Darwin and the Evolution of The

Darwin and the evolution of the eye To celebrate the sesquicentennial of The Origin of Species, Nick Lane takes a look at what Charles Story Darwin did for the eye, and what he would love to know about eyes if he were still alive today Nick Lane Cover WHAT use is half an eye? No sentence is lens, cornea and all the other accoutrements Others are less more closely linked with Darwin’s doubters of eyes just get in the way of photons, they’re convinced, and point than that; and none is more likely to be simply stripped away. to the difficulties trotted out by the genuinely perplexed, involved in growing a those who accept that the eye evolved but Mechanical contrivances functional lens from can’t imagine how. And Richard Dawkins’s A naked retina is a sexier name for a light- scratch. The trilobites truculent riposte – “half an eye is precisely sensitive spot, which was Darwin’s own are a case in point: one per cent better than 49 per cent of an starting point for evolving the eye. He is often their lenses were eye” – doesn’t help those who can’t picture quoted deliberately out of context, even by formed not from half an eye. scientists seeking to solve Darwin’s ‘mystery’, crystallin proteins Ophthalmologists, of course, know all as saying, “to suppose that the eye evolved but from crystals of about half an eye – either the back half or by natural selection seems, I freely confess, calcite, clear rhombs the front. It has always amazed me how little absurd in the highest possible degree.” with specific optical cataract and refractive surgeons really need With the benefit of hindsight, that was an properties. The to talk to retinal specialists or vice versa, unfortunate rhetorical flourish. In the very fact that trilobites even if EuroTimes now caters for both. And next sentence he went on to say, “Though fell extinct in the anyone reading this who prefers to keep the insuperable to our imagination, the difficulty Permian extinction, old boundaries alive can take some comfort can hardly be considered real.” 250 million years in evolution, which backs the old split. Darwin argued that the eye could evolve, ago, makes it hard to Rimicaris exoculata (copyright P. Briand–Ifremer, France) There’s no better illustration of how so long as the three conditions of natural know how they grew useful half an eye can be than the ‘eyeless’ rift such crystals. selection are met. First, eyesight should vary ‘gene sharing’ and have no inherent optical shrimp Rimicaris exoculata. Swarming in hordes Until the discovery of crystal lenses between individuals. Second, these variations properties. in the black depths of the ocean abyss, on in brittlestars, that is. In 2001, Joanna should be heritable. And third, they should “The diverse lens crystallins comprise a ledges beneath the black smoker vents, the Aizenberg and her colleagues, then at make some difference to survival. Even variety of unrelated multifunctional proteins supposedly blind shrimp have a pair of naked Bell Labs, showed that the spiny calcite in Darwin’s day, it was plain that all three serving refractive functions in the lens and retinas on their backs (See image above). skeleton of brittlestar Ophicoma wendtii conditions are met in full. But that didn’t nonoptical functions, often enzymatic or Discovered by Cindy Van Dover, who now forms an array of calcite knobs on its arms make the actual succession of steps any more stress protective functions, in other tissues,” heads the Duke Marine Laboratory, these resembling trilobite lenses. Each knob has superable to the imagination. he says. naked retinas are packed with invertebrate light-sensitive neurons underlying it; and Then about a decade ago Suzanne Pelger The α-crystallins, for example, are rhodopsins (very similar to melanopsin, this optical system helps the brittlestar and Dan-Eric Nilsson, at Lund University, stress-inducible small heat-shock proteins, responsible for regulating circadian rhythms scuttle away at the first sign of danger. Sweden, modelled a realistic sequence of discovered in Drosophila and since found in in human retinal ganglion cells). It soon Similar calcite lenses can be seeded in steps beginning with a light-sensitive spot and many human tissues. transpired that other vent species, from vitro by crystallisation of a calcium carbonate ending with a simple camera eye, complete The vertebrate crystallins are united not shrimp to crabs, also sport naked retinas. solution onto proteins with acidic side-chains, with a lens. Each step was a conservative by common properties or descent, but Many suspected that the naked retinas are even those found in mollusc shells, which estimate – a recess in the sheet, a slight by equivalent changes in their regulatory some form of degenerate organ, not actually certainly play no role in sight. Each crystal deepening into a pit, the first swelling of a sequences, specifically the cis-control elements used for sight, until a succession of larvae is a perfect rhomb, with its optical ‘c-axis’ lens and so on. of their promoter and enhancer regions. were discovered, all of which turned out pointing directly up. No magic involved: The surprise was that fewer than 400,000 “A change in the molecular function of a to have quite normal eyes. These disappear just the spontaneous reaction of any acidic tiny steps are needed to get from a light- protein by a change in the regulation of its during development, to be replaced by naked protein in a saturated mineral solution, sensitive spot to a fully functional eye, gene means that gene duplication is not a retinas sensitive to green light at around pressed into service by natural selection. albeit one lacking in optional extras like prerequisite for functional innovation as was 500 nm. This theme of opportunism is rife with accommodation. thought for many years,” Piatigorsky notes. That was another mystery, as the hot vents lenses. Numerous other animals have evolved If each step (limited to a one per cent A fine example of how the crystallins glow faintly red, but not detectably green. crystal lenses, typically composed of organic change in an existing structure) were to were first recruited is found in the brain of NASA intervened with a probe called ALISS crystals like isoxanthopterin, cysteine or take place in a single generation, and each the larval sea squirt Ciona intestinalis. Literally (Ambient Light Imaging and Spectral System), guanine (the latter more usually known as a generation lived for a year, then an eye could a pillar of intestines, the adult sea squirt is which did detect a small spectral peak of base in DNA). Indeed guanine crystals are evolve in less than half a million years. famous for anchoring itself to a rock and then green light in the vent wonderland. It might found in fish scales, giving them their silvery And that helps to make sense of the reabsorbing its own brain. But the larvae are be generated by bubbles or crystals crushed lustre and are added to cosmetics for the abrupt appearance of animals in the fossil tadpole-like creatures, betraying the squirt as instantaneously by the huge pressure in the same reason (they also lend their name to record, around 550 million years ago – the an early chordate that branched away from abyss, they say. guano, the dried excrement of birds and so-called Cambrian explosion, whose speed the vertebrates before the origin of the lens. Whatever its cause, the faint green glow bats). Again, a naturally forming crystal was had troubled Darwin himself. After aeons of In the last few years, Sebastian Shimeld is enough to power photosynthesis in some simply pressed into service. emptiness, large animals like trilobites burst and his colleagues at Oxford have shown bacteria; and although we can’t see it with the Even bits of the cell have been enlisted into the fossil record in a couple of million that despite lacking a lens, C. intestinalis larvae naked eye, the distinguished neurobiologist in this way. My own favourite example is years, and the very first trilobites already have bona fide βγ-crystallins tucked away Mike Land, at the University of Sussex, has the tiny parasitic flatworm Entobdella soleae, had eyes, as did other animals in the early in their brains (specifically the palps and calculated that the naked retinas of ‘blind’ which has a lens formed from mitochondria Cambrian period. otolith, pigmented cells in the light-sensing shrimp are some seven million times more fused together. Other flatworms don’t Oxford biologist Andrew Parker has ocellus). What’s more, the crystallin gene sensitive to photons than the shrimp’s own even bother to fuse their mitochondria – a argued that the fossil record did not lie – is under regulatory control of the same larval eyes. cluster of quite ordinary cellular components eyes really did evolve that fast. The sudden genes responsible for lens development in Presumably, detecting the faint glow of apparently bends light well enough to serve appearance of eyes, he says, transformed vertebrates, including Pax-6. the vents falling on their backs makes the some advantage. relationships between predator and prey. As Shimeld put it, “The evolutionary difference between life and death, whether But the best example of opportunism is The ensuing arms race gave rise to the hard origin of the lens was based on co-option of by drifting away from the vents, or baking in surely the crystallins of the vertebrate lens. shells wielded by the strange Cambrian pre-existing regulatory circuits controlling them. Half an eye is better than a whole eye Over several decades Joram Piatigorsky, at creatures, and that in turn made them more the expression of a key structural gene in a when sensitivity matters more than resolution the National Eye Institute, has shown that likely to fossilise.

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