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Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup

Key Points

  • 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.

Abstract

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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Figure 1: The origin of vertebrates.
Figure 2: The structure of ciliary photoreceptors at various stages of chordate/vertebrate evolution.
Figure 3: The evolution of vertebrate opsins.
Figure 4: Development of the vertebrate eye cup.
Figure 5: development of retinal neurons and circuitry.

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Acknowledgements

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.).

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Glossary

Opsins

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.

Protostome

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.

Deuterostome

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.

Chordate

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.

Agnathan

A jawless fish within the chordate phylum (agnatha is Greek for 'no jaw'). The two extant groups are hagfish and lampreys.

Gnathostome

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.

Amphioxus

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.

Ascidia

Commonly known as sea-squirts. A class within the tunicate sub-phylum. The larval form is tadpole-shaped and possesses a simple nervous system.

Phototransduction

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.

Placode

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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