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Review
. 2007 Dec;8(12):960-76.
doi: 10.1038/nrn2283.

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

Trevor D Lamb  1 , Shaun P Collin, Edward N Pugh Jr
Affiliations
Review

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

Trevor D Lamb et al. Nat Rev Neurosci. 2007 Dec.

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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Figures

Figure 1
Figure 1. The origin of vertebrates
The evolution of jawed vertebrates is illustrated against an approximate time-scale of millions of years ago (Mya). The taxa considered in this Review are indicated with an asterisk and are accompanied by schematics and diagrams of the ‘eye’ region. The earliest chordates, represented by extant cephalochordates and tunicates, are thought to have appeared around 550 Mya. Jawless craniates (agnathans) were present in the early Cambrian, by 525 Mya, and a time of 530 Mya has been indicated for their presumed first appearance. As elaborated on in BOX 1, there is considerable controversy as to whether myxiniformes (solely represented by extant hagfish) diverged before or after the separation of lampreys from jawed vertebrates (shown as dashed black and grey lines). Numerous lines of jawless fish evolved between 500 and 430 Mya ago, although none have survived to the present day. The first jawed vertebrate arose around 430 Mya, and this line is represented today by cartilagenous fish, bony fish and tetrapods. Six ‘stages of interest’ in vertebrate eye evolution correspond to the time intervals between the divergence of important surviving taxa. This diagram does not include the evolutionary changes that have occurred in the last 400 million years. The presented timeline is based primarily on evidence from the fossil record; see REFS ,,,,,,–. The schematics are modified, with permission, from REF. © (1996) Oxford University Press (lancelet, sea squirt, hagfish and lamprey) and REF. © (2004) Academic Press (jawed vertebrate). The eye images are reproduced, with permission, from the following references: lancelet, REF. © BIODIDAC (1996) University of California Museum of Paleontology; sea squirt, REF. © (2006) Blackwell Publishing; hagfish, REF. © (2006) Australian Museum. Lamprey and jawed vertebrate eye images are courtesy of G. Westhoff and S. P. Collin).
Figure 2
Figure 2. The structure of ciliary photoreceptors at various stages of chordate/vertebrate evolution
The middle row shows schematic diagrams of the entire photoreceptor; the top and bottom rows show electron micrographs of the outer segment and the synaptic terminal, respectively. Note the gradual transition towards a highly organized laminar structure in the outer segment and the appearance of ribbons in the synaptic terminal. The schematics are modified with permission from, and the micrographs are reproduced with permission from, the following references: ascidian larva (schematic), REF. © (1971) Springer Verlag; ascidian larva (outer segment), REF. © (1971) Springer Verlag; hagfish eye, REF. © (1971) Springer Verlag; larval lamprey pineal, REF. © (1981) American Physiological Society; adult lamprey retina, REF. © (2006) Science Publishers; gnathostome retina (outer segment), REF. © (1980) Wiley-Liss; gnathostome retina (schematic), REF. © (1997) Springer Verlag; gnathostome retina (synaptic terminal), REF. © (1975) Rockerfeller University Press.
Figure 3
Figure 3. The evolution of vertebrate opsins
On the left of the main figure is a dendrogram of the major opsin classes that are relevant to the evolution of the vertebrate eye. Before the separation of protostomes and deuterostomes, the primordial opsin had already diverged into three main classes: rhabdomeric opsins, which are characteristic of protostome rhabdomeric photoreceptors (see upper photoreceptor schematic) but are also found in melanopsin-containing vertebrate retinal ganglion cells; ‘photoisomerase’ opsins, such as retinal G-protein-coupled receptor (RGR) opsin and peropsin, which may in fact be G-protein-coupled receptors; and ciliary opsins (see lower photoreceptor schematic), which are characteristic of those photoreceptors in which the pigment-containing region is an expansion of the membrane of a cilium. Vertebrate retinal opsins are represented by the lowermost six rows in the diagram. The primordial retinal opsin of vertebrates diverged into long-wavelength sensitive (LWS) and short-wavelength-sensitive (SWS) branches, and then the latter split into several sub-groups: SWS1, SWS2 and Rh2/RhB, each of which is associated with cone-like photoreceptors. The Rh1 pigment of jawed vertebrates (bottom line) seems to represent the most recent development among these classes, and is expressed in vertebrate rod photoreceptors. A separate class of rod, the ‘green rod’ of non-mammalian vertebrates, uses the SWS2 pigment that is also present in the blue-sensitive cones of these species. On the right of the main figure are presumed classes of G-protein coupling mechanism, residues at four important locations (in the numbering system for bovine rhodopsin; blue and green shading highlights residue similarity; pink shading highlights a chloride-binding site), and the regional expression of the opsins in vertebrate tissues. AC, amacrine cell; GC, ganglion cell; HC, horizontal cell; RPE, retinal pigment epithelium; VA, vertebrate ancient. The dendrogram is a composite, based on data from REFS ,,,, and elsewhere. The schematic of the rhabdomeric photoreceptor is modified, with permission, from REF. © (2001) Macmillan Publishers Ltd. The schematic of the ciliary photoreceptor is modified, with permission, from REF. © (2003) MIT Press.
Figure 4
Figure 4. Development of the vertebrate eye cup
a | The neural plate is the starting point for the development of the vertebrate eye cup. b | The neural plate folds upwards and inwards. c | The optic grooves evaginate. d | The lips of the neural folds approach each other and the optic vesicles bulge outwards. e | After the lips have sealed the neural tube is pinched off. At this stage the forebrain grows upwards and the optic vesicles continue to balloon outwards: they contact the surface ectoderm and induce the lens placode. f | The optic vesicle now invaginates, so that the future retina is apposed to the future retinal pigment epithelium (RPE), and the ventricular space that was between them disappears. Developing retinal ganglion cells send axons out across the retinal surface. The surface ectoderm at the lens placode begins to form the lens pit. This section is midline in the right eye, through the choroid fissure, so only the upper region of the retina and the RPE are visible. g | The eye cup grows circumferentially, eventually sealing over the choroidal fissure and enclosing the axons of the optic nerve (as well as the hyaloid/retinal vessels; not shown). The ectodermal tissue continues to differentiate and eventually forms the lens. This figure is animated online (see Supplementary information S1).
Figure 5
Figure 5. The development of retinal neurons and circuitry
a | The cell cycle in the vertebrate retina. The soma of a replicating cell migrates between the outer (ventricular) surface, where mitosis (M) occurs, and the inner (vitread) surface. b | The sequential birth of cell classes in the vertebrate retina, with timings indicated for the ferret in both post-natal weeks and caecal time (that is, the time relative to eye opening), which is probably a better comparator for other species. c–e | The maturation of neural connectivity in the retina,, (again, timings are for the ferret). c | Initially photoreceptors (which exhibit few adult morphological characteristics) send transient processes to the inner plexiform layer (IPL), where they make synaptic contacts with the two sub-laminae. d | Subsequently these processes retract, and developing bipolar cells insert themselves into the pathway between the photoreceptors and the inner nuclear layer (INL). e | At a later stage, the rod and cone photoreceptors develop inner segments (IS) and outer segments (OS). A, amacrine cell; B, bipolar cell; C, cone photoreceptor cell; G, ganglion cell; H, horizontal cell; ILM, inner limiting membrane; OLM, outer limiting membrane; OPL, outer plexiform layer; R, rod photoreceptor cell.
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