What is Color Vision?
Biological Significance of Color Vision
Visual Pigment
Color Vision and Visual Pigments
Visual Opsin Repertoire in Vertebrates
Creation of Opsin Subtypes in Fish and Primates
Primate Color Vision
Color Vision Variation in New World Monkeys
What's Good with Color Vision Variation in New World Monkeys?

What is Color Vision?

Color vision is the sensation of perceiving different wavelengths of light differently. Color is not a physical entity of environment but a brain-made painting to distinguish different wavelengths of light. Color vision may differ greatly among animals. Human color vision is just one example of animal vision and is not particularly excellent compared to other species.


Biological Significance of Color Vision

Color can provide us with important information relevant to foraging, mate choice, competitors, predators, harmful objects, landscape, etc. Coloration of animals and plants conveys a message only when their observers can perceive it. Therefore, color vision can be a driving force of evolution of colorations, and, vice versa, colorations can drive color vision evolution.


Visual Pigment

There are two types of photoreceptor cells in vertebrate retina, rods and cones. Rods work for dim-light vision whereas cones work for daylight and color vision. These cells sense light by photoreceptive molecules called visual pigments.
　Visual pigments consist of a protein moiety, opsin, and a light-sensing chromophore, retinal (vitamin A aldehyde). Opsin is a seven-transmembrane protein that surrounds the chromophore with the seven transmembrane domains, hence directly affecting the electrostatic environment and energy status of the chromophore. Thus, the range of absorption wavelength of a chromophore differs greatly depending on the opsin type surrounding it. One advantage of studying opsins in evolutionary genetics is that visual pigments can be reconstituted and their absorption spectra are measurable in the lab.


Color Vision and Visual Pigments

With a few exceptions, one photoreceptor cell produces one type of opsin. Roughly speaking, the number of visual pigment types possessed by an animal corresponds to the number of photoreceptor cell types in the retina of the animal. Color vision is the brain-computation outcome of neuronal signals from different types of (cone) photoreceptor cells with different wavelength sensitivities. So, with more numbers of cone photoreceptor types (up to, say, four), color vision becomes more complicated and sophisticated. With only one cone visual pigment type in the retina, such animals cannot distinguish wavelengths and would be colorblind. Principally, with two, three, and four cone visual pigment types, animals would be dichromatic, trichromatic and tetrachromatic in color vision, respectively. Many mammals are dichromatic and not completely colorblind. While many humans are trichromatic (see the figure below), many birds, lizards and fish are tetrachromatic or, possibly, more.

Absorption wavelength of human visual pigments Many humans are trichromatic with three cone visual pigments (red, green and blue). A pigment indicated with black is the rod visual pigment specialized for dimlight but not for color vision.

Visual Opsin Repertoire in Vertebrates

There are only two types of retinal chromophore for vertebrate visual pigments and only one of them (11-cis retinal) is used in most terrestrial vertebrates. On the other hand, there are five types of opsins used for vertebrate visual pigments. Furthermore, each opsin type has diverged evolutionarily through gene duplications and/or amino acid substitutions. Therefore, opsin has made tremendous contribution to the diversity of color vision among vertebrates.
　Five types of opsins are considered to have emerged from a common ancestor of vertebrates on the basis of molecular phylogenetic analyses (see the figure below). The five types of opsins are: RH1 (specialized opsin for rod photoreceptor cells [rod opsin, also generaly called "rhodopsin"]), RH2 (green-sensitive cone opsin), SWS2 (blue-sensitive cone opsin), SWS1 (uv-to-blue sensitive cone opsin), and M/LWS (red-green sensitive cone opsin).

Creation of Opsin Subtypes in Fish and Primates

Basically, fish, reptiles and birds retain all four cone opsin types as well as rod opsin, and hence are tetrachromatic. In contrast, mammals lost RH2 and SWS2 types of opsins probably in their nocturnal ancestor during dinosaur's era and retain only M/LWS and SWS1 cone opsins and rod opsin. This is the reason why mammals are basically dichromatic. Some nocturnal mammals, including some nocturnal primates, further lost SWS1 opsin and hence are completely colorblind.
　Characteristic of higher primates is restoration of high dimensional color vision (trichromacy) by creating subtypes in the M/LWS type of opsins. Human red and green opsins are such subtypes in the M/LWS type. Creation of opsin subtypes is unique in primates among terrestrial vertebrates. However, it appears a common feature among bony fish. Among bony fish, subtypes have been found in all five opsin types. This probably mirrors highly variable light environments in water depending on depth, microorganisms contained, muddiness, etc. These subtypes occurred through opsin gene duplication in most cases, and in a few cases through allelic diversification of opsin genes.
　Fish and primates are thus excellent subjects to study the evolution of color vision and its diversification.

Vertebrate visual opsin gene repertoire

	M/LWS	RH2	SWS2	SWS1	RH1
Fish	◎	◎	◎	◎	◎
Amphibians	○	?	○	○	○
Reptiles	○	○	○	○	○
Birds	○	○	○	○	○
Mammals	○	×	×	○	○
Higher Primates	◎ （Red・Green）	×	×	○ （Blue）	○
Nocturnal Primates*	○	×	×	×	○

○, one gene present; ◎；two or more subtype genes known (gene duplication or allelic variation); ×, absent; ?, presence unknown. *Owl monkey (a New World monkey) and lorisiform prosimians lack functional SWS1 opsin gene, but other nocturnal primates seem to retain it (Kawamura and Kubotera 2004).


Primate Color Vision

Mammalian M/LWS opsins are also called red-green opsins and the genes are located on the X chromosome. The gene is duplicated and the duplicated genes are differentiated to so called red and green opsin genes in common ancestor of catarrhines (human, apes and Old World monkeys). With the two M/LWS opsins and an autosomal SWS1 (called blue) opsin, these primates became trichromatic in color vision. Prosimians (the most distant primate group from human) are basically dichromatic with one each of red-green and blue opsin gene as many mammals. New World monkeys, phylogenetically in-between catarrhines and prosimians, are very unique in having polymorphic color vision, through allelic variation (typically three variants) of single-locus red-green opsin gene.



Color Vision Variation in New World Monkeys

Males have only one X chromosome and have only one allelic red-green opsin gene. Therefore, male New World monkeys are doomed to be dichromatic having only one red-green opsin allelic gene and one autosomal blue opsin gene. However, it should be noted that three dichromatic phenotypes can appear among males because of the three allelic variations of red-green opsin gene. Females with two identical red-green opsin alleles are also dichromatic with the three different phenotypes. Either one of the two X chromosomes of females is inactivated in mammals, and only one allele of the red-green opsin gene is expressed in a given red-green cone photoreceptor cell. So, females with two distinct red-green opsin alleles have three distinctive cone cell types in the retina, two different red-green cone cell types and a blue cone cell type, and are trichromatic. Again, three trichromatic phenotypes are possible by combinatorial differences of the red-green opsin alleles possessed. As a whole, six different color vision types co-exist within one species in New World monkeys.




What's Good with Color Vision Variation in New World Monkeys?

Color vision variation has been observed in many genera of New World monkeys including spider monkeys, sakis, capuchins and marmosets. This implies that the polymorphism of vision arose in their common ancestor and has persisted for a long evolutional time (> ~25 million years). This suggests the great importance of this variation for the New World monkeys. However, it is largely unknown how the color vision is used by them and whether the variation is associated with any of their behaviors. Food items and foraging behaviors are incredibly diverse among species of New World monkeys. To explore correlations between color vision variation and behavioral variation, it is necessary to carry out a field work in which color vision types are determined for wild populations of New World monkeys and their behaviors are assessed in light of vision types.
　New World monkeys provide a rare and excellent opportunity to study the relationship between vision and behavior. The study of adaptive meaning of vision type variation in New World monkeys would also shed a new light on why we humans have red-green colorblindness and anomalous trichromacy in our population.



Phylogeny of New World monkeys Variations in color vision have been reported for New World monkey species in the genera indicated with red letters. Howler monkeys and owl monkeys (indicated with black letters) are exceptions. Howler monkeys acquired uniform trichromacy (like the one catarrhine primates, including humans, have) independently from catarrhines while owl monkeys, the only nocturnal primate among New World and catarrhine primates, lost allelic variation of red-green opsin gene and the functional blue opsin gene and consequently are monochromatic. Color vision of monkeys indicated with gray letters is unknown.