wong, R. O. L., Henry, G. H. & Medveczky, C. J. Bistratified amacrine cells in the retina of the tammar wallaby - Macropus eugenii. Exp. Brain Res. 63, 102–105 (1986).
Kuchnow, K. P. Elasmobranch pupillary response. Vision Res. 11, 1395–1406 (1971).
Sivak, J. G. & Gilbert, P. W. Refractive and histological study of accommodation in two species of sharks (Ginglymostoma cirratum and Carcharhinus milberti). Can. J. Zool. 54, 1811–1817 (1976).
Sivak, J. G., Levy, B., Weber, A. P. & Glover, R. F. Environmental influence on shape of the crystalline lens — the amphibian example. Exp. Biol. 44, 29–40 (1985).
Jacobs, G. H. & Rowe, M. P. Evolution of vertebrate colour vision. Clin. Exp. Optom. 87, 206–216 (2004).
Conway Morris, S. The fossil record and the early evolution of the Metazoa. Nature 361, 219–225 (1993).
Peterson, K. J. & Butterfield, N. J. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proc. Natl Acad. Sci. USA 102, 9547–9552 (2005).
Janvier, P., Desbiens, S., Willett, J. A. & Arsenault, M. Lamprey-like gills in a gnathostome-related Devonian jawless vertebrate. Nature 440, 1183–1185 (2006).
Botella, H., Blom, H., Dorka, M., Ahlberg, P. E. & Janvier, P. Jaws and teeth of the earliest bony fishes. Nature 448, 583–586 (2007).
Stadler, P. F. et al. Evidence for independent Hox gene duplications in the hagfish lineage: a PCR-based gene inventory of Eptatretus stoutii. Mol. Phylogenet. Evol. 32, 686–694 (2004).
Houseman, J. External features of the anterior region of amphioxus, the lancelet. BIODIDAC [online]
McGrouther, M. Head of a broadgilled hagfish. Australian Museum [online] (2006).
Collin, S. P. & Trezise, A. E. O. in Communication in Fishes (eds Ladich, F., Collin, S. P., Moller, P. & Kapoor, B. G.) 303–335 (Science Publishers, 2006).
Steinberg, R. H., Fisher, S. K. & Anderson, D. H. Disk morphogenesis in vertebrate photoreceptors. J. Comp. Neurol. 190, 501–518 (1980).
Vigh, B., Debreceni, K., Fejer, Z. & Vigh-Teichmann, I. Immunoreactive excitatory amino acids in the parietal eye of lizards, a comparison with the pineal organ and retina. Cell Tissue Res. 287, 275–283 (1997).
Raviola, E. & Gilula, N. B. Intramembrane organization of specialized contacts in outer plexiform layer of retina — a freeze-fracture study in monkeys and rabbits. J. Cell Biol. 65, 192–222 (1975).
Hardie, R. C. & Raghu, P. Visual transduction in Drosophila. Nature 413, 186–193 (2001).
Burns, M. E. & Lamb, T. D. in The Visual Neurosciences (eds Chalupa, L. M. & Werner, J. S.) 215–233 (MIT Press, Cambridge, Massachusetts, 2003).
Dreher, B. & Robinson, S. R. Development of the retinofugal pathway in birds and mammals: evidence for a common 'timetable'. Brain Behav. Evol. 31, 369–390 (1988).
Johnson, P. T., Raven, M. A. & Reese, B. E. Disruption of transient photoreceptor targeting within the inner plexiform layer following early ablation of cholinergic amacrine cells in the ferret. Vis. Neurosci. 18, 741–751 (2001).
We wish to thank T. Cronin, I. Meinertzhagen, S. Conway Morris and P. Janvier for constructive comments on the manuscript. This work was supported by the Australian Research Council (FF0344672; T.D.L. and S.P.C.) and by the US National Institutes of Health and the Research to Prevent Blindness Foundation (E.N.P.).
Proteins homologous to rhodopsin that comprise seven α-helical transmembrane regions and covalently bind retinaldehyde (the chromophore, a vitamin A derivative). In addition to retinal opsins, which function as G-protein-coupled receptors, there are many non-visual opsins, including molecules that might act as photoisomerases, using light to convert all-trans retinaldehyde to its 11-cis isomer.
An animal belonging to the protostome super-phylum, which is characterized by its members' embryonic development, in which the first opening (the blastopore) becomes the mouth (protostome is Greek for 'first mouth'). All protostomes are invertebrates.
An animal belonging to the deuterostome super-phylum of the animal kingdom, which is characterized by its members' embryonic development, in which the first opening (the blastopore) becomes the anus (deuterostome is Greek for 'second mouth'). In addition to the chordate phylum (which includeds vertebrates), the other two main phyla are the echinoderm phylum and the hemichordate phylum.
An animal belonging to the chordate phylum, which comprises vertebrates, tunicates and cephalochordates. These animals are characterized by the presence of a notochord, a dorsal-nerve cord and pharyngeal slits or pouches.
A jawless fish within the chordate phylum (agnatha is Greek for 'no jaw'). The two extant groups are hagfish and lampreys.
The jawed vertebrates (gnathostome is Greek for 'jaw mouth'), comprising fish and tetrapods (including birds and mammals).
- Vertebrate organizer
An evolutionarily conserved region of the developing vertebrate embryo that specifies the patterning of the embryonic axis.
- Extraocular and intraocular muscles
In jawed vertebrates, extraocular muscles orientate the eyeball in its orbit, whereas intraocular muscles focus the lens and adjust the pupil. In lampreys, the extraocular muscles perform the focusing by changing the curvature of the cornea.
- Bipolar cells
Retinal neurons that convey information from photoreceptors to the output neurons, retinal ganglion cells.
- Horizontal cells
Large retinal neurons that mediate lateral interactions at the outer plexiform layer by contacting both photoreceptors and bipolar cells.
- Amacrine cells
A diverse class of retinal neurons that make synaptic contacts at the inner plexiform layer and are involved in a number of different processing functions involving bipolar cells and ganglion cells.
- Ganglion cells
The output neurons of the retina, the axons of which form the optic nerve and transmit information to the visual centres of the brain.
- Pineal organ
Also known as the epiphysis. A protrusion from the dorsal surface of the diencephalon that is involved in the secretion of melatonin and the regulation of circadian rhythms. In non-mammalian vertebrates the pineal contains photoreceptors that are homologous to those in the retina of higher species, but in mammals the corresponding cells do not have outer segments and are not intrinsically light-sensitive.
Also known as lancelets. Members of the cephalochordate sub-phylum, and perhaps the most basal members of the chordates.
- Ciona intestinalis
A well studied member of the ascidian class.
Commonly known as sea-squirts. A class within the tunicate sub-phylum. The larval form is tadpole-shaped and possesses a simple nervous system.
In both ciliary and rhabdomeric photoreceptors, phototransduction is mediated by a photoactivated opsin (a G-protein-coupled receptor) activating a G protein. In vertebrate photoreceptors the G protein activates a phosphodiesterase that hydrolyses cyclic GMP in the cytoplasm, leading to the closure of ion channels in the plasma membrane. Shut-off is mediated by phosphorylation of the opsin followed by the binding of a capping protein, arrestin.
- Retinal pigment epithelium
The pigmented monolayer of cells intervening between the retina and the choroidal circulation, that serves multiple functions in recycling retinoid, phagocytosing the apical tips of the outer segments, absorbing light that passes through the retina, etc. In hagfish the retinal epithelium is not pigmented.
- Retinoid cycle
In both ciliary and rhabdomeric photoreceptors the chromophore 11-cis retinaldehyde is isomerized by light to the all-trans isomer, thereby activating the opsin. In ciliary photoreceptors the isomerized retinaldehyde is released from opsin and undergoes a complicated cycle (the retinoid cycle) of transport and multiple chemical reactions through which it is isomerized back to the 11-cis isomer.
- Ribbon synapse
A specialized structure in vertebrate sensory neurons that use graded voltage changes rather than action potentials; these sensory neurons include photoreceptors, retinal bipolar cells, hair cells and electroreceptors. Ribbon synapses might act as conduits for conveying synaptic vesicles to release sites.
- Schiff base
A class of chemical bond that covalently links the retinaldehyde chromophore of visual pigments to the terminal amino group of a lysine residue in the opsin protein.
A localized area of the epithelial surface of the developing embryo where an organ or structure subsequently develops. The lens placode both develops into a lens and induces the underlying optic vesicle to invaginate to form the eye cup.
- Choroid fissure
The gap between the two edges of the developing eye cup, as it expands circumferentially but before it seals over. It is through this opening that the axons of retinal ganglion cells exit the eye to form the optic nerve and the retinal vessels enter. Eventually the fissure disappears, once the edges of the retina join.
- Parapineal organ
A pineal-like organ that lies adjacent to the pineal organ in the brains of some vertebrates.
- Parietal eye
The so-called 'third eye' of certain vertebrates, which is part of the pineal complex and exhibits homology to the pineal organ and to the retina. It contains photoreceptors and regulates circadian rhythms.
- Müller cell
A type of radial glial cell that provides support and nutrition in the retina. These cells appear to have an important (although not fully understood) role in the embryological development of the retina.
- ON pathway
The pathway through the retina, comprising ON-bipolar cells and ON-ganglion cells, that is activated by an increment in light intensity. It is complemented by the OFF-pathway, which is activated by a decrement in light intensity.
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Lamb, T., Collin, S. & Pugh, E. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8, 960–976 (2007). https://doi.org/10.1038/nrn2283
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