Eye evolution: common use and independent recruitment of genetic components

Abstract

Animal eyes can vary in complexity ranging from a single photoreceptor cell shaded by a pigment cell to elaborate arrays of these basic units, which allow image formation in compound eyes of insects or camera-type eyes of vertebrates. The evolution of the eye requires involvement of several distinct components-photoreceptors, screening pigment and genes orchestrating their proper temporal and spatial organization. Analysis of particular genetic and biochemical components shows that many evolutionary processes have participated in eye evolution. Multiple examples of co-option of crystallins, Galpha protein subunits and screening pigments contrast with the conserved role of opsins and a set of transcription factors governing eye development in distantly related animal phyla. The direct regulation of essential photoreceptor genes by these factors suggests that this regulatory relationship might have been already established in the ancestral photoreceptor cell.

Figure 1.

A schematic diagram of opsin distribution among eyes in different animal phyla. Particular opsins subfamilies are distinguished by different colouring. The lines leading to different phyla depict the hypothetical evolutionary fate of given opsin lineage based on available genomic and other data. The question mark denotes such animals where the presence of a given opsin lineage has not been confirmed yet. The colour of the eye-like pictogram corresponds to the type of photoreceptor cell employed in the eye. The class of opsin employed in the eye is represented by the colour of the rectangle next to the eye-like pictogram. If known, the Gα subunit interacting with the opsin is shown. Note that a small subset of vertebrate retinal ganglion cells expresses melanopsin coupled to a Gq signalling cascade (Panda et al. 2005). Although these cells fulfil the definition of a minimal eye, they are not the major photoreceptors of the eye and are not considered in this figure.

Figure 2.

A schematic diagram of distribution of screening pigments in different animal phyla. The photoreceptor cell type screened by particular pigments is depicted on the left side of the box of each phylum. There is no apparent correlation between the photoreceptor cell type and shielding pigment used. Note the unknown type of photoreceptor and unique deployment of haemoglobin as a shielding pigment of nematode Mermis, caused probably by independent origin of the eye in this organism. See electronic supplementary material for further details and references.

Figure 3.

Dual role of transcription factors in regulation of both eye development and differentiation genes. The box on the left-hand side represents the sum of largely unknown developmental genes regulated by corresponding transcription factors based on functional data. The letters represent different animals (V, vertebrates; A, ascidians; D, Drosophila; C, cnidarians; M, molluscs; P, planarians). The arrows on the right-hand side represent a direct influence of a given factor on differentiation set of genes proved by biochemical methods (DNA-binding assay, ChIP, transgenesis, luciferase assays, etc.) The green arrows indicate the ancestral interaction proposed by the ‘bipartite’ model. The red arrow highlights the proposed role of Otx in the regulation of ancestral phototransduction genes. Co-option of a certain transcription factor to a new role is indicated by dashed line. We propose that the transcription factors were independently co-opted for regulation of genes governing eye development in different species and these downstream genes may vary among species. Please note that cross-regulatory interactions of transcription factors are not considered in this scheme for simplicity.

Figure 4.

A hypothetical scenario suggesting the ancient regulatory relationship between Otx and ur-opsin predating the cnidarian–bilaterian split. The ur-opsin has been already regulated by the Otx gene and probably by Pax (not excluding other transcription factors involved). After the duplication and diversification of r- and c-opsin, the regulation by Otx has been preserved in both lineages, whereas Pax-dependent regulation has been lost in c-opsin lineage. Retinal homeobox Rx might have been recruited for regulation of c-opsin. Alternatively, Rx has regulated the ur-opsin and this role has been lost in r-opsin lineage. With increasing complexity of animal body plans, all the transcription factors have consequently acquired additional roles in eye development.