Evolution of the eye

Evolution of the eye

The evolution of the eye has been a subject of significant study, as a distinctive example of a homologous organ present in a wide variety of taxa. The development of the eye is considered by some experts to be monophyletic; that is, all modern eyes, varied as they are, have their origins in a proto-eye believed to have evolved some 540 million years ago. [Halder, G., Callaerts, P. and Gehring, W.J. (1995). "New perspectives on eye evolution." "Curr. Opin. Genet. Dev." 5 (pp. 602–609).] [Halder, G., Callaerts, P. and Gehring, W.J. (1995). "Induction of ectopic eyes by targeted expression of the "eyeless" gene in "Drosophila". "Science" 267 (pp. 1788–1792).] [Tomarev, S.I., Callaerts, P., Kos, L., Zinovieva, R., Halder, G., Gehring, W., and Piatigorsky, J. (1997). "Squid "Pax-6" and eye development." Proc. Natl. Acad. Sci. USA, 94 (pp. 2421–2426).] Much of the evolution is believed to have been concentrated in just a few million years: the first predator to gain true imaging would have initiated an "arms race".Fact|date=July 2007 Prey animals and competing predators alike would be forced to match or exceed any such capabilities to survive. Hence multiple eye types and subtypes developed in parallel.Fact|date=July 2007 However, other experts suggest that the sharing of genes instead only shows convenient pathways, with the eye evolving independently in some cases. [Kozmik, Z., Daube, M., Frei, E. et al. (2003). " [http://dx.doi.org/10.1016/S1534-5807(03)00325-3 Role of Pax Genes in Eye Evolution A Cnidarian PaxB Gene Uniting Pax2 and Pax6 Functions.] " "Developmental Cell." Volume 5, issue 5 (pp. 773–785).] [Land, M.F. and Nilsson, D.-E., "Animal Eyes", Oxford University Press, Oxford (2002).]

Eyes in various animals show adaption to their requirements. For example, birds of prey have much greater visual acuity than humans and some, like diurnal birds of prey, can see ultraviolet light. The different forms of eye in, for example, vertebrates and mollusks are often cited as examples of parallel evolution. As far as the vertebrate/mollusk eye is concerned, intermediate, functioning stages have existed in nature, which is also an illustration of the many varieties and peculiarities of eye construction. In the monophyletic model, these variations are less illustrative of non-vertebrate types such as the arthropod (compound) eye, but as those eyes are simpler to begin with, there are fewer intermediate stages to find.

Primatologist Prof. Lynne Isbell, UC Davis, suggests that the ability to spot dangerous snakes may have played a major role in the evolution of primate close-up vision with its eye for color, detail, movement and depth of field. She points out: "A snake is the only predator you really need to see close up. If it's a long way away it's not dangerous." Our ancestors and snakes with mouths big enough to eat them appeared at about the same time, while other serious predators evolved much later. [cite journal | last = | first = | year = 2006 | month = July | title = Seeing The Serpent: Ability To Spot Venomous Snakes May Have Played Major Role In Primate Evolution | journal = Science Daily | url = http://www.sciencedaily.com/releases/2006/07/060720094341.htm
format = | accessdate = 2008-05-24 | laysummary = | laysource = | laydate = | quote = Some primate groups less threatened by snakes show fewer signs of evolutionary pressure to evolve better vision. For example, the lemurs of Madagascar do not have any venomous snakes in their environment, and in evolutionary terms "have stayed where they are," Isbell said. In South America, monkeys arrived millions of years before venomous snakes, and show less specialization in their visual system compared with Old World monkeys and apes, which all have good vision, including color.

History of research

Since 1802, the evolution of a structure as complex as the projecting eye by natural selection has been said to be difficult to explain. [In 1802, William Paley claimed that the eye was a miracle of design.] Charles Darwin himself wrote, in his "Origin of Species", that the evolution of the eye by natural selection at first glance seemed "absurd in the highest possible degree". However, he went on to explain that despite the difficulty in imagining it, it was perfectly feasible:

...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.Darwin, Charles (1859). "On the Origin of Species". London: John Murray.]

He suggested a gradation from "an optic nerve merely coated with pigment, and without any other mechanism" to "a moderately high stage of perfection", giving examples of wict|extant intermediate grades of evolution.

Darwin's suggestions were soon proven to be correct, and current research is investigating the genetic mechanisms responsible for eye development and evolution.

Rate of evolution

The first fossils of eyes appeared during the lower Cambrian period (about Ma|540). This period saw a burst of apparently rapid evolution, dubbed the "Cambrian explosion". One of the many hypotheses for "causes" of this diversification (backed up by scant evidence) holds that the evolution of eyes initiated an arms race that caused a rapid spate of evolution.Fact|date=March 2008 Earlier than this, organisms may have had use for light sensitivity, but not for fast locomotion and navigation by vision.

Since the fossil record, particularly of the Early Cambrian, is so poor, it is difficult to constrain the rate of eye evolution. Simple modelling, invoking nothing other than small mutations exposed to natural selection, demonstrates that a primitive optical sense organ could evolve into a complex human-like eye within under a million years,cite journal|author=Nilsson, D-E; Pelger S|year=1994|title=A pessimistic estimate of the time required for an eye to evolve|journal=Proc R Soc Lond B|volume= 256|pages=53–58|doi=10.1098/rspb.1994.0048] ref|berlinski|* but this only provides a lower bound for the process.

One origin or many?

It is a matter of debate whether the "eye" evolved once, or independently in many clades. The genetic machinery employed in eye development is common to all eyed organisms. The only unique prerequisite for vision is the use of vitamin-A-related chromophores in the visual pigment, and this is also found in bacteria. Even photoreceptor cells may have evolved more than once from molecularly similar chemoreceptors, and photosensitive cells probably existed long before the Cambrian explosion.cite journal
author = Nilsson, D.E.
year = 1996
title = Eye ancestry: old genes for new eyes
journal = Curr. Biol
volume = 6
pages = 39–42 | url = http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6VRT-4D7CBY3-C&_user=10&_rdoc=1&_fmt=&_orig=search&_sort=d&view=c&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=04ec410ef75358030c44d8e1feb48b88
accessdate = 2008-03-04
doi = 10.1016/S0960-9822(02)00417-7

All light-sensitive organs rely on photoreceptor systems employing a family of proteins called opsins. All seven sub-families of opsin were already present in the last common ancestor of animals. Further, the genetic toolkit for positioning eyes is common to all animals: the PAX6 gene controls where the eye develops in organisms ranging from mice to humans to fruit flies. [Halder, G., Callaerts, P. and Gehring, W.J. (1995). "New perspectives on eye evolution." "Curr. Opin. Genet. Dev." 5 (pp. 602–609).] [Halder, G., Callaerts, P. and Gehring, W.J. (1995). "Induction of ectopic eyes by targeted expression of the "eyeless" gene in "Drosophila". "Science" 267 (pp. 1788–1792).] [Tomarev, S.I., Callaerts, P., Kos, L., Zinovieva, R., Halder, G., Gehring, W., and Piatigorsky, J. (1997). "Squid "PAX-6" and eye development." Proc. Natl. Acad. Sci. USA, 94 (pp. 2421–2426).] However, these master control genes would be much older than many of the structures they control in modern animals, and were probably co-opted for a different purpose.

Sensory organs probably evolved before the brain did – there is no need for an information-processing organ (brain) before there is information to process.

tages of eye evolution

The earliest predecessors of the eye were photoreceptor proteins that sense light, found even in unicellular organisms, called "eyespots". Eyespots can only sense ambient brightness: they can distinguish light from dark, sufficient for photoperiodism and daily synchronization of circadian rhythms. They are insufficient for vision, as they can not distinguish shapes or determine the direction light is coming from. Eyespots are found in nearly all major animal groups, and are common among unicellular organisms, including euglena. The euglena's eyespot, called a "stigma", is located at its anterior end. It is a small splotch of red pigment which shades a collection of light sensitive crystals. Together with the leading flagellum, the eyespot allows the organism to move in response to light, often toward the light to assist in photosynthesis, and to predict day and night, the primary function of circadian rhythms.

Vision itself relies on a basic biochemistry which is common to all eyes. However, how this biochemical toolkit is used to interpret an organism's environment varies widely: eyes have a wide range of structures and forms, all of which have evolved quite late relative to the underlying proteins and molecules.cite journal
author = M F Land; R D Fernald
year = 1992| doi = 10.1146/annurev.ne.15.030192.000245
title = The Evolution of Eyes
journal = Annual Review of Neuroscience
volume = 15
pages = 1-29

At a cellular level, there appear to be two main "designs" of eyes, one possessed by the protostomes (molluscs, annelid worms and arthropods), the other by the deuterostomes (chordates and echinoderms).

The functional unit of the eye is the receptor cell, which contains the opsin proteins and responds to light by initiating a nerve impulse. The light sensitive opsins are borne on a hairy layer, to maximse the surface area. The nature of these "hairs" differs: in the protostomes, they are microvilli – extensions of the cell wall. But in the deuterostomes, they are derived from cilia – separate structures. This now looks like something of a simplification, as some microvilli contain traces of cilia - but other observations appear to support a fundamental difference between protostomes and deuterostomes. These considerations centre on the response of the cells to light - some use sodium to cause the electric signal that will form a nerve impulse, and others use potassium; further, protostomes on the whole constrcut a signal by allowing "more" sodium to pass through their cell walls, whereas deuterostomes allow less through.

This suggests that when the two lineages diverged in the Precambrian, they had only very primitive light receptors, which developed into more complex eyes independently.

Early eyes

The basic light-processing unit of eyes is the photoreceptor cell, a specialized cell consisting of two molecules in a membrane: the opsin, a light-sensitive protein, surrounding the chromophore, a pigment that distinguishes colors. Groups of such cells are termed "eyespots", and have evolved independently somewhere between 40 and 65 times. These eyespots permit animals to gain only a very basic sense of the direction and intensity of light - enough to know when they are safely in a cave, for example, but not enough to discriminate an object from its surroundings.

Developing an optical system that can discriminate the direction of light to within a few degrees is apparently much more difficult, and only six of the thirty-something phylathe precise number varies from author to author] possess such a system. However, these phyla account for 96% of living species.

These complex optical systems started out as the multicellular eyepatch gradually depressed into a cup, which first granted the ability to discriminate brightness in directions, then in finer and finer directions as the pit deepened. While flat eyepatches were ineffective at determining the direction of light, as a beam of light would activate the exact same patch of photo-sensitive cells regardless of its direction, the "cup" shape of the pit eyes allowed limited directional differentiation by changing which cells the lights would hit depending upon the light's angle. Pit eyes, which had arisen by the Cambrian period, were seen in ancient snails,clarifyme|Do you mean gastropods? which ones? and are found in some snails and other invertebrates living today, such as planaria. Planaria can slightly differentiate the direction and intensity of light because of their cup-shaped, heavily-pigmented retina cells, which shield the light-sensitive cells from exposure in all directions except for the single opening for the light. However, this proto-eye is still much more useful for detecting the absence or presence of light than its direction; this gradually changes as the eye's pit deepens and the number of photoreceptive cells grows, allowing for increasingly precise visual information. [http://library.thinkquest.org/28030/eyeevo.htm Eye-Evolution?] ]

When a photon is absorbed by the chromophore, a chemical reaction causes the photon's energy to be transduced into electrical energy and relayed, in higher animals, to the nervous system. These photoreceptor cells form part of the retina, a thin layer of cells that relays visual information,Fernald, Russell D. (2001). [http://www.karger.com/gazette/64/fernald/art_1_3.htm The Evolution of Eyes: How Do Eyes Capture Photons?] "Karger Gazette" 64: "The Eye in Focus".] as well as the light and daylength information needed by the circadian rhythm system, to the brain. However, some jellyfish, such as Cladonema, have elaborate eyes but no brain. Their eyes transmit a message directly to the muscles without the intermediate processing provided by a brain.cite journal | last = Gehring | first = W. J. | date = 13 January 2005
title = New Perspectives on Eye Development and the Evolution of Eyes and Photoreceptors | journal = Journal of Heredity | volume = 96 | issue = 3 | pages = 171–184 | publisher = Oxford Journals
pmid = 15653558| doi = 10.1093/jhered/esi027 | url = http://jhered.oxfordjournals.org/cgi/content/full/96/3/171
format = Full text | accessdate = 2008-04-26

During the Cambrian explosion, the development of the eye accelerated rapidly, with radical improvements in image-processing and detection of light direction. [Conway-Morris, S. (1998). "The Crucible of Creation". Oxford: Oxford University Press.] As certain organisms benefited from the dramatic advantages given by full-fledged eyes, many other organisms were forced to evolve similarly advanced eyes in order to compete.Fact|date=April 2008 As a result, the majority of major developments in eyes are thought to have occurred over the span of only a few million years. In the book "In the Blink of an Eye", Andrew Parker discusses a theory that the evolution of the eye was the catalyst for the Cambrian Explosion. Korthof, Gert (2003) [http://home.planet.nl/~gkorthof/korthof60.htm "In the Blink of an Eye" review] ]

The "pinhole camera" eye was developed as the pit deepened into a cup, then a chamber. By reducing the size of the opening, the organism achieved true imaging, allowing for fine directional sensing and even some shape-sensing. Eyes of this nature are currently found in the nautilus. Lacking a cornea or lens, they provide poor resolution and dim imaging, but are still, for the purpose of vision, a major improvement over the early eyepatches.Dawkins, Richard (1986). "The Blind Watchmaker".]

Overgrowths of transparent cells prevented contamination and parasitic infestation. The chamber contents, now segregated, could slowly specialize into a transparent humour, for optimizations such as colour filtering, higher refractive index, blocking of ultraviolet radiation, or the ability to operate in and out of water. The layer may, in certain classes, be related to the moulting of the organism's shell or skin.

It is likely that a key reason eyes specialize in detecting a specific, narrow range of wavelengths on the electromagnetic spectrum—the visible spectrum—is because the earliest species to develop photosensitivity were aquatic, and only two specific ranges of electromagnetic radiation can travel through water, the most significant of whichClarifyme|date=April 2008 is visible light. This same light-filtering property of water also influenced the photosensitivity of plants. [Fernald, Russell D. (2001). [http://www.karger.com/gazette/64/fernald/art_1_1.htm The Evolution of Eyes: Why Do We See What We See?] "Karger Gazette" 64: "The Eye in Focus".] [Fernald, Russell D. (1998). "Aquatic Adaptations in Fish Eyes". New York, Springer.] [Fernald, Russell D. (1997). [http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=9310200&dopt=Abstract" The evolution of eyes."] "Brain Behav Evol." 50 (pp. 253–259).]

Lens formation and diversification

The transparent cells over the pinhole eye's aperture split into two layers, with liquid in between. The liquid originally served as a circulatory fluid for oxygen, nutrients, wastes, and immune functions, allowing greater total thickness and higher mechanical protection. In addition, multiple interfaces between solids and liquids increase optical power, allowing wider viewing angles and greater imaging resolution. Again, the division of layers may have originated with the shedding of skin; intracellular fluid may infill naturally depending on layer depth.

Note that this optical layout has not been found, nor is it expected to be found. Fossilization rarely preserves soft tissues, and even if it did, the new humour would almost certainly close as the remains desiccated, or as sediment overburden forced the layers together, making the fossilized eye resemble the previous layout.

Vertebrate lenses are composed of adapted epithelial cells which have high concentrations of the protein crystallin. The refractive index gradient which makes the lens useful is caused by the radial shift in crystallin concentration in different parts of the lens, rather than by the specific type of protein: it is not the presence of crystallin, but the relative distribution of it, that renders the lens useful. [Fernald, Russell D. (2001). [http://www.karger.com/gazette/64/fernald/art_1_4.htm The Evolution of Eyes: Where Do Lenses Come From?] "Karger Gazette" 64: "The Eye in Focus".]

It is biologically difficult to maintain a transparent layer of cells. Deposition of transparent, nonliving, material eased the need for nutrient supply and waste removal. In trilobites, the material was calcite; in humans, the material is crystallin. A gap between tissue layers naturally forms a biconvex shape, which is optically and mechanically ideal for substances of normal refractive index. A biconvex lens confers not only optical resolution, but aperture and low-light ability, as resolution is now decoupled from hole size—which slowly increases again, free from the circulatory constraints.

Independently, a transparent layer and a nontransparent layer may split forward from the lens: a separate cornea and iris. (These may happen before or after crystal deposition, or not at all.) Separation of the forward layer again forms a humour, the aqueous humour. This increases refractive power and again eases circulatory problems. Formation of a nontransparent ring allows more blood vessels, more circulation, and larger eye sizes. This flap around the perimeter of the lens also masks optical imperfections, which are more common at lens edges. The need to mask lens imperfections gradually increases with lens curvature and power, overall lens and eye size, and the resolution and aperture needs of the organism, driven by hunting or survival requirements. This type is now functionally identical to the eye of most vertebrates, including humans.

Other developments

Annotated image | float=right | caption=Vertebrates and octopuses developed the camera eye independently. The vertebrate version is less efficient because the nerve fibers pass "in front" of the retina, and there is a blind spot where the nerves pass through the retina.|

annotations =
;"Backward" Illumination of RetinaThe retina may revert on itself, forming a double layer. The nerves and blood vessels can migrate to the middle, where they do not block light, or form a blind spot on the retina. This type is seen in squids, which live in the dim oceans. In cats, which hunt at night, the retina does not revert. Instead a second, reflective layer (the tapetum) forms behind the retina. Light which is not absorbed by the retina on the first pass may bounce back and be detected. As a predator, the cat simply accommodates blind spots with head and eye motion.

;Color visionThe ability to see colors presents distinct selective advantages for species, such as being better able to recognize predators, food and mates. As opsin molecules were subtly fine-tuned to detect different wavelengths of light, at some point, color vision developed when photoreceptor cells developed multiple pigments. As a chemical instead of mechanical adaptation, this may have occurred at any of the early stages of the eye's evolution, and the capability may have disappeared and reappeared, as organisms became predator or prey. Similarly, night and day vision emerged when receptors differentiated into rods and cones, respectively.

;Focusing mechanismSome species move the lens back and forth, some stretch the lens flatter. Another mechanism regulates focusing chemically and independently of these two, by controlling growth of the eye and maintaining focal length. Note that a focusing method is not a requirement. As photographers know, focal errors increase as aperture increases. Thus, countless organisms with small eyes are active in direct sunlight and survive with no focus mechanism at all. As a species grows larger, or transitions to dimmer environments, a means of focusing need only appear gradually.

Evolutionary baggage

The eyes of many taxa record their evolutionary history in their "imperfect" design. The mammalian eye, for instance, is built "backwards and upside down", requiring "photons of light to travel through the cornea, lens, aquaeous fluid, blood vessels, ganglion cells, amacrine cells, horizontal cells, and bipolar cells before they reach the light-sensitive rods and cones that transduce the light signal into neural impulses- which are then sent to the visual cortex at the back of the brain for processing into meaningful patterns." [Dr. Michael Shermer, as quoted by Christopher Hitchens in his book "God is Not Great" (pg.82)]

In creationism and intelligent design

The eye is often used by creationists as an example of an organ which is irreducibly complex and so must have been created by a divine creator. [cite book|title=Darwin's Black Box|author=Michael Behe] Sarfati, Jonathan (2000). [http://www.answersingenesis.org/home/area/re2/chapter10.asp Argument: 'Irreducible complexity'] , from "Refuting Evolution" (Answers in Genesis).]

The concept of irreducible complexity has been criticised by some as being an argument from ignorance. [Index to Creationist Claims. Mark Isaak. The Talk.Origins Archive. "Irreducible complexity and complex specified information are special cases of the "complexity indicates design" claim; they are also arguments from incredulity." [http://www.talkorigins.org/indexcc/CI/CI101.html] ] If a particular author cannot imagine a way in which the eye evolved, this does not have any bearing upon whether or not the eye actually did evolve.

The available scientific evidence, summarised in this article, in the form of fossil and genetic evidence, demonstrates overwhelmingly that the complex eyes seen in some modern-day species evolved from much simpler forms over millions of years. In addition, many species alive today can be found which have significantly simpler eyes, disproving the notion of irreducible complexity as it applies to the eye.

External links

* [http://www.youtube.com/watch?v=Stb9pQc9Kq0 The Evolution of the Eye] Video about the model proposed by Zoologist Dan-Eric Nilsson
* [http://www.youtube.com/watch?v=fOtP7HEuDYA&eurl=http://www.expelledexposed.com/ Creationism Disproved?] Video from the National Center for Science Education on the evolution of the eye

*cite web | url = http://scienceblogs.com/pharyngula/2007/12/evolution_of_vertebrate_eyes.php | title = Evolution of vertebrate eyes | accessdate = 2007-12-23 | last = Myers | first = PZ |date=2007-12-21 | work = Pharyngula | publisher = ScienceBlogs | quote = a review of Lamb TD, Collin SP, Pugh EN Jr. (2007) Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8(12):960-76.


David Berlinski, an intelligent design proponent, questioned the basis of the calculations,cite journal|title=Commentary magazine|author=Berlinski, David|authorlink=David Berlinski|month=April | year=2001] and the author of the original paper wict|refuted Berlinski's criticism.cite journal|author=Nilsson, Dan-E.|title=Beware of Pseudo-science: a response to David Berlinski's attack on my calculation of how long it takes for an eye to evolve|url=http://www.talkreason.org/articles/blurred.cfm#lund] [http://www.pbs.org/wgbh/evolution/library/01/1/l_011_01.html "Evolution of the Eye" on PBS] ]


* Lamb, T. D., Collin, S. P., & Pugh, E. N., "Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup", "Nature Reviews: Neuroscience", v. 8 no. 12 (December 2007) pp. 960-976 doi:10.1038/nrn2283, [http://www.nature.com/nrn/journal/v8/n12/fig_tab/nrn2283_F4.html illustration]

* Land, M. F., & Nilsson, D-E, "Animal Eyes", Oxford: Oxford University Press, 2002 ISBN 0-19-8509685 "The origin of vision", Chapter 1, pages 1-15

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