Evolution of color vision in primates
Encyclopedia
The evolution of color vision
in primates is unique compared to most eutherian mammals. A remote vertebrate
ancestor of primates possessed tetrachromacy, but nocturnal, warm-blooded
, mammalian ancestors lost two of four cones in the retina
at the time of dinosaur
s. Most teleost fish, reptile
s and bird
s are therefore tetrachromatic while all mammals, with the exception of some primate
s and marsupial
s, are strictly dichromats.
Primates achieve trichromacy through color photoreceptors (cone cell
s), with spectral
peaks in the violet
(short wave, S), green
(middle wave, M), and yellow
-green (long wave, L) wavelengths. Opsin is the primary photopigment in primate eyes, and the sequence of an organism's opsin proteins determines the spectral sensitivity of its cone cells. Not all primates, however, are capable of trichromacy. The catarrhines (Old World monkey
s and ape
s) are routine trichromats, meaning both males and females possess three opsin
s (pigments) sensitive to 430 nm
, 530 nm, and 560 nm wavelengths. In contrast, with the exception of Alouatta
and Aotus
, all platyrrhines (New World monkey
s) are allelic or polymorphic trichromats.
on chromosome 7. Catarrhine primates have two adjacent opsin genes on the X chromosome
which code of L and M opsin pigments.
In contrast, platyrrhines have only a single, polymorphic X chromosome M/L opsin gene locus
. Therefore, every male platyrrhine is dichromatic because it can only receive either the M or L photopigment on its single X chromosome in addition to its S photopigment. However, the X chromosome gene locus is polymorphic
for M and L allele
s, rendering heterozygous platyrrhine females with trichromatic vision, and homozygous females with dichromatic vision.
This hypothesis proposes that this crossing over event occurred in a heterozygous catarrhine female sometime after the platyrrhine/catarrhine divergence. A genetic phenomenon known as X-inactivation permits each cone cell to express only an M or an L opsin (not both), which endowed the catarrhines with routine trichromacy.
s" technique to determine an evolutionary sequence of events. It deduces elapsed time from a number of minor differences in DNA sequences. 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%). Hence, the New World primate color vision alleles are likely to have arisen after Old World gene duplication. It is also proposed that the polymorphism in the opsin gene might have arisen independently through point mutation on one or more occasions, 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.
. Diurnal primates generally eat fruits and young leaves, and it has been argued that trichromatic color vision is an adaptation
for folivory
and frugivory
. Trichromacy is observed in nearly all New World primates, and can offer a selective advantage in the discrimination for the most nutritive, colorful items; behavioral studies have shown that trichromats are 50% more likely to detect fruits compared to dichromats. However, in dim light, trichromats have exhibited a slight disadvantage for discriminating fruit from foliage. In many situations, dichromats have a foraging advantage when food is camouflaged or similar in color to the background. Since almost all New World monkeys are known to search for food cooperatively, the entire group can benefit from the advantages of trichromacy and dichromacy.
s (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 monkey
s (Alouatta) have reinvented routine trichromacy through a relatively recent gene duplication
of the M/L gene. 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 reccurence 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, 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.
Color vision
Color vision is the capacity of an organism or machine to distinguish objects based on the wavelengths of the light they reflect, emit, or transmit...
in primates is unique compared to most eutherian mammals. A remote vertebrate
Vertebrate
Vertebrates are animals that are members of the subphylum Vertebrata . Vertebrates are the largest group of chordates, with currently about 58,000 species described. Vertebrates include the jawless fishes, bony fishes, sharks and rays, amphibians, reptiles, mammals, and birds...
ancestor of primates possessed tetrachromacy, but nocturnal, warm-blooded
Warm-blooded
The term warm-blooded is a colloquial term to describe animal species which have a relatively higher blood temperature, and maintain thermal homeostasis primarily through internal metabolic processes...
, mammalian ancestors lost two of four cones in the retina
Retina
The vertebrate retina is a light-sensitive tissue lining the inner surface of the eye. The optics of the eye create an image of the visual world on the retina, which serves much the same function as the film in a camera. Light striking the retina initiates a cascade of chemical and electrical...
at the time of dinosaur
Mesozoic
The Mesozoic era is an interval of geological time from about 250 million years ago to about 65 million years ago. It is often referred to as the age of reptiles because reptiles, namely dinosaurs, were the dominant terrestrial and marine vertebrates of the time...
s. Most teleost fish, reptile
Reptile
Reptiles are members of a class of air-breathing, ectothermic vertebrates which are characterized by laying shelled eggs , and having skin covered in scales and/or scutes. They are tetrapods, either having four limbs or being descended from four-limbed ancestors...
s and bird
Bird
Birds are feathered, winged, bipedal, endothermic , egg-laying, vertebrate animals. Around 10,000 living species and 188 families makes them the most speciose class of tetrapod vertebrates. They inhabit ecosystems across the globe, from the Arctic to the Antarctic. Extant birds range in size from...
s are therefore tetrachromatic while all mammals, with the exception of some primate
Primate
A primate is a mammal of the order Primates , which contains prosimians and simians. Primates arose from ancestors that lived in the trees of tropical forests; many primate characteristics represent adaptations to life in this challenging three-dimensional environment...
s and marsupial
Marsupial
Marsupials are an infraclass of mammals, characterized by giving birth to relatively undeveloped young. Close to 70% of the 334 extant species occur in Australia, New Guinea, and nearby islands, with the remaining 100 found in the Americas, primarily in South America, but with thirteen in Central...
s, are strictly dichromats.
Primates achieve trichromacy through color photoreceptors (cone cell
Cone cell
Cone cells, or cones, are photoreceptor cells in the retina of the eye that are responsible for color vision; they function best in relatively bright light, as opposed to rod cells that work better in dim light. If the retina is exposed to an intense visual stimulus, a negative afterimage will be...
s), with spectral
Visible spectrum
The visible spectrum is the portion of the electromagnetic spectrum that is visible to the human eye. Electromagnetic radiation in this range of wavelengths is called visible light or simply light. A typical human eye will respond to wavelengths from about 390 to 750 nm. In terms of...
peaks in the violet
Violet (color)
As the name of a color, violet is synonymous with a bluish purple, when the word "purple" is used in the common English language sense of any color between blue and red, not including either blue or red...
(short wave, S), green
Green
Green is a color, the perception of which is evoked by light having a spectrum dominated by energy with a wavelength of roughly 520–570 nanometres. In the subtractive color system, it is not a primary color, but is created out of a mixture of yellow and blue, or yellow and cyan; it is considered...
(middle wave, M), and yellow
Yellow
Yellow is the color evoked by light that stimulates both the L and M cone cells of the retina about equally, with no significant stimulation of the S cone cells. Light with a wavelength of 570–590 nm is yellow, as is light with a suitable mixture of red and green...
-green (long wave, L) wavelengths. Opsin is the primary photopigment in primate eyes, and the sequence of an organism's opsin proteins determines the spectral sensitivity of its cone cells. Not all primates, however, are capable of trichromacy. The catarrhines (Old World monkey
Old World monkey
The Old World monkeys or Cercopithecidae are a group of primates, falling in the superfamily Cercopithecoidea in the clade Catarrhini. The Old World monkeys are native to Africa and Asia today, inhabiting a range of environments from tropical rain forest to savanna, shrubland and mountainous...
s and ape
Ape
Apes are Old World anthropoid mammals, more specifically a clade of tailless catarrhine primates, belonging to the biological superfamily Hominoidea. The apes are native to Africa and South-east Asia, although in relatively recent times humans have spread all over the world...
s) are routine trichromats, meaning both males and females possess three opsin
Opsin
Opsins are a group of light-sensitive 35–55 kDa membrane-bound G protein-coupled receptors of the retinylidene protein family found in photoreceptor cells of the retina. Five classical groups of opsins are involved in vision, mediating the conversion of a photon of light into an electrochemical...
s (pigments) sensitive to 430 nm
Nanometre
A nanometre is a unit of length in the metric system, equal to one billionth of a metre. The name combines the SI prefix nano- with the parent unit name metre .The nanometre is often used to express dimensions on the atomic scale: the diameter...
, 530 nm, and 560 nm wavelengths. In contrast, with the exception of Alouatta
Howler monkey
Howler monkeys are among the largest of the New World monkeys. Fifteen species are currently recognised. Previously classified in the family Cebidae, they are now placed in the family Atelidae. These monkeys are native to South and Central American forests...
and Aotus
Night monkey
The night monkeys, also known as the owl monkeys or douroucoulis, are the members of the genus Aotus of New World monkeys . They are widely distributed in the forests of Central and South America, from Panama south to Paraguay and northern Argentina...
, all platyrrhines (New World monkey
New World monkey
New World monkeys are the five families of primates that are found in Central and South America: Callitrichidae, Cebidae, Aotidae, Pitheciidae, and Atelidae. The five families are ranked together as the Platyrrhini parvorder and the Ceboidea superfamily, which are essentially synonymous since...
s) are allelic or polymorphic trichromats.
Mechanism of color vision
Genetically, there are two ways for a primate to be a trichromat. All primates share an S opsin encoded by an autosomal geneAutosome
An autosome is a chromosome that is not a sex chromosome, or allosome; that is to say, there is an equal number of copies of the chromosome in males and females. For example, in humans, there are 22 pairs of autosomes. In addition to autosomes, there are sex chromosomes, to be specific: X and Y...
on chromosome 7. Catarrhine primates have two adjacent opsin genes on the X chromosome
X chromosome
The X chromosome is one of the two sex-determining chromosomes in many animal species, including mammals and is common in both males and females. It is a part of the XY sex-determination system and X0 sex-determination system...
which code of L and M opsin pigments.
In contrast, platyrrhines have only a single, polymorphic X chromosome M/L opsin gene locus
Locus (genetics)
In the fields of genetics and genetic computation, a locus is the specific location of a gene or DNA sequence on a chromosome. A variant of the DNA sequence at a given locus is called an allele. The ordered list of loci known for a particular genome is called a genetic map...
. Therefore, every male platyrrhine is dichromatic because it can only receive either the M or L photopigment on its single X chromosome in addition to its S photopigment. However, the X chromosome gene locus is polymorphic
Polymorphism (biology)
Polymorphism in biology occurs when two or more clearly different phenotypes exist in the same population of a species — in other words, the occurrence of more than one form or morph...
for M and L allele
Allele
An allele is one of two or more forms of a gene or a genetic locus . "Allel" is an abbreviation of allelomorph. Sometimes, different alleles can result in different observable phenotypic traits, such as different pigmentation...
s, rendering heterozygous platyrrhine females with trichromatic vision, and homozygous females with dichromatic vision.
Hypotheses
Some evolutionary biologists believe that the L and M photopigments of New World and Old World primates had a common evolutionary origin; molecular studies demonstrate that the spectral tuning (response of a photopigment to a specific wavelength of light) of the three pigments in both sub-orders is the same. 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. 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.This hypothesis proposes that this crossing over event occurred in a heterozygous catarrhine female sometime after the platyrrhine/catarrhine divergence. A genetic phenomenon known as X-inactivation permits each cone cell to express only an M or an L opsin (not both), which endowed the catarrhines with 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 M and L opsins diverged later by small changes in the gene sequences. Geneticists use the "molecular clockMolecular clock
The molecular clock is a technique in molecular evolution that uses fossil constraints and rates of molecular change to deduce the time in geologic history when two species or other taxa diverged. It is used to estimate the time of occurrence of events called speciation or radiation...
s" technique to determine an evolutionary sequence of events. It deduces elapsed time from a number of minor differences in DNA sequences. 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%). Hence, the New World primate color vision alleles are likely to have arisen after Old World gene duplication. It is also proposed that the polymorphism in the opsin gene might have arisen independently through point mutation on one or more occasions, 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
Amino acid
Amino acids are molecules containing an amine group, a carboxylic acid group and a side-chain that varies between different amino acids. The key elements of an amino acid are carbon, hydrogen, oxygen, and nitrogen...
that define these alleles have been maintained.
New World monkeys
These two conflicting forces (homogenization and polymorphism) suggest that a balancing selection for trichromacy is present in the form of heterozygote advantageHeterozygote advantage
A heterozygote advantage describes the case in which the heterozygote genotype has a higher relative fitness than either the homozygote dominant or homozygote recessive genotype. The specific case of heterozygote advantage is due to a single locus known as overdominance...
. Diurnal primates generally eat fruits and young leaves, and it has been argued that trichromatic color vision is an adaptation
Adaptation
An adaptation in biology is a trait with a current functional role in the life history of an organism that is maintained and evolved by means of natural selection. An adaptation refers to both the current state of being adapted and to the dynamic evolutionary process that leads to the adaptation....
for folivory
Folivore
In zoology, a folivore is a herbivore that specializes in eating leaves. Mature leaves contain a high proportion of hard-to-digest cellulose, less energy than other types of foods, and often toxic compounds. For this reason folivorous animals tend to have long digestive tracts and slow metabolisms....
and frugivory
Frugivore
A frugivore is a fruit eater. It can be any type of herbivore or omnivore where fruit is a preferred food type. Because approximately 20% of all mammalian herbivores also eat fruit, frugivory is considered to be common among mammals. Since frugivores eat a lot of fruit they are highly dependent...
. Trichromacy is observed in nearly all New World primates, and can offer a selective advantage in the discrimination for the most nutritive, colorful items; behavioral studies have shown that trichromats are 50% more likely to detect fruits compared to dichromats. However, in dim light, trichromats have exhibited a slight disadvantage for discriminating fruit from foliage. In many situations, dichromats have a foraging advantage when food is camouflaged or similar in color to the background. Since almost all New World monkeys are known to search for food cooperatively, the entire group can benefit from the advantages of trichromacy and dichromacy.
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. For example, the night monkeyNight monkey
The night monkeys, also known as the owl monkeys or douroucoulis, are the members of the genus Aotus of New World monkeys . They are widely distributed in the forests of Central and South America, from Panama south to Paraguay and northern Argentina...
s (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 monkey
Howler monkey
Howler monkeys are among the largest of the New World monkeys. Fifteen species are currently recognised. Previously classified in the family Cebidae, they are now placed in the family Atelidae. These monkeys are native to South and Central American forests...
s (Alouatta) have reinvented routine trichromacy through a relatively recent gene duplication
Gene duplication
Gene duplication is any duplication of a region of DNA that contains a gene; it may occur as an error in homologous recombination, a retrotransposition event, or duplication of an entire chromosome.The second copy of the gene is often free from selective pressure — that is, mutations of it have no...
of the M/L gene. 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 reccurence 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, 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.