Evolution of Colour Vision

Introduction

Plants and animals display visual attractions, which are often colourful. The evolution of colour vision gave animals the opportunity to respond to these colourful signals to enhance their survival and fecundity. For instance, colour vision assisted with mate selection and food foraging. ^[1] Thus, colour vision could be considered to be a life supporting capacity.^[2]

One can define colour vision as the ability to discriminate the wavelength of light.^[4] In order to be able to discriminate wavelengths at least two types of photoreceptors is necessary.

These photoreceptors must have different yet overlapping spectral sensitivities. Wavelengths cause the two receptors to become excited and the colour signal that is provided is due to the ratios of the receptor excitations. More than one class of photoreceptor is mandatory for colour vision. ^[4]Two types of photoreceptor cells in vertebrates include rods and cones.

The rods and cones in vertebrates support night vision and colour vision, respectively. In general, the rods and codes vary in responsiveness as the cones are less sensitive than the rods and also respond more rapidly.^[3] The relative representation of the two types of receptors varies dramatically between species. This variation of receptors is largely niche-specific.^[5]

There is remarkable variation in colour vision among species.^[2] The eyes of insects have completely different structures than vertebrate eyes. But both types of eyes function and discriminate colour in similar ways.^[6] It is hypothesized that a primitive colour vision system might have been composed of two pigments. One pigment would be UV-sensitive to detect open areas because common light sources have short UV wavelengths. The other pigment would be middle/long wavelength sensitive to detect habitat or food-rich areas because the light reflected from objects mainly contains such wavelength.^[6] This system of two pigments may then have evolved into a broader range of wavelength sensitivities. This evolution would have occurred through the addition of other pigments along with the diversification of opsins.^[6]

Opsins have been classified into four groups based on their absorption spectra, whether they absorb UV, blue, green or red light. In vertebrates the opsins are subdivided into cone-opsins or rod-specifc opsins, also known as rhodopsins. ^[6] In vertebrates there are five opsin gene families with four linked to cone pigments and one linked to rod pigments.^[5]The opsins diversified after the separation of invertebrates and vertebrates occurred but both of these lineages are very similar.^[6]

Mammals

The eye is one of the more complex organs, having many different structures and layers that come together to perform one important task, the ability to see the world around us.

Layers of the Eye

The eye of a mammal can be divided into three main layers: the fibrous tunic, the vascular tunic, and the nervous tunic. All three parts perform specific tasks to enable vision in mammals. ^[10]

The Fibrous tunic, the outer layer of the eye, is formed by cornea and sclera. It consists of a dense connective tissue, which is filled with collagen and protects the eye as well as helping to maintain shape. ^[10]

The Vascular tunic, the middle layer of the eye, consists of the choroid, iris, and ciliary body. The choroid gives the inner eye a dark color, which helps in preventing disruptive reflections in the eye. The pupil, the main part of the iris, is black due to no light being reflected out of the interior eye. The ciliary body plays a role in lens focusing, as well as providing nutrients to the cornea. ^[10]

The Nervous tunic is the inner sensory layer of the eye, which houses the retina. ^[10]

Cones vs Rods

The retina is composed of three types of photosensitive cells. Out of the three, the two that play an important role in vision are cones and rods.

Cone cells are what enable us to see color vision, which are activated when they come into contact with bright light. The reason as to why we are able to see various colors is due to the different types of cones. There are three different types of cones: L (long), which is activated by long wavelengths and peaks at a yellowish color. The second cone is M (medium), which is in response to medium wavelengths and peaking at a green color. S (short) is the last type of cone, which is sensitive to short wavelengths and peaks and a blueish color. Cones are highly concentrated in the fovea, making this part where vision is the clearest and the most in focus. ^[12]

Rods on the other hand are photosensitive cells that enable us to see at night. In contrast to cones, rods work best under low light conditions, making them useful at night. Unlike cones, rods are spread evenly across the retina, but none are present in the fovea. This results in the vision at night not as clear as vision during the day. Rod cells are prevalent during night vision due to them being very sensitive to light. ^[13] A single photon of light can activate a rod cell, whereas it takes plenty more to activate cones.

Nocturnal Mammals

Nocturnality is a characteristic that is present in certain mammals that sleep during the day, and are mostly active during the night. ^[14] The structure of the eye is not much different from nocturnal mammals, and diurnal mammals. There are only a few significant differences that benefit the vision of nocturnal mammals at night. The most obvious difference between a nocturnal mammal and a diurnal mammal is the size of the eye. Having large eyes, accompanied by wider pupils and increased retinal surface, a nocturnal mammal is able to absorb much more light, which helps them see what is happening around them.

As explained in the section above, rod cells help with vision at night, whereas cones are active during the day. The eye of a nocturnal mammal is filled with rods, which are more helpful to them rather than cones. The lack of cones, results in nocturnal mammals having almost no color vision, meaning they only see black and white. Another downfall to not having many cones is that a nocturnal mammals vision is often blurry and not well focused. ^[15]

The other difference between nocturnal mammals and diurnal mammals is the presence of tapetum lucidum (bright tapestry). ^[15] Also known as “eye shine”, this is prevalent in nocturnal mammals, which increases the light being taken in by the mammal. It works by reflecting light back in the retina, and giving the mammal a second chance to absorb light and determine what it is seeing. Tapetum lucidum is an adaption that has grown over the years to improve vision for nocturnal mammals. ^[15]

Vision Variation Among Mammals

Horses have a type of vision called binocular vision.

With this kind of vision horses cannot see what is in between their eyes. The left eye will see the left side of a picture, while the right eye will see the right side and there will be no middle. ^[11]

Monkeys have vision that is almost similar to that of a human, which is trichromatic vision, in which they are able to see all three colors (red, green, blue) ^[11]

Pigeons have many more cones than humans do, resulting in them being able to see many more colours. They are thought to be one of the best at color detection on earth. ^[11]

Cats and dogs do not have the strongest of vision but due to their placement of eyes, they have a much better perception for depth and perspective than humans do. ^[11]

Snakes are equipped with infrared vision, and a pair of regular eyes for normal vision. They have vision “pits” that detect and see heat. ^[11]

Adaptations

Since sight is such a vital sense when hunting or being hunted, animals' eyes have adapted to best suit their situations. ^[10] Predator vision has adapted over the years, they have large, front facing eyes, which allow them to see best in the downward and forward direction. ^[10] This adjustment is made over generations, because of its ability to help predators in hunting and capture prey. Prey, on the other hand, generally have eyes situated more to the sides and top of the head. ^[10] Since prey are usually attacked from above, left or right, or behind, they adjusted over the years to have vision which is really good in those areas, resulting in poor frontal vision, because it is not needed as much.

Insects

Vision is the change in membrane potential of a photoreceptor induced by absorption of photons by pigments.^[7] The main differences between insect and vertebrate vision are in the response of photoreceptors to an increase in illumination (vertebrates hyperpolarize, insects depolarize upon illumination); and insects respond faster than vertebrates to illumination. Insects are known to live in very diverse habitats and visual conditions. They have very sophisticated visual systems. While it is popularly believed that insects see the world in a “pixelated” way, this is wrong. ^[7]

Eye structure

Insects have compound eyes. Their eye lens is composed of repetitive elements called “facets”.

The relative location of these facets and the photoreceptors responsible for vision determines the type an insect’s eyes falls into. There are two basic types: the apposition eye in which the photoreceptors reside within the optically individually isolated facets; and the superposition eye in which the optical apparatus is separated from the photoreceptors by a zone with many facets acting together as one. Apposition type eyes are generally found in insects with diurnal lifestyles. ^[7]

It is these compound eyes that allow insects to recognize and react to same species individuals, distinguish and avoid predators, forage for food, and navigate. ^[9] Compound eyes are composed of structural units called ommatidia which are composed of 8-9 photoreceptor cells. ^[8] The ommatidia are classified according to rhabdom structure, a protrusion of photoreceptor cells that bears visual pigments. These rhabdoms may be open, in which case, each photoreceptor cell has its own and see its individual portion of the visual field; fused, which act as lateral filters for the other; and tiered, in which photoreceptor cells filter the light that reaches more proximal photoreceptor cells. Most insects have a combination of fused and tiered rhabdoms.

Photoreceptors

There is a very high diversity of color receptor across insect species. This is believed to offer great potential for adaptation. ^[8] Found within these receptors are the opsins which fall into three major clades: UV, blue, and green. UV receptors have been found in every species while red receptors have been observed in very few species. Lifestyle has been suggested as a factor contributing to the kind of receptor present or absent in each species but has been rejected since species with the same receptor have also been observed to have very different lifestyles. For example, the owlfly, cockroach, and some ants have been noted to lack blue receptors. These species differ widely in lifestyle so there is likely no common adaptive cause for the loss of on receptor type. It has been concluded that the Devonian ancestor of all pterygote insects likely possessed UV, blue, and green receptors.

UV-receptors have been suggested to be optimally suited to detect the open sky or to detect small objects against the bright sky. ^[8] It has also been demonstrated as a useful ability of pollinating insects. For example bees can distinguish between similar looking flowers. This makes them be more efficient nectar collectors and pollenizers. Green-receptors are also important for honey bees. It is related to the motion-perceptual channel which makes it very suitable to the habitats inhabited by bees which are plentiful in green leaves. Blue-receptors have also been correlated to nectar rewards. Although thought so, it is not known with certainty whether the ancestral ommatidium contained all three color receptor types, with fewer receptor types arising after as adaptations or not. It is also not known how quickly dorsal-ventral differences in receptor distributions evolve.

Chromophores

The chromophores are densely packed in the rhabdomere which allows a larger surface area. ^[7] The visual pigment in insect is a protein called opsin that is bound to the light-sensitive chromophore. Once a photon has been captured, the chromophore isomerizes and a shape change occurs in the protein. Most insects use one or two chromophores, A1 or A3, or both. This has been said to be linked with the precursors of A1 and A3, carotene and xanthophylls obtained from plants. Xanthophylls are derived from carotene in a process that requires molecular oxygen. It has been argued that the large increase in atmospheric oxygen during the Carboniferous period may have increased the reaction rate of xanthophyll synthesis and hence increased the A3 precursor availability. ^[8]

Evolutionary development

It has been questioned if similarities between insects are adaptations for an unknown common purpose, but it has been suggested that instead, insects might have certain constraints that does not allow them to adapt as usual. ^[8] Receptor types also have been observed to differ between sexes. For example, in the butterfly species, L. heteronea, the males have blue-green visual capacity, while females have additional red receptors. This is thought to be an adaptation to detect the red foliage of the host plants for ovipositioning by females.

While adaptation, genetic drift, and differences in opsin protein expression have been suggested, the most parsimonious idea is that these differences are due to inheritance from common ancestors and retaining these specific adaptations due to constraints. ^[8] Not all differences between populations may be adaptive, random evolutionary processes might also be responsible. Differences might also be due to effects opsin expression which has been linked to developmental constraints, fine-scale molecular characterization, and developmental mechanisms. It is believed that if the developmental processes that regulate opsin expression are relatively easy to modify genetically, eyes might be more easily modified by natural selection. In contrast, if opsin expression is regulated by processes that are not easily modified, then the observed patterns of opsin expression might be a direct reflection of such developmental constraints. ^[8]

Birds

Eye Structure

The avian eye is fairly similar to the mammals in structure with some very important variations:

First, the lens of the eyeball is flattened, and placed as far away from the retina as possible. This helps the bird see far in the distance as it functions as a telescope. By having the lens farther away, it increases the focal length, thus magnifying the image for the bird. This aids in the birds ability to see predators or prey far away, but it makes it so that most birds are myopic. To ensure the maximum amount of light possible comes through, they also have large pupils and a highly curved cornea. There are strong muscles in the eye that allow the bird to contract and further curve their cornea and lens when needed, which increases the refractive power of both.

This produces the brightest, clearest image possible. ^[16] The retina also displays some important differences that attain to bird vision. They are densely packed with photoreceptors to produce extremely clear images. The type of receptors that dominate depend on whether they are diurnal or nocturnal. Diurnal animals need good vision in bright sunlight so they have a very high concentration of cones. This means however, that there isn’t room for many rods and, subsequently, they have very poor night vision. The opposite is true of course for nocturnal animals (i.e. an owl). This means that diurnal birds are almost blind at night, and the same goes for nocturnal birds during the day. ^[16] Songbirds have about 120,000 cones/mm2 whereas humans have around 10,000 cones/mm2. This explains why birds are able to see UV light under daylight conditions, and we are not. Humans have about 200,000 rods/mm2 whereas owls have 1,000,000 rods/mm2. This explains why owls can see so much better at night than humans. Another important difference between a human retina and an avian retina, is the lack of blood vessels present. The blood vessels in our retina causes the light to scatter and leads to lower acuity. ^[17] The blood vessels in an avian retina are concentrated in a structure called the pectin so that they don’t disturb the integrity of the image. The avian retina also exhibits an inner nuclear layer that is far more rich in horizontal and amacrine cells than primates. The complex inter-connections in their retina lead to visual processing to occur at a lower level than in primates. The avian retina is able to process visual information that would be processed in the forebrain in primates. ^[20]

Photopigments

Another important distinguishing factor is the presence of not 3, but 4 or 5 visual pigments (depending on the species) which leads to much greater color sensitivity compared to our own. By sequencing the SWS1 gene in birds, it was determined that birds can see twice as well as humans due to the 4 classes of cones found.

Thus birds are either tetrachromatic or pentachromatic. ^[21] Each type of cone is sensitive to a narrow range of light. SWS1 cone is most sensitive to UV (shortwave) light. It is important for many birds to have the ability to distinguish UV light for many reasons including, but not limited to, finding food, detecting plumage coloring in mates and seeing predetors and prey. ^[22]

UV Vision

In a study of Zebra Finches, they used filters on the female finches’ eyes to study their behavioral responses to males with different types of filters. They found that when they couldn’t sense the UV differences, they were far less interested in the males then when they couldn’t sense one of the other colors, even though humans cannot detect the difference in UV, it appears to be very important for birds. ^[18]

The UV vision also helps them sense polarization patterns and intensity gradients form in the sky which helps them orient themselves during flight. Most fruit eaten by birds reflect UV light, whereas the leaves of the plants do not and appear duller.

This helps the fruit stand out to birds so they can forage more quickly and efficiently. ^[19] They also have a different type of photoreceptor called a doublecone. These doublecones contain a principle cone and an accessory cone that curves around the principle cone. This allows the birds to process color within the photoreceptors themselves. ^[20]

Oil Droplets

Many species of birds also have oil droplets in their eyes to filter different light (ex. Sea birds have red oil droplets to filter the blue light from the ocean surface and produce a clearer image). These droplets are composed of lipids and dissolved carotenoid pigments and are located at the distal end of inner cone segments and cover entire width of the receptor. The light therefore passes through the oil before it reaches the photosensitive outer segment. These oils act as cut off filters as they absorb light below their characteristic wavelength of transmission and conveying longer wavelength to their associated photopigments. The net effect is a shift towards longer wavelengths which enhances contrast and creates a clearer image. ^[20]

Fish

The term fish describes a taxonomic group of huge diversity, living in extremely different spectral environments in streams, lakes, and oceans around the world. While some classes, such as hagfish (myxini), lamprey (Petromyzontida), or sharks (Chondrichthyes) have existed for hundreds of millions of years and are considered ‘living fossils’, the fish that humans are most familiar with are teleost fish, particularly the Salmoniformes and Perciformes. ^[26] With increasing depth and turbidity, less light is available. While red and orange with their long wavelength, and ultraviolet with its very short wavelength are absorbed rapidly, green, violet, and especially blue can penetrate the water bodies much deeper. ^[2]

Anatomy

Through the optic characteristics of water, particularly refraction, light appears to come from numerous sources, instead of just from one as on land. Reflection off planktonic particles in the water column, reefs, sand, and scales of other fish lead to diffuse light approaching the eye from all angles. This led to the evolution of very round eyes that secondarily flattened in mammals. While humans are able to alter the curvature of the lens in order to shift their focus to a different distance, fish lenses are rigid. Instead, they can vary the distance from lens to retina by shifting their lens. Cameras function similarly. ^[24] The round lens results in very good vision at close range. Additionally, the iris cannot expand or contract. As light intensity is never very high under water, there was never a need for such an adaptation. ^[24] Many fish living in the dark deep sea have enlarged eyes to capture any light that does penetrate that deeply (especially around 480nm wavelength), or that is emitted through bioluminescence. ^[24]

Rods and Cones

As rods are used to detect light in general, they are more prevalent in deep sea fishes. Such dark water fishes can have a rod to cone ratio of several hundred to one. Contrarily, a coral reef fish living in shallow water can have a cone to rod ratio of 10:1. Retinal cones detect the colour ranges of light. ^[25]

This results in fish living in scotopic (dark) environments not being able to see much chromatic and spatial detail. Some deep-sea fish even reduced their cones completely.

Additionally, they evolved a tapetum behind the photoreceptors. This tapetum reflects the little bit of light that is available back through the photoreceptors increasing the stimulation of the latter. This also results in the phenomenon of eyeshine. ^[24]

Many fish in photopic (light intense) environments have more than one spectral class of cones, just like some birds, they can have double, triple, or even quadruple cones. It is thought that multiple cones enhance chromatic and spatial sensitivity. Some fish that start their lifecycle near the surface may have only one set of cones, but gain a second set when they move down in the water column when reaching maturity. The multitude of cone structures allows fish to have the largest spectral range of all vertebrates, namely from 320nm to 800nm. ^[24] There is even a difference between fresh and salt water fish eyes. On the one hand, fresh water better transmits longwave radiation, so fresh water fish have rather red-shifted visual pigments. On the other hand, salt water is better at transmitting long-wave radiation, leading to blue- and violet-shifted pigments. Widespread fresh water pigments are porphyropsin, compared to rhodopsin in oceanic fish. Migratory fish, such as salmon, have adapted to these changing spectral environments by altering their pigments over their lifecycle. This change in pigments is reached through activation and deactivation of specific genes. ^[24]

Origin of the Optic Organ

Adult lampreys, which are considered living fossils and the earliest vertebrates, have astonishingly similar eyes to humans. They already have a lens, iris, retina, photoreceptors, and extra-ocular muscles, but they lack intra-ocular muscles and greater specialization found in gnathostomes. ^[27] When looking at the next ancestral lineage, one can find some differences that may explain the origin of the eye. Hagfish, which are chordates, but not vertebrates, have light sensitive organs that lack iris, cornea, extra- or intra-ocular muscles. These primitive eyes are located beneath an unpigmented layer of transparent skin. The photoreceptors of the retina are directly connected to ganglion cells, which serve as output neurons that connect to the hypothalamus region of the brain. Because the photoreceptors are poorly organized, they look a lot like the pineal organs of non-mammalian vertebrates. Behavioural studies indicate that hagfish are nearly blind, so that their primitive eye spots are assumedly used in regulating their circadian clock. ^[27] The lamprey, being the most ancestral vertebrate, illustrates next step the eye took in evolution very nicely. In Sea Lamprey (Petromyzon marinus), the filter feeding larval lamprey, also known as the ammocoete, has eyes that resemble those of hagfish. As it slowly grows and then transforms into a predatory adult, the optic organ differentiates into ganglion cells, amacrine and horizontal cells, and photoreceptors. During this metamorphosis, the organ grows, a lens and a differentiated cornea develop, ocular muscles are built up, and the eye breaks through the skin and now sits at the surface. All this is believed to have evolved between 530 and 500 mya, giving the lamprey a huge competitive advantage over blind organisms. ^[27]

Variation Due to Adaptation

As fish live in a such different habitats and have various life histories, it is not surprising that fish eyes are not all equal. Bottom dwelling fish, such as rays, have eyes that sit on the dorsal side of its head, looking upwards. ^[25] UV vision is common in some taxa, while others don’t have it, and others again are capable of seeing UV light for some part of their life. Some prey fish, such as the Ambon damselfish (Pomacentrus amboinensis) reflect UV light off their scales in order to warn other damselfish of predators or to recognize other fish of the same species. ^[28] UV vision has been traced back to a common ancestor gnathostome. UV vision can be used for foraging, mate choice, and communication, giving organisms with UV vision a selective advantage. Conversely, if the fish doesn’t live in shallow waters, UV light will not be available, while violet light penetrates the open water much deeper. Switching from UV to violet helps see, survive, and reproduce in those deeper waters. The gene responsible for this adaptation is SWS1. ^[29]

Another reason to switch to violet vision is that UV light at about 360nm wavelength can damage retinal tissues. Yellow pigments in the lenses can help deflect damaging UV light. Some fish, such as the brown trout (salmo trutta) turn off their SWS1 gene when they mature, as they move from shallow to deeper waters. ^[29] Many deep sea fish, those living below 200m, have bright yellow lenses in order to absorb large parts of the shortwave end of the spectrum, especially between 468 – 494nm. This seems to be an adaptation for the detection of bioluminescence. Interestingly, a species of deep sea dragonfish (malacosteus niger) is able to both produce and see red bioluminescence (about 700nm wavelength). No other organism in that environment has been shown to be able to absorb light at these longer wavelengths. Thus, it appears to be a private signal invisible to predators and prey, while helping find a mate. ^[24] ^[23]

While most fish have symmetrical lenses, so called ‘four-eyed’ fish (Anableps anableps), have an asymmetrical lens that facilitates simultaneous vision in air and water. ^[31] It is interesting to note that fish vision improves as they become older. This is due to enlarged lenses and the continuous addition of photoreceptors. ^[24]

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