Evolution of vertebrate retinal photoreception

Abstract

Recent findings shed light on the steps underlying the evolution of vertebrate photoreceptors and retina. Vertebrate ciliary photoreceptors are not as wholly distinct from invertebrate rhabdomeric photoreceptors as is sometimes thought. Recent information on the phylogenies of ciliary and rhabdomeric opsins has helped in constructing the likely routes followed during evolution. Clues to the factors that led the early vertebrate retina to become invaginated can be obtained by combining recent knowledge about the origin of the pathway for dark re-isomerization of retinoids with knowledge of the inability of ciliary opsins to undergo photoreversal, along with consideration of the constraints imposed under the very low light levels in the deep ocean. Investigation of the origin of cell classes in the vertebrate retina provides support for the notion that cones, rods and bipolar cells all originated from a primordial ciliary photoreceptor, whereas ganglion cells, amacrine cells and horizontal cells all originated from rhabdomeric photoreceptors. Knowledge of the molecular differences between cones and rods, together with knowledge of the scotopic signalling pathway, provides an understanding of the evolution of rods and of the rods' retinal circuitry. Accordingly, it has been possible to propose a plausible scenario for the sequence of evolutionary steps that led to the emergence of vertebrate photoreceptors and retina.

Figure 1.

Conservation of cell polarity and topology between Drosophila rhabdomeric and mammalian ciliary photoreceptor cells (see text). r, rhabdome; s, fly stalk; ZA, zonula adherens; os, outer segment; cc, connecting cilium; is, inner segment; ELM, external limiting membrane; N, nucleus. Adapted with permission from Ready & Tepass (2004).

Figure 2.

Ciliary opsins. (a) Simplified phylogenetic tree of animal opsins based on Suga et al. (2008); r denotes (rhabdomeric) r-opsins; c denotes (ciliary) c-opsins. Mauve background indicates those opsin classes that are discussed in the text. (b) Phylogenetic relationship of chordate ciliary opsins, summarizing a consensus view from a number of studies (including Okano et al. 1992, 1994; Yokoyama 2000; Kusakabe et al. 2001; Collin et al. 2003; Carleton et al. 2005; Kozmik et al. 2008; Peirson et al. 2009; Shichida & Matsuyama 2009). (c) Notable amino acid residues that assist in distinguishing the properties of chordate ciliary opsins. Numbering is according to bovine rhodopsin; coloured shading is simply to aid visualization of groupings.

Figure 3.

Schematic wiring diagram of the mammalian retina, emphasizing the rod (scotopic) pathways. Left, ON pathways. Right, OFF pathways. Cone circuitry is indicated using just two cone photoreceptors; that in the left half is shown connecting via an ON cone bipolar cell to an ON ganglion cell; that in the right half is shown connecting via an OFF cone bipolar cell to an OFF ganglion cell. The rod pathways are described in the text. Adapted with permission from Wässle (2004).