Eyes and their evolution
The eye is probably the classic example of a highly specialised organ, with many early biologists concluding that it must have been designed for its purpose. For example, in the 17th century the biologist John Ray (noted for formulating the biological definition of a species) wrote:
Seeing then the Eye is composed of so great Variety of Parts, all conspiring to the Use of Vision, whereof some are absolutely necessary others very useful and convenient, none idle or superfluous; and which is remarkable, many of them of a different Figure and Consistency from any others in the Body besides, as being transparent, which it was absolutely necessary they should be, to transmit the Rays of Light: Who can but believe that this Organ was designed and made Purposely for the Use for which it serves? 
And Paley argued that just as it is obvious that a watch must have been designed and purposefully constructed:
WERE there no example in the world, of contrivance, except that of the eye, it would be alone sufficient to support the conclusion which we draw from it, as to the necessity of an intelligent Creator. 
Darwin and natural selection
However, of course, Ray and Paley preceded Darwin who introduced the concept of natural selection which presented the possibility that even complex organs could have evolved gradually through a series of intermediates where each was a small improvement over its predecessor. In other words, it was no longer necessary to conclude that specialised organs such as eyes had been designed, they merely had the appearance of design due to the guiding hand of natural selection. In his autobiography, Darwin wrote:
The old argument of design..., as given by Paley, which formerly seemed to me so conclusive, fails, now that the law of Natural Selection has been discovered. There seems to be no more design in the variability of organic beings and in the action of natural selection, than in the course which the wind blows. Everything in nature is the result of fixed laws.
In the Origin, Darwin recognised that ‘organs of extreme perfection and complication’, such as eyes, are an obvious challenge to his theory. Nevertheless, he argued that even these could have arisen via a series of advantageous variations:
Yet reason tells me, that if 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; if further, the eye does vary ever so slightly, and the variations be inherited, which is certainly the case; and if any variation or modification in the organ be ever useful to an 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. 
That is, Darwin knew that individuals within a species vary, and (in general) variations are heritable and can be accumulated (evident from the success of breeding). And, although he knew that there is a limit to how much morphological change can be effected by breeding, he believed that given enough time, nature could transcend those limits; i.e. that, given time, new variations would arise and could be inherited. He did not know the cause of variations, believing that they probably arose in some way in response to an organism’s way of life. So it was quite conceivable to him that substantial structures such as eyes and wings could have evolved progressively via a series of intermediate forms, each offering at least some advantage over its predecessor. And, given the biological knowledge of his time, there was no compelling reason to refute his extrapolation.
Genes and molecular biology
However, since the middle of the 20th century it has become abundantly clear that morphology is absolutely dependent on genes. Biological tissues are not indeterminately plastic – able to vary freely (as Darwin had thought) – but morphological variations are limited by the available genetic variability. And novel variations do not arise in response to an organism’s way of life, but only if appropriate new genes arise – which, it is generally accepted, only occurs in an undirected manner, such as by random mutations.
However, there are strong biochemical reasons against new genes arising. And, particularly relevant for genes required for significant new structures (such as eyes), the more we discover about the highly complex genetic and molecular mechanisms involved in embryonic development (e.g. see embryonic development of human eye), the more it is evident that new structures would require many new genes (for new proteins, and with appropriate regulatory sequences), with complementary functions, to arise more or less simultaneously – which is prohibitively improbable. In the light of what we now know about the nature and functioning of genes, and of embryonic mechanisms, it is no longer tenable to propose evolutionary development solely in terms of morphology (as Darwin did) – to be credible they must also take on board the genetic implications.
Unfortunately, these biochemical realities are generally overlooked by biologists proposing evolutionary scenarios for the development of novel structures, such as eyes. Their scenarios are no better than that proposed by Darwin. A notable example is that proposed by Nilsson & Pelger (see Fig. 2) which is the sort of scenario that Darwin envisaged. All that we have learned about genetics and molecular biology in the last 100 years is completely ignored! Despite what we now know to the contrary, the authors tacitly assume that new genes (to build substantial new structures) will arise as readily as new variations (of existing structures) arise through the mixing and segregation of existing genes in new ways. Indeed, there seems to be a marked lack of clear thinking among evolutionary biologists about when and what new genes would be required, and the substantial reasons against them arising.
Notes display in the main text when the cursor is on the Note number.
1. John Ray, The Wisdom of God Manifested in the Works of the Creation 7th edition, 1717, p260 (http://www.jri.org.uk/ray/wisdom/wisdom_of_god.pdf, p104).
2. William Paley, Natural theology; or evidences of the existence and attributes of the Deity. Collected from the appearances of nature. 12th edition, p75 (http://darwin-online.org.uk).
3. Image credit: Wellcome Library, London, Descarte: Optics – discourse on methods ... The Eye, 1637. Copyrighted work available under Creative Commons Attribution only licence CC BY 4.0 http://creativecommons.org/licenses/by/4.0/
4. Charles Darwin, The autobiography of Charles Darwin 1809-1882 with original omissions restored, edited and with appendix and notes by his grand-daughter Nora Barlow. 1958, p87.
5. Charles Darwin, On the Origin of Species, 1959, edited with an introduction by J. W. Burrow, Penguin Books, 1968, p217.
6. Dan-E. Nilsson and Susanne Pelger, A pessimistic estimate of the time required for an eye to evolve, Proceedings: Biological Sciences, Vol. 256, No. 1345 (Apr. 22. 1994), 53-58.
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