Evolution of color vision in primates

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Baboons, like other old world monkeys and apes, have eyes which can discern blue, green and red wavelengths of light Olive Baboon Papio anubis in Tanzania 4426 cropped Nevit.jpg
Baboons, like other old world monkeys and apes, have eyes which can discern blue, green and red wavelengths of light

The evolution of color vision in primates is highly unusual compared to most eutherian mammals. A remote vertebrate ancestor of primates possessed tetrachromacy, [1] but nocturnal, warm-blooded, mammalian ancestors lost two of four cones in the retina at the time of dinosaurs. Most teleost fish, reptiles and birds are therefore tetrachromatic while most mammals are strictly dichromats, the exceptions being some primates and marsupials, [2] who are trichromats, and many marine mammals, who are monochromats.

Contents

Cones and opsins

While color vision is dependent on many factors, discussion of the evolution of color vision is typically simplified to two factors:

In vertebrates, both of these are almost perfectly correlated to an individual's cone complement.

The retina comprises several different classes of photoreceptors, including cone cells and rod cells. Rods usually do not contribute to color vision (except in mesopic conditions[ citation needed ]) and have not evolved significantly in the era of primates[ citation needed ], so they will not be discussed here. It is the cone cells, which are used for photopic vision, that facilitate color vision.

Each type - or class - of cones is defined by its opsin, a protein fundamental to the visual cycle that tunes the cell to certain wavelengths of light. The opsins present in cone cells are specifically called photopsin. The spectral sensitivities of the opsins are dependent on their genetic sequence. The most important (and often only important for discussions of opsin evolution) parameter of the spectral sensitivity is the peak wavelength, i.e. the wavelength of light to which they are most sensitive. For example, a typical human L-opsin has a peak wavelength of 560 nm. The cone complement defines an individual's set of cones in their retina - usually consistent with the set of opsins in their genome.

The breadth of an individual's visual spectrum is equal to the minimum and maximum wavelengths to which at least one of their cones is sensitive. In vertebrates, the dimensionality of the color gamut is usually equal to the number of cones/opsins, though this simple equivalence breaks down for invertebrates.

Primate cone complement

The cone complements exhibited by primates can be monochromatic, dichromatic or trichromatic. The catarrhines (Old World monkeys and apes) are routine trichromats, meaning both males and females possess three opsins classes. [3] In nearly all species of platyrrhines (New World monkeys) males and homozygous females are dichromats, while heterozygous females are trichromats, a condition known as allelic or polymorphic trichromacy. Among platyrrhines, the exceptions are Alouatta (routine trichromats) and Aotus (routine monochromats). [4] [5]

All primates with the exception of Aotus exhibit an S-opsin (short wave sensitive) in the cone most sensitive to blue light (S-cone). This opsin is encoded by an autosomal gene on chromosome 7. The other cones differ between primates.

Catarrhine cone complement

The taxa Catarrhini includes old world monkeys (e.g. baboons) and apes (e.g. humans). In addition to the S-opsin, catarrhine primates have two adjacent opsin genes on the X chromosome: [6]

Platyrrhine cone complement

The taxa Platyrhini includes new world monkeys (e.g. Squirrel monkeys). In addition to the S-opsin, trichromatic platyrrhine primates generally have only a single opsin gene locus, but it is polymorphic, with different alleles encoding opsins of different peak wavelength. Individuals homozygous for the gene will have only two opsin classes and therefore exhibit dichromacy. However, heterozygous individuals will have three opsin classes and therefore be trichromats. Since the gene is on the X-chromosome, [6] of which males possess only one, all males are monozygous. They therefore always have 2 opsin classes and are dichromatic. Females can be either heterozygous or homozygous, so can be either dichromats or trichromats. [7]

Phylogenetics

Mammalian Ancestors

The common vertebrate ancestor (ca. 540MYA) had 4 photopsins in their complement (SWS1, SWS2, Rh2, LWS) and likely had tetrachromatic vision. Today, most other vertebrate classes have retained their 4 cones and exhibit tetrachromacy, including birds, reptiles, teleosts (fish) and amphibians. However, mammalian ancestors lost 2 of the 4 opsins due to the nocturnal bottleneck and most modern mammals are therefore dichromats, retaining only the SWS1 (UV–sensitive) and LWS (red–sensitive) opsins. [8] There is little data indicating the advantages of UV-sensitivity in early mammals that led to the retention of SWS1 instead of SWS2 and Rh2 opsins. [8]

Approximately 35 MYA the LWS class of opsins in catarrhine ancestors split into OPN1MW and OPN1LW. [8] At about the same time, the SWS opsin shifted from its ancestral UV–sensitivity form to a violet-sensitive form with a peak wavelength of ~420 nm. [9]

Evolutionary pathway of SWS1

Mutagenesis experiments involving the Boreoeutherian ancestor to humans have shown that seven genetic mutations are linked to losing UV vision and gaining the blue light vision that most humans have today over the course of millions of years. [9] These mutations: F46T, F49L, T52F, F86L, T93P, A114G and S118T, include 5040 potential pathways for the amino acid changes required to create genetic changes in the short wavelength sensitive, or blue opsin. [9] Of the 5040 pathways, 335 have been deemed as possible trajectories for the evolution of blue opsin. [9] It has been discovered that each individual mutation has no effect on its own, and that only multiple changes combined following an epistatic pattern in a specific order resulted in changes in the evolutionary direction of blue vision. [9]

Incomplete trajectories, or evolutionary pathways, are shown to be caused by T52F mutations occurring first because T52F does not have a peak for the absorption of light within the entire visible region. [9] T52F mutations are deemed to be structurally unstable, and the evolutionary path is immediately terminated. Having any of the other stable mutations occur first, including F46T, F49L, F86L, T93P, A114G or S118T, opens up the possibility of having 1032 out of 5042 potential trajectories open up to evolution. [9] This is because having any of the other mutations occur first would allow for 134, 74, 252, 348, 102 and 122 potential pathways for mutations involving each of the remaining 6 mutants, equal to 1032 potential pathways for the evolution of short wavelength sensitive opsins to take place. [9]

Studies using in vitro assays have shown that epistatic evolution took place in ancestral Boreoeutherian species with the 7 mutations on genetically reconstructed Boreoetherian short wavelength sensitive opsins. [9] λmax values were shifted from a value of 357 nm  to 411 nm , an increase which indicated that human short wavelength sensitive opsins did indeed evolve from ancestral Boreoeutherian species using these 7 mutations. [9]

Further analysis has shown that 4008 out of the 5040 possible trajectories were terminated prematurely due to nonfunctional pigments that were dehydrated. [9] Mutagenesis results also reveal that ancestral human short wavelength sensitive opsin remained UV-sensitive until about 80 million years ago, before gradually increasing its λmax by 20 nm  75 million years ago and 20 nm  45 million years ago. It eventually reached the current λmax of 430 nm  30 million years ago. [9]

It is believed that middle and long wave sensitive pigments appeared after the final stages of short wavelength sensitive opsin pigments evolved, and that trichromatic vision was formed through interprotein epistasis. [9]

Early mammal ultraviolet vision, or ultraviolet sensitivity, included sensitivity in the wavelength ranges between 350 nm  and 430 nm . [8] These wavelengths are shorter than visible light but longer than X-rays. In some rare cases, some modern day humans can see within the UV spectrum at wavelengths close to 310 nm . [9]

In other animals that possess UV vision such as birds, ultraviolet sensitivity can be advantageous for courtship and reproductive success. This is because some birds have feathers with certain favourable colourations that can not be distinguished by human vision outside of the UV spectrum. [8]

It has been theorized that λ max-shifts might have been required as human ancestors started to switch from leading nocturnal lifestyles to more diurnal lifestyles. This caused their vision to adjust to various twilight settings over time. To identify the path from which short wavelength opsins evolved, increases in absolute max values were used by researchers with a limitation of approximately |Δλmax|<25 nm  per step. [9] This allows for subdivision of the 1032 potential pathways that were generated by analysis of first mutations beginning with any of the stable mutants: F46T, F49L, F86L, T93P, A114G or S118T to be narrowed down to 335 potential pathways. [9]

It was found that the last two mutations, F46T and T52F, occurred between 45 million and 30 million years ago as the absolute max for short wave length opsins was increasing from 400 nm  to 430 nm . [9]

Evolutionary pathway of LWS

Approximately 35MYA, ancestral Boreotherian LWS opsin class split into two opsin sub-classes, with one retaining the peak wavelength of 560 nm , equal to the ancestral value. [9] The other LWS opsin decreased its peak wavelength to 530 nm  and became the M-opsin, or green-sensitive opsin. The details of this split are disputed. Some evolutionary biologists believe that the L and M photopigments of catarrhines and platyrrhines had a common evolutionary origin; molecular studies demonstrate that the peak wavelengths of the three pigments in both sub-orders is the same. [10] There are two popular hypotheses that explain the evolution of the primate vision differences from this common origin.

Polymorphism

The first hypothesis is that the two-gene (M and L) system of the catarrhine primates evolved from a crossing-over mechanism. Unequal crossing over between the chromosomes carrying alleles for L and M variants could have resulted in a separate L and M gene located on a single X chromosome. [6] This hypothesis requires that the evolution of the polymorphic system of the platyrrhine pre-dates the separation of the Old World and New World monkeys. [11]

This hypothesis proposes that this crossing-over event occurred in a heterozygous catarrhine female sometime after the platyrrhine/catarrhine divergence. [4] Following the crossing-over, any male and female progeny receiving at least one X chromosome with both M and L genes would be trichromats. Single M or L gene X chromosomes would subsequently be lost from the catarrhine gene pool, assuring routine trichromacy.

Gene duplication

The alternate hypothesis is that opsin polymorphism arose in platyrrhines after they diverged from catarrhines. By this hypothesis, a single X-opsin allele was duplicated in catarrhines and catarrhine M and L opsins diverged later by mutations affecting one gene duplicate but not the other. Platyrrhine M and L opsins would have evolved by a parallel process, acting on the single opsin gene present to create multiple alleles. Geneticists use the "molecular clocks" technique to determine an evolutionary sequence of events. It deduces elapsed time from a number of minor differences in DNA sequences. [12] [13] Nucleotide sequencing of opsin genes suggests that the genetic divergence between New World primate opsin alleles (2.6%) is considerably smaller than the divergence between Old World primate genes (6.1%). [11] Hence, the New World primate color vision alleles are likely to have arisen after Old World gene duplication. [4] It is also proposed that the polymorphism in the opsin gene might have arisen independently through point mutation on one or more occasions, [4] and that the spectral tuning similarities are due to convergent evolution. Despite the homogenization of genes in the New World monkeys, there has been a preservation of trichromacy in the heterozygous females suggesting that the critical amino acid that define these alleles have been maintained. [14]

Ultimate causation hypotheses

There exist several theories for the main evolutionary pressure that caused primates to evolve trichromatic color vision, namely the red-green opponent channel.

Fruit theory

Simulation of trichromatic (above) and dichromatic (below) perception of red and green apples Assorted Red and Green Apples (deuteranope view).jpg
Simulation of trichromatic (above) and dichromatic (below) perception of red and green apples

This theory postulates that trichromacy became favorable due to the increased ability to find ripe fruit against a foliage background. Research has found that the spectral separation between the L and the M cones is closely proportional to the optimal for detection of many colors of fruit (red) against foliage (green). [15] The reflectance spectra of fruits and leaves naturally eaten by the Alouatta seniculus were analyzed and found that the sensitivity in the L and M cone pigments is optimal for detecting fruit among leaves. [16]

While the “fruit theory” holds much data to support its reasoning, [15] [16] [17] [18] some recent research has criticized this theory. [19] One study shows that the difference in the fruit-spotting task between trichromats and dichromats is largest when the tree is far away (~12m), inferring that the evolutionary pressure may have been on spotting fruit trees from a distance, rather than picking fruit. [20] Those findings were based upon the fact that there is a larger variety of background S/(L+M) and luminance values under long-distance viewing. [18] However, spatiochromatic properties of the red-green system of color vision may be optimized for detecting any red objects against a background of leaves at relatively small viewing distances equal to that of a typical “grasping distance." [21]

Young leaf hypothesis

This theory is centered around the idea that the benefit for possessing the different M and L cone pigments are so that during times of fruit shortages, an animal's ability to identify the younger and more reddish leaves, which contain higher amounts of protein, will lead to a higher rate of survival. [7] [22] In addition, a prominent visual discriminant between young and mature leaves is their red-green color channel, which is only discernible to trichromats. [23] This theory supports the evidence showing that trichromatic color vision originated in Africa, as figs and palms are scarce in this environment thus increasing the need for this color vision selection. However, this theory does not explain the selection for trichromacy polymorphisms seen in dichromatic species that are not from Africa. [22]

Evolution of olfactory systems

The sense of smell may have been a contributing factor in selection of color vision. One controversial study suggests that the loss of olfactory receptor genes coincided with the evolved trait of full trichromatic vision; [24] this study has been challenged, and two of the authors retracted it. [25] The theory is that as sense of smell deteriorated, selective pressures increased for the evolution of trichromacy for foraging. In addition, the mutation of trichromacy could have made the need for pheremone communication redundant and thus prompted the loss of this function.

Overall, research has not shown that the concentration of olfactory receptors is directly related to color vision acquisition. [26] Research suggests that the species Alouatta does not share the same characteristics of pheromone transduction pathway pseudogenes that humans and Old World monkeys possess and leading howler monkeys to maintain both pheromone communication systems and full trichromatic vision. [27]

Therefore, trichromacy alone does not lead to the loss of pheromone communication but rather a combination of environmental factors. Nonetheless research shows a significant negative correlation between the two traits in the majority of trichromatic species.

Skin tone

Trichromacy may also be evolutionarily favorable in recognizing changes in skin tone. The spectral sensitivity of M- and L-opsins maximize sensitivity to changes in skin color that correspond to blood oxygen levels. [28]

Recognizing changes in skin tone that indicate states of health would be one advantage. Dichromatic humans report trouble with recognizing sunburn, rash, pallor and jaundice. [29] Recognizing when offspring are sick allows parents to care for or provide treatment to them. Likewise, mate choice that excludes sick individuals increases the viability of offspring. Similarly, other causes of skin tone change such as blushing or rump-reddening convey important information between potential sexual partners. [28] Therefore, the formation of trichromatic color vision in certain primate species may have been beneficial in recognizing the state of health/fertility of others.

Anomalies in New World monkeys

Aotus and Alouatta

There are two noteworthy genera within the New World monkeys that exhibit how different environments with different selective pressures can affect the type of vision in a population. [7] For example, the night monkeys (Aotus) have lost their S photopigments and polymorphic M/L opsin gene. Because these anthropoids are and were nocturnal, operating most often in a world where color is less important, selection pressure on color vision relaxed. On the opposite side of the spectrum, diurnal howler monkeys (Alouatta) have reinvented routine trichromacy through a relatively recent gene duplication of the M/L gene. [7] This duplication has allowed trichromacy for both sexes; its X chromosome gained two loci to house both the green allele and the red allele. The recurrence and spread of routine trichromacy in howler monkeys suggests that it provides them with an evolutionary advantage.

Howler monkeys are perhaps the most folivorous of the New World monkeys. Fruits make up a relatively small portion of their diet, [30] and the type of leaves they consume (young, nutritive, digestible, often reddish in color), are best detected by a red-green signal. Field work exploring the dietary preferences of howler monkeys suggest that routine trichromacy was environmentally selected for as a benefit to folivore foraging. [4] [7] [22]

See also

Related Research Articles

<span class="mw-page-title-main">Color</span> Visual perception of the light spectrum

Color or colour is the visual perception based on the electromagnetic spectrum. Though color is not an inherent property of matter, color perception is related to an object's light absorption, reflection, emission spectra and interference. For most humans, colors are perceived in the visible light spectrum with three types of cone cells (trichromacy). Other animals may have a different number of cone cell types or have eyes sensitive to different wavelength, such as bees that can distinguish ultraviolet, and thus have a different color sensitivity range. Animal perception of color originates from different light wavelength or spectral sensitivity in cone cell types, which is then processed by the brain.

<span class="mw-page-title-main">Color blindness</span> Decreased ability to see color or color differences

Color blindness or color vision deficiency (CVD) is the decreased ability to see color or differences in color. The severity of color blindness ranges from mostly unnoticeable to full absence of color perception. Color blindness is usually an inherited problem or variation in the functionality of one or more of the three classes of cone cells in the retina, which mediate color vision. The most common form is caused by a genetic condition called congenital red–green color blindness, which affects up to 1 in 12 males (8%) and 1 in 200 females (0.5%). The condition is more prevalent in males, because the opsin genes responsible are located on the X chromosome. Rarer genetic conditions causing color blindness include congenital blue–yellow color blindness, blue cone monochromacy, and achromatopsia. Color blindness can also result from physical or chemical damage to the eye, the optic nerve, parts of the brain, or from medication toxicity. Color vision also naturally degrades in old age.

<span class="mw-page-title-main">Visible spectrum</span> Portion of the electromagnetic spectrum that is visible to the human eye

The visible spectrum is the band of the electromagnetic spectrum that is visible to the human eye. Electromagnetic radiation in this range of wavelengths is called visible light. The optical spectrum is sometimes considered to be the same as the visible spectrum, but some authors define the term more broadly, to include the ultraviolet and infrared parts of the electromagnetic spectrum as well.

<span class="mw-page-title-main">Color vision</span> Ability to perceive differences in light frequency

Color vision, a feature of visual perception, is an ability to perceive differences between light composed of different frequencies independently of light intensity.

<span class="mw-page-title-main">New World monkey</span> Parvorder of mammals

New World monkeys are the five families of primates that are found in the tropical regions of Mexico, Central and South America: Callitrichidae, Cebidae, Aotidae, Pitheciidae, and Atelidae. The five families are ranked together as the Ceboidea, the only extant superfamily in the parvorder Platyrrhini.

<span class="mw-page-title-main">Catarrhini</span> Group of Old World monkeys and apes

The parvorder Catarrhini consists of the Cercopithecoidea and apes (Hominoidea). In 1812, Geoffroy grouped those two groups together and established the name Catarrhini, "Old World monkeys",. Its sister in the infraorder Simiiformes is the parvorder Platyrrhini. There has been some resistance to directly designate apes as monkeys despite the scientific evidence, so "Old World monkey" may be taken to mean the Cercopithecoidea or the Catarrhini. That apes are monkeys was already realized by Georges-Louis Leclerc, Comte de Buffon in the 18th century. Linnaeus placed this group in 1758 together with what we now recognise as the tarsiers and the New World monkeys, in a single genus "Simia". The Catarrhini are all native to Africa and Asia. Members of this parvorder are called catarrhines.

<span class="mw-page-title-main">Lagoon triggerfish</span> A triggerfish found on reefs in the Indo-Pacific region.

The lagoon triggerfish, also known as the blackbar triggerfish, the Picasso triggerfish, or the Picassofish, is a triggerfish, up to 30 cm in length, found on reefs in the Indo-Pacific region.

<span class="mw-page-title-main">Tetrachromacy</span> Type of color vision with four types of cone cells

Tetrachromacy is the condition of possessing four independent channels for conveying color information, or possessing four types of cone cell in the eye. Organisms with tetrachromacy are called tetrachromats.

<span class="mw-page-title-main">Trichromacy</span> Possessing of three independent channels for conveying color information

Trichromacy or trichromatism is the possession of three independent channels for conveying color information, derived from the three different types of cone cells in the eye. Organisms with trichromacy are called trichromats.

<span class="mw-page-title-main">Cone cell</span> Photoreceptor cells responsible for color vision made to function in bright light

Cone cells or cones are photoreceptor cells in the retinas of vertebrates' eyes. They respond differently to light of different wavelengths, and the combination of their responses is responsible for color vision. Cones function best in relatively bright light, called the photopic region, as opposed to rod cells, which work better in dim light, or the scotopic region. Cone cells are densely packed in the fovea centralis, a 0.3 mm diameter rod-free area with very thin, densely packed cones which quickly reduce in number towards the periphery of the retina. Conversely, they are absent from the optic disc, contributing to the blind spot. There are about six to seven million cones in a human eye, with the highest concentration being towards the macula.

Dichromacy is the state of having two types of functioning photoreceptors, called cone cells, in the eyes. Organisms with dichromacy are called dichromats. Dichromats require only two primary colors to be able to represent their visible gamut. By comparison, trichromats need three primary colors, and tetrachromats need four. Likewise, every color in a dichromat's gamut can be evoked with monochromatic light. By comparison, every color in a trichromat's gamut can be evoked with a combination of monochromatic light and white light.

<span class="mw-page-title-main">Monochromacy</span> Type of color vision

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<span class="mw-page-title-main">Melanopsin</span> Mammalian protein found in Homo sapiens

Melanopsin is a type of photopigment belonging to a larger family of light-sensitive retinal proteins called opsins and encoded by the gene Opn4. In the mammalian retina, there are two additional categories of opsins, both involved in the formation of visual images: rhodopsin and photopsin in the rod and cone photoreceptor cells, respectively.

<span class="mw-page-title-main">OPN1SW</span> Protein-coding gene in the species Homo sapiens

Blue-sensitive opsin is a protein that in humans is encoded by the OPN1SW gene.

<span class="mw-page-title-main">OPN1LW</span> Protein-coding gene in humans

OPN1LW is a gene on the X chromosome that encodes for long wave sensitive (LWS) opsin, or red cone photopigment. It is responsible for perception of visible light in the yellow-green range on the visible spectrum. The gene contains 6 exons with variability that induces shifts in the spectral range. OPN1LW is subject to homologous recombination with OPN1MW, as the two have very similar sequences. These recombinations can lead to various vision problems, such as red-green colourblindness and blue monochromacy. The protein encoded is a G-protein coupled receptor with embedded 11-cis-retinal, whose light excitation causes a cis-trans conformational change that begins the process of chemical signalling to the brain.

Color vision, a proximate adaptation of the vision sensory modality, allows for the discrimination of light based on its wavelength components.

Gene therapy for color blindness is an experimental gene therapy of the human retina aiming to grant typical trichromatic color vision to individuals with congenital color blindness by introducing typical alleles for opsin genes. Animal testing for gene therapy began in 2007 with a 2009 breakthrough in squirrel monkeys suggesting an imminent gene therapy in humans. While the research into gene therapy for red-green colorblindness has lagged since then, successful human trials are ongoing for achromatopsia. Congenital color vision deficiency affects upwards of 200 million people in the world, which represents a large demand for this gene therapy.

<span class="mw-page-title-main">Evolution of primates</span> Origin and diversification of primates through geologic time

The evolutionary history of the primates can be traced back 57-90 million years. One of the oldest known primate-like mammal species, Plesiadapis, came from North America; another, Archicebus, came from China. Other similar basal primates were widespread in Eurasia and Africa during the tropical conditions of the Paleocene and Eocene. Purgatorius is the genus of the four extinct species believed to be the earliest example of a primate or a proto-primate, a primatomorph precursor to the Plesiadapiformes, dating to as old as 66 million years ago.

<span class="mw-page-title-main">Congenital red–green color blindness</span> Most common genetic condition leading to color blindness

Congenital red–green color blindness is an inherited condition that is the root cause of the majority of cases of color blindness. It has no significant symptoms aside from its minor to moderate effect on color vision. It is caused by variation in the functionality of the red and/or green opsin proteins, which are the photosensitive pigment in the cone cells of the retina, which mediate color vision. Males are more likely to inherit red–green color blindness than females, because the genes for the relevant opsins are on the X chromosome. Screening for congenital red–green color blindness is typically performed with the Ishihara or similar color vision test. There is no cure for color blindness.

<span class="mw-page-title-main">Vertebrate visual opsin</span>

Vertebrate visual opsins are a subclass of ciliary opsins and mediate vision in vertebrates. They include the opsins in human rod and cone cells. They are often abbreviated to opsin, as they were the first opsins discovered and are still the most widely studied opsins.

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  18. 1 2 Sumner, P. (2000). "Catarrhine photopigments are optimized for detecting targets against a foliage background". Journal of Experimental Biology. 203 (Pt 13): 1963–86. doi: 10.1242/jeb.203.13.1963 . PMID   10851115.
  19. ↑ Carvalho, Livia S.; Pessoa, Daniel M. A.; Mountford, Jessica K.; Davies, Wayne I. L.; Hunt, David M. (2017). "The Genetic and Evolutionary Drives behind Primate Color Vision". Frontiers in Ecology and Evolution. 5: 34. doi: 10.3389/fevo.2017.00034 . ISSN   2296-701X.
  20. ↑ Bompas, Aline; Kendall, Grace; Sumner, Petroc (2013-04-01). "Spotting Fruit versus Picking Fruit as the Selective Advantage of Human Colour Vision". i-Perception. 4 (2): 84–94. doi:10.1068/i0564. ISSN   2041-6695. PMC   3677335 . PMID   23755352.
  21. ↑ Párraga, C. A. (2002). "Spatiochromatic properties of natural images and human vision". Current Biology. 12 (6): 483–487. doi: 10.1016/s0960-9822(02)00718-2 . PMID   11909534. S2CID   6442059.
  22. 1 2 3 Dominy, N. J., Svenning, J., and W. Li (2003). "Historical contingency in the evolution of primate color vision". Journal of Human Evolution. 44 (1): 25–45. doi:10.1016/S0047-2484(02)00167-7. PMID   12604302.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  23. ↑ Dominy, N. J.; Lucas, P. W. (2001-03-15). "Ecological importance of trichromatic vision to primates". Nature. 410 (6826): 363–366. Bibcode:2001Natur.410..363D. doi:10.1038/35066567. ISSN   0028-0836. PMID   11268211. S2CID   205015005.
  24. ↑ Gilad, Y. (2004). "Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates". PLOS Biology. 2 (1): e5. doi: 10.1371/journal.pbio.0020005 . PMC   314465 . PMID   14737185.
  25. ↑ Gilad, Y. (2007). "Correction: Loss of Olfactory Receptor Genes Coincides with the Acquisition of Full Trichromatic Vision in Primates". PLOS Biology. 5 (6): e148. doi: 10.1371/journal.pbio.0050148 . PMC   1892826 .
  26. ↑ Nei, Masatoshi; Niimura, Yoshihito; Nozawa, Masafumi (2008). "The evolution of animal chemosensory receptor gene repertoires: Roles of chance and necessity". Nature Reviews Genetics. 9 (12): 951–963. doi:10.1038/nrg2480. PMID   19002141. S2CID   11135361.
  27. ↑ Webb, D. M. (2004). "Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys". Molecular Biology and Evolution. 21 (4): 697–704. doi: 10.1093/molbev/msh068 . PMID   14963105.
  28. 1 2 Changizi, M. (2006). "Bare skin, blood and the evolution of primate colour vision". Biology Letters. 2 (2): 217–221. doi:10.1098/rsbl.2006.0440. PMC   1618887 . PMID   17148366.
  29. ↑ Campbell JL, Spalding AJ, Mir FA (2004). "The description of physical signs of illness in photographs by doctors with abnormal colour vision". Clin Exp Optom. 87 (4–5): 334–338. doi:10.1111/j.1444-0938.2004.tb05063.x. PMID   15312036. S2CID   43828781.
  30. ↑ Robert W. Sussman (2003). Primate Ecology and Social Structure, Volume 2: New World Monkeys (Revised First ed.). Boston, MA: Pearson Custom Publ. p. 133. ISBN   978-0-536-74364-0.
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