“To suppose that the eye […] could have been formed by natural selection seems, I freely confess, absurd in the highest degree.”- Charles Darwin: The Origin of Species (1859)
Eye evolution is a topic of great study and sometimes controversy. The eye is a homologous organ, which is present in a wide variety of taxa. A homologous organ is adapted to different purposes, depending on the animal. Even though there may be changes in eyes from phylum to phylum (such as the ability to see in colour), certain components, such as the visual pigments, appear to have a common ancestry and thus, evolved before animals radiated. (Haszprunar, 1995). Many more complex characteristics of the eye may have evolved 50-100 times, but using the same genes and proteins in their construction (Land et al, 2002). Here, the evolution of the eye will be explored, using both morphological and genetic evidence.
The first, most primitive eye, evolved during the Cambrian Explosion. This happened very quickly in geological terms, within a few million years. There is no fossil evidence for eyes before the Cambrian, but there is fossil evidence in assemblages such as the Burgess Shale and the Emu Bay Shale; Anomalocaris was the very first animal, which we know of, to have eyes, dating back 515 million years ago. Anomalocaris’ eyes were compound and evolved before jointed appendages or a hardened exoskeleton. These eyes were able to sense night and day, and were 30 times stronger than that of trilobites’. In fact, with 16,000 lenses, the resolution of the 3 centimetres wide eyes would have been rivalled only by that of the modern Dragonfly, which has 28,000 lenses in each eye (Salleh, Anna, 2011).
Here you can see a fossil of an Anomalocaris’ 2–3-cm paired eyes. Their preserved visual surfaces are composed of at least 16,000 hexagonally packed ommatidial lenses (in a single eye), rivalling the most acute compound eyes in modern arthropods. The specimens show two distinct taphonomic modes, preserved as iron oxide (after pyrite) and calcium phosphate. The inferred acuity of the anomalocaridid eye is consistent with other evidence that these animals were highly mobile visual predators in the water column (Briggs 1994).
But, before the Cambrian Explosion, organisms may have had a use for light sensitivity, but not for fast movement or navigation by vision. The poor fossil record of eyes makes their rate of evolution difficult to estimate however, simple modelling demonstrates that a primitive optical sense organ based upon efficient photopigments could evolve into a complex human-like eye in approximately 400,000 years (Nilsson & Pelger S 1994). One study at Lund University confirmed this; starting with a flat, light-sensitive patch, they gradually made over 1,800 tiny improvements- forming a cup, constricting the opening, adding a lens- until they had a complex, image-forming eye. Every change they made improved the image quality and these steps could have taken place in about 360,000 generations, or just a few hundred thousand years. 550 million years have passed since the formation of the oldest fossil eyes, enough time for complex eyes to have evolved more than 1,500 times.
A lot of the genetic ‘machinery’ used in the development of the eye is common to all eyed organisms suggesting that ancient ‘toolkit’ genes (opsins, Pax, and Otx) first evolved in a primitive ancestor that gave rise to all animals with eyes. And so, throughout evolution, these genes have been retained and the diversity of eyes we see in different animals are modifications built on top of this basic genetic framework. Opsins, which detect light, only evolved once. All opsins in eyed organisms today, are modified versions of this ancestor 600 million years ago. Different opsins detect a variety of intensities and wavelengths of light and so many species have a variety of opsins, which allows them to see a wide range of wavelengths; this forms the basis of colour vision.
A variety of proteins interact within a fully-functioning eye. Pax proteins are coordinators and attach directly to the DNA, turning on the necessary genes at the appropriate place and time. Oddly enough, Pax is the same in vertebrates and insects so must have evolved before they separated. Even organisms without eyes, such as sponges, have Pax genes; this finding suggests that Pax proteins originally controlled other processes and were later recruited into the eye. Those individuals born missing eyes had defects in the same gene- Pax6- this is required for normal eye development in all bilaterally symmetrical animals.
It appears that unicellular organisms had very primitive ‘eyespots’. These were made of photoreceptive proteins that sense light and dark, allowing these organisms to have photoperiodism- being able to time day and night. However, this is not sufficient enough for vision, as they cannot detect where the light is coming from, or distinguish shapes (Land and Fernald, 1992).
The three basic functions an eye needs are: light detection; shading, in the form of dark pigment, for sensing the direction light is coming from and connection to motor structures, for movement in response to light. Sometimes, all three of these functions are carried out by a single cell. The single-celled euglena has a light-sensitive spot, pigment granules for shading, and motor cilia. However, this is not considered as a true eye, but a stigma, a small splotch of red pigment which shades a collection of light sensitive crystals, and is located at its anterior end. With the flagellum, the eyespot allows the single-celled organism to move in response to light, often towards it to assist in photosynthesis (Land and Fernald, 1992). The most-basic structure that is widely accepted as an eye has just two cells: a photoreceptor that detects light, and a pigment cell that provides shading. The photoreceptor connects to ciliated cells, which engage to move the animal in response to light (Nilsson, D.-E., 2009).The marine ragworm embryo (below) has a two-celled eye.
Complex optical systems started out as multicellular eyespots gradually developing a depressed cup, granting the organism the ability to detect the direction of light, and then in iner and finer directions as the pit deepened. Pit eyes were seen in the Cambrian and were seen in ancient snails, and modern representatives such as planaria. This animal can slightly differentiate the intensity and direction 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. But, the proto-eye is still a lot more efficient at detecting the presence of lack of light, than its direction (Autrum, 1979).
As animals evolved more-complex bodies and behaviours, the eye too became more complex. Eyes evolved connections to muscle cells rather than cells that moved by waving cilia. Neurons evolved that could process signals and coordinate behaviour (Arendt, Hausen, Purschke, 2009). Based on cells, there appears to be two main designs for eyes- one is seen in the protostomes (molluscs, annelid worms and arthropods) and the other seen in deuterostomes (chordates and echinoderms) (Land and Fernald, 1992). The ‘pinhole camera’ eye is seen in protostomes such as nautiloids. It 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. These animals’ eyes have poor resolution and dim imaging, as they lack a cornea or lens, but are still a massive improvement from eyespots. To prevent infection, a transparent film of cells is grown over the pinhole (Dawkins, 1986). The segregated chamber contents specialised for optimisations such as colour filtering, higher refractive index, blocking of ultraviolet radiation, or the ability to operate in and out of water. It is likely that a key reason eyes specialise in detecting a 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 wavelength ranges of electromagnetic radiation (blue and green visible light) can travel through water (Fernald, 2001).
So, it seems that different forms of the eye, for example in vertebrates and molluscs, are often cited as a form of parallel evolution. Microvillous receptors of arthropods and molluscs depolarise in response to light, meaning that photon absorptions open Na+ channels. Ciliary receptors of vertebrates, in contrast, hyperpolarise in response to light by closing Na+ channels (Fernald, 2000). The structures of the two major chambered eyes, those of vertebrates and cephalopods, arise from distinctly different parts of the embryo. The cephalopod eye forms from an epidermal placode through successive infoldings, whereas the vertebrate eye emerges from the neural plate and induces the overlying epidermis to form the lens. The cephalopod eye also lacks a cornea, which is present in all vertebrates. The striking diversity in structure, function and development of extant eyes supports their polyphyletic origin (Fernald, 1997).
Flies have compound eyes; compared with simple eyes, compound eyes possess a very large view angle, and can detect fast movement and, in some cases, the polarisation of light (Völkel et al., 2003). Below is a table comparing simple eyes to compound ones. As you can see, compound eyes are ideal for insects as they detect movement and create a 3D image.
Trilobites also had compound eyes (although some were eyeless); their lenses were made of inorganic calcite crystal, a mineral that is also the main component of limestone and chalk. These crystal eyes are unique to trilobites, with the compound eyes of modern invertebrates being made of chitin, an organic substance. Due to their unusual composition, trilobite eyes were completely rigid and could not be adjusted to focus; instead, the trilobite corrected its focus with an internal eye mechanism which not only solved any potential problems caused by the mineral lens, but also gave the trilobite such good vision, that it could keep both close and distant objects in focus at the same time (Clarkson et al., 1975).
Even though we are vertebrates and cephalopods are not, our eyes seem very similar. Squid and octopus have arguably the best eyes in the invertebrate world. They have a camera-type eye, consisting of a lens projecting onto a camera. Unlike the vertebrate camera eye, the cephalopods’ form as invaginations of the body surface (rather than outgrowths of the brain), and consequently they lack a cornea. A cephalopod eye is focused through movement, like the lens of a camera or telescope, rather than changing the shape as the lens in a human eye does. The eye is almost spherical, like the lens, which is internal (Yamamoto, 1985). The crystalins, a water-soluble structural protein found in the lens and the cornea of the eye accounting for the transparency of the structure (Jester, 2008), used in the lens appear to have developed independently from vertebrate crystalins, suggesting a homoplasious, or convergent evolution, origin of the lens (Brahma, 1978).
The eyes of many animals show their evolutionary history in their contemporary anatomy. For example, our vertebrate eye is built ‘backwards and upside down’, whereas cephalopods’ eyes are built the ‘right way out’. We require photons of light to travel through the cornea, lens, aqueous fluid, blood vessels and all manner of cells before they reach the light sensitive rods and cones, allowing us to see. While such a construct has some drawbacks, it also allows the outer retina of the vertebrates to sustain higher metabolic activities as compared to the non-inverted design (Reichenbach and Bringmann2010). However, in the cephalopod eye, the nerves are attached to the rear of the retina, meaning they do not have a blind spot. This may because of the origins of eyes; in cephalopods they develop an invagination of the head surface whereas in vertebrates they originate as an extension of the brain.
Autrum, H (1979). “Introduction”. In H. Autrum (editor). Comparative Physiology and Evolution of Vision in Invertebrates- A: Invertebrate Photoreceptors. Handbook of Sensory Physiology. VII/6A. New York: Springer-Verlag. pp. 6–9.
Arendt, D., Hausen, H., Purschke, G. (2009). The ‘division of labour’ model of eye evolution. Philosophical Transactions of the Royal Society of London, Biological Sciences, 364(1531), 2809-2817.
Samir K. Brahma1 (1978). “Ontogeny of lens crystallins in marine cephalopods”
Brett Williamson (30 June 2011). “Ancient discovery puts world’s scientific eyes on Kangaroo Island”. ABC News (Australia).
Briggs, D. E. G. Giant predators from the Cambrian of China. Science 264, 1283–1284 (1994)
Clarkson, E. N. K.; Levi-Setti, R. L. (1975), “Trilobite eyes and the optics of Descartes and Huygens”, Nature 254 (5502): 663–7
Dawkins, Richard (1986). The Blind Watchmaker.
Fernald RD: The evolution of eyes. Brain Behav Evol
Fernald, Russell D. (2001). The Evolution of Eyes: Why Do We See What We See? Karger Gazette 64: “The Eye in Focus”.
Haszprunar (1995). “The mollusca: Coelomate turbellarians or mesenchymate annelids?”. In Taylor. Origin and evolutionary radiation of the Mollusca : centenary symposium of the Malacological Society of London. Oxford: Oxford Univ. Press.
“Homology”. Encyclopædia Britannica Online.
Jester JV (2008). “Corneal crystallins and the development of cellular transparency”. Seminars in Cell & Developmental Biology 19 (2): 82–93.
Lamb, T. D., Collin, S. P., Pugh, Jr., E. N. (2007). Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nature Reviews Neuroscience, 9(12), 960-976 (subscription required).
Land, M.F. and Nilsson, D.-E., Animal Eyes, Oxford University Press, Oxford (2002).
M F Land; R D Fernald (1992). “The Evolution of Eyes”. Annual Review of Neuroscience 15: 1–29
Nilsson, D.-E. (2009). The evolution of eyes and visually guided behaviour. Philosophical Transactions of the Royal Society of London, Biological Sciences, 364(1531), 2833-2847.
Nilsson, D-E; Pelger S (1994). “A pessimistic estimate of the time required for an eye to evolve”. Proceedings of the Royal Society B 256 (1345): 53–58
Reichenbach A, Bringmann A. (2010). Müller cells in the healthy and diseased retina. New York: Springer. pp 15 – 20.
Salleh, Anna (December 8, 2011). “Cambrian predator had killer eyes”. ABC Science.
Shubin, N., Tabin, C., & Carroll, S. (2009). Deep homology and the origins of evolutionary novelty. Nature, 457, 818-823
Völkel, R; Eisner, M and Weible, K. J (June 2003). “Miniaturized imaging systems” (PDF). Microelectronic Engineering. 67–68 (1): 461–472.
Vopalensky, P. & Kozmik, Z. (2009). Eye evolution: common use and independent recruitment of genetic components. Philosophical Transactions of the Royal Society of London, Biological Sciences, 364(1531)
Yamamoto, M. (Feb 1985). “Ontogeny of the visual system in the cuttlefish, Sepiella japonica. I. Morphological differentiation of the visual cell”. The Journal of Comparative Neurology 232 (3): 347–361