Charles Darwin famously highlighted the eye, "with all its inimitable contrivances", as one of the hurdles in the acceptance of his theory of natural selection. "[It} seems, I freely confess, absurd in the highest possible degree", that this complex organ arose as the result of natural selection. This confession has in the past been seized upon by the bright lights of the intelligent design movement and their ilk as proof that Darwin himself had doubts about his own theories.
Creationists have gone a bit quiet on this front in recent years as more is known about the evolution of the eye, and they might just be done away with completely if a hypothesis set out in a Nature Reviews Neuroscience paper last December proves to be correct.
"If," Darwin wrote in On the Origin of Species, "numerous gradations from a perfect and complex eye to one very imperfect and simple, each grade being useful to its possessor, can be shown to exist ... and if any variation or modification in the organ be ever useful to the animal under changing conditions of life, then the difficulty of believing that a perfect and complex eye could be formed by natural selection, though insuperable by our imagination, can hardly be considered real."
In the Nature Reviews paper, the team of Professors Trevor Lamb of the John Curtin School of Medical Research at the Australian National University, Shaun Collin of the School of Biomedical Sciences at the University of Queensland and Ed Pugh of the FM Kirby Centre for Molecular Ophthalmology at the University of Pennsylvania have taken up Darwin's challenge and set out a proposed sequence of the evolution of the vertebrate eye which they believe might satisfy Darwin's prescription. And they have even set homework to test the hypothesis.
The team sets out their view of the sequence of events in the evolution of opsins, photoreceptors, the retina and the eye cup in vertebrates. They begin with the separation of primitive bilateral animals into the super-phyla of the protostomes and the deuterostomes approximately 580 million years ago. There have been multiple splits since then, the emergence of the chordates about 550 million years ago being an important one for our purposes.
These little animals, Trevor Lamb says, had developed a notochord and a dorsal nerve chord. They also had developed photosensitive regions at the rostral end. "These were just little spots with a few photoreceptors," Lamb says, "but their primitive receptors were remarkably similar to the cones that we have."
These photoreceptors were ciliary, as opposed to the rhabdomeric photoreceptors primarily found in the protostomes, the invertebrates. And the organs were not eyes as such, having no image forming ability, but presumably were used to distinguish light from dark, to regulate diurnal rhythms and for shadow detection.
"But in order to go to deeper waters, to work in lower light levels, one of these ancestors probably started expanding the photoreceptor region - it just grew and grew, there were more photoreceptors and they could absorb more light so they could work at lower light intensities," Lamb says. "That probably involved a spreading out of this retinal layer sideways."
At the same time, the skull was beginning to develop - the evolution of the craniates. "If you have your photosensitive region on the midline, covered by a skull, that's not going to be much good," he says. "It's going to be advantageous if you expand outwards to the side.
"Then there was probably a contact between this expanding light-sensitive region and the ectoderm [surface]. And what seems likely to have happened is that the proto-eye region induced changes in the surface and kept that surface clear - it stopped the pigmentation there. And subsequently that surface region probably bulged inwards and pushed in as an expansion that ultimately became the lens. Once you've got a thickening of the skin that has any kind of lens-like properties, you start getting some imaging. If you've got a light-sensitive region there, and something that's acting a bit like a lens in front of it, then you've got the rudiments of an imaging eye."
Even with something as rudimentary as this, you are likely to get an advantage. As Shaun Collin puts it, all of a sudden these animals were able to see what was going to eat them. "So they now needed to evolve something to stop being eaten, so you can either camouflage yourself or swim faster, hide or all of the above," he says. "That started what might have been predation and meant that a lot of animals could go in a lot of different directions - all these new groups popped up. Some of them have disappeared since but in this period all these new phyla of invertebrates and of chordates started and we think that the evolution of image-forming eyes was the catalyst to push this forward very quickly."
A perfectly straight-forward hypothesis, but where is the evidence that would have satisfied Mr Darwin? For this team, it lies not just in the fossil record but in the morphological data that can be evaluated in extant species. One of those necessary gradations is found in the hagfish, a rather unattractive species of jawless fish that lurks in deep water and exudes a gooey mess of slime when disturbed. They propose that the hagfish 'eye' is that missing step from primitive photosensitive regions to the development of the modern eye.
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