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

Abstract

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.