Evolution of the eye
The evolution of the eye is the history of how organs that detect the direction of light, and in some animals form an image, arose from light-sensitive cells. Eyes of several quite different designs exist, and they have appeared independently many times. In 1977 Luitfried Salvini-Plawen and Ernst Mayr counted at least 40 independent origins of photoreceptor organs, and perhaps as many as 65.[1] Robert Fernald wrote in 2006 that only a handful of eye types exist, because the physics of light limits how it can be detected, and that the genes involved, opsin for the light-absorbing protein and some developmental genes, were old and were recruited again and again, while the proteins of the lens were drawn separately from other jobs.[2]
The eye was Charles Darwin's best-known difficulty with his own theory. It has since become the standard example of how a complex organ can arise by small steps, and it is the organ whose first appearance in the fossil record is claimed as the trigger of the Cambrian explosion in the Light switch hypothesis.
Darwin's problem
In On the Origin of Species (1859) Darwin gave the eye a section of its own, headed "Organs of extreme perfection and complication". It begins: "To suppose that the eye, with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest possible degree." The next sentence turns: reason tells him that if gradations from a perfect eye to a very imperfect and simple one can be shown to exist, each useful to its possessor, and if the eye varies and the variations are inherited, then the difficulty "though insuperable by our imagination, can hardly be considered real."[3]
He looked for the gradations among living animals, since the ancestors had left none. In the Articulata, the group of jointed animals that includes crustaceans, he could begin with "an optic nerve merely coated with pigment" and follow two lines of increasing complexity through crustaceans with lens-shaped swellings in each facet of the cornea. Among the vertebrates, he wrote, there is little gradation, and the earlier stages must lie "far beneath the lowest known fossiliferous stratum". His reason, he concluded, ought to conquer his imagination. He also proposed a thought experiment: take a thick layer of transparent tissue with a nerve sensitive to light beneath it, and suppose every part of the layer to be changing slowly in density, so that it separates into layers of different densities and thicknesses.[3]
Nilsson and Pelger
In 1994 two Swedish zoologists, Dan-Eric Nilsson and Susanne Pelger, turned the thought experiment into arithmetic. They began with a flat patch of light-sensitive cells between a transparent layer above and a layer of dark pigment below, and asked how many small changes of shape it would take to reach a focusing lens eye if each change had to improve the spatial information the eye could detect. The patch curves into a cup and the cup deepens. A pinhole forms, the cup fills with transparent material, and a region of the material develops a graded refractive index and becomes a lens.[4]
They made every assumption pessimistic, with small variation, weak selection and low heritability. By their count the transformation takes 1,829 steps of one percent each, which at one generation a year is 364,000 generations. The paper's abstract calls the time "amazingly short: only a few hundred thousand years." The model does not say that eyes evolved this way, only that nothing in the sequence is a barrier. For scale, the Cambrian began about 539 million years ago.[4]
Function first
In 2013 Nilsson argued that eyes evolve as the behavior that needs them becomes more demanding. He proposed four stages, each with its own physical requirements: nondirectional photoreception, which senses the level of light; directional photoreception, in which a shaded photoreceptor tells which way the light comes from; low-resolution vision, enough to notice a looming shadow; and high-resolution vision. The sequence, he suggested, ran from the first opsin to high-resolution vision in about 170 million years and was largely complete by the onset of the Cambrian, about 530 million years ago. Vertebrate rods and cones are ciliary photoreceptors, while the eyes of insects and cephalopods use rhabdomeric ones. Nilsson's analysis suggests that the last common ancestor of the bilaterian animals had a simple set of both kinds, used for directional photoreception, and that directional photoreception had by then evolved independently at least twice.[5]
Borrowed proteins
The lens was built out of proteins that had other jobs. In 1987 Graeme Wistow and colleagues showed that ε-crystallin, a major protein of bird and crocodile lenses, is lactate dehydrogenase, the glycolytic enzyme, present in the duck lens in amounts far beyond any need for catalysis. The duck's was indistinguishable from its own LDH-B4. The enzyme had been recruited "without gene duplication and sequence divergence" to work as a structural protein.[6] Joram Piatigorsky and Wistow called the strategy gene sharing.[7]
Designs
Living animals show most of the stages that Darwin asked for.
| Design | Example | How it forms an image or gathers light |
|---|---|---|
| Eyespot | Green alga Chlamydomonas | Pigment granules with photoreceptor proteins in the membrane; the photoreceptor is itself a light-gated ion channel (channelrhodopsin)[8] |
| Camera eye with a lens | Vertebrates, cephalopods, box jellyfish | A lens focuses light on a retina; in the box jellyfish Tripedalia the lens has a refractive index gradient and nearly no aberration, but the retina sits where the image is not sharp[9] |
| Concave-mirror eye | Scallop, which has up to 200 eyes | A mirror of square guanine crystals focuses light on a double-layered retina[10] |
| Compound eye | Arthropods | Many lenses, each serving one unit of the retina[11] |
| Compound eye with calcite lenses | Trilobites | Each lens is a crystal of calcite[12] |
The vertebrate eye and the eye of an octopus are both camera eyes, and they were built separately. The vertebrate retina is wired so that light passes through the nerve fibers before it reaches the photoreceptors, with a blind spot where the fibers leave; the cephalopod retina is not wired that way.
Genes
In 1995 Georg Halder, Patrick Callaerts and Walter Gehring expressed the eyeless gene of the fruit fly Drosophila in tissues that normally make a wing, a leg or an antenna. Ectopic eyes grew there, with fully differentiated ommatidia and a complete set of photoreceptor cells. Eyeless is homologous to the mouse gene Small eye (Pax6) and the human gene Aniridia; mutations of either lead to a loss or reduction of the eyes. The authors proposed that eyeless is a master control gene for eye development, and that it may serve as one throughout the animal kingdom.[13] The eyes of fly and mouse are not inherited from a common ancestral eye, since a fly's eye is compound and a mouse's has a lens, yet the same regulatory gene starts both. Shubin, Tabin and Carroll called this kind of sharing deep homology.[14]
Fossil record
The oldest eyes known in detail are Cambrian. Trilobites had eyes whose lenses were crystals of calcite. In 1975 Euan Clarkson and Riccardo Levi-Setti showed that in one group the thick lenses were double structures that eliminate spherical aberration, and that the shape of the corrected surface agrees with the constructions of René Descartes and Christiaan Huygens in the seventeenth century.[12]
The eyes of soft-bodied animals fossilize only in exceptional deposits. From the Emu Bay Shale of South Australia, about 515 million years old, Michael Lee and colleagues described in 2011 compound eyes of arthropods, each with more than 3,000 large lenses and a specialized bright zone, the pattern of an active predator that could see in dim light. Eyes of similar complexity that were not mineralized are not known again until about 85 million years later.[11] From the same deposit come the eyes of the large predator Anomalocaris, each with at least 16,000 lenses, described in the article on the Cambrian explosion.[15]
Company materials
Molecular Reality Corporation uses a vertebrate camera eye as its emblem, drawn with a blue iris and a protein emerging from the pupil; the emblem is described in The Seeing Eye.[16] Its mascot Keltar, a puppet, has a single large eye, and the gallery of animations called Iridian contains 197 eyes.
See also
References
- ^ Salvini-Plawen, L. von; Mayr, E. (1977). "On the evolution of photoreceptors and eyes". In Salvini-Plawen, L. von (ed.). Evolutionary Biology. Vol. 10. New York: Plenum. pp. 207-263. doi:10.1007/978-1-4615-6953-4_4.
- ^ Fernald, Russell D. (2006). "Casting a genetic light on the evolution of eyes". Science 313 (5795): 1914-1918. doi:10.1126/science.1127889.
- ^ a b Darwin, Charles (1859). On the Origin of Species by Means of Natural Selection. London: John Murray. pp. 186-188.
- ^ a b Nilsson, Dan-Eric; Pelger, Susanne (1994). "A pessimistic estimate of the time required for an eye to evolve". Proceedings of the Royal Society B 256 (1345): 53-58. doi:10.1098/rspb.1994.0048.
- ^ Nilsson, Dan-Eric (2013). "Eye evolution and its functional basis". Visual Neuroscience 30 (1-2): 5-20. doi:10.1017/S0952523813000035.
- ^ Wistow, G. J.; Mulders, J. W. M.; de Jong, W. W. (1987). "The enzyme lactate dehydrogenase as a structural protein in avian and crocodilian lenses". Nature 326 (6113): 622-624. doi:10.1038/326622a0.
- ^ Piatigorsky, Joram; Wistow, Graeme (1989). "Enzyme/crystallins: gene sharing as an evolutionary strategy". Cell 57 (2): 197-199. doi:10.1016/0092-8674(89)90956-2.
- ^ Nagel, Georg; Szellas, Tanjef; Huhn, Wolfram; et al. (2003). "Channelrhodopsin-2, a directly light-gated cation-selective membrane channel". Proceedings of the National Academy of Sciences 100 (24): 13940-13945. doi:10.1073/pnas.1936192100.
- ^ Nilsson, Dan-Eric; Gislén, Lars; Coates, Melissa M.; Skogh, Charlotta; Garm, Anders (2005). "Advanced optics in a jellyfish eye". Nature 435 (7039): 201-205. doi:10.1038/nature03484.
- ^ Palmer, Benjamin A.; Taylor, Gavin J.; Brumfeld, Vlad; et al. (2017). "The image-forming mirror in the eye of the scallop". Science 358 (6367): 1172-1175. doi:10.1126/science.aam9506.
- ^ a b Lee, Michael S. Y.; Jago, James B.; García-Bellido, Diego C.; Edgecombe, Gregory D.; Gehling, James G.; Paterson, John R. (2011). "Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia". Nature 474 (7353): 631-634. doi:10.1038/nature10097.
- ^ a b Clarkson, E. N. K.; Levi-Setti, R. (1975). "Trilobite eyes and the optics of Des Cartes and Huygens". Nature 254 (5502): 663-667. doi:10.1038/254663a0.
- ^ Halder, Georg; Callaerts, Patrick; Gehring, Walter J. (1995). "Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila". Science 267 (5205): 1788-1792. doi:10.1126/science.7892602.
- ^ Shubin, Neil; Tabin, Clifford; Carroll, Sean (2009). "Deep homology and the origins of evolutionary novelty". Nature 457 (7231): 818-823. doi:10.1038/nature07891.
- ^ Paterson, John R.; García-Bellido, Diego C.; Lee, Michael S. Y.; Brock, Glenn A.; Jago, James B.; Edgecombe, Gregory D. (2011). "Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes". Nature 480 (7376): 237-240. doi:10.1038/nature10689.
- ^ "Molecular Reality Corporation". Molecular Reality Corporation. August 19, 2026.