Evolution of color vision in primates

The evolution of color vision in primates is unique compared to most eutherian mammals. While our remote vertebrate ancestors possessed trichromacy, our nocturnal, warm-blooded, mammalian ancestors lost one of three cones in the retina at the time of dinosaurs. Fish, reptiles and birds are therefore trichromatic while all mammals, with the exception of some primates and marsupials, [cite journal | author=Arrese, C. A., "et al" | year=2005 | title=Cone topography and spectral sensitivity in two potentially trichromatic marsupials, the quokka (Setonix brachyurus) and quenda (Isoodon obesulus) | journal=Proc. Biol. Sci. | volume=272 | issue=1565 | page=791–796 | doi=10.1098/rspb.2004.3009] are strictly dichromats.

Primates achieve trichromacy through color receptors (cone cells), with spectral peaks in the violet (short wave, S), green (middle wave, M), and yellow-green (long wave, L) wavelengths. Not all primates, however, are capable of trichromacy. The catarrhines (Old World monkeys and apes) are routinely trichromatic, meaning that both males and females possess three opsins (pigments) sensitive to 430 nm, 530 nm, and 560 nm wavelengths.cite journal | author = Bowmaker, J. K., and S. Astell | year = 1991 | title = Photosensitive and photostable pigments in the retinae of Old World monkeys | journal = J Exp Biol. | volume = 156 | pages = 1–19] Platyrrhines (New World monkeys), on the other hand are non-routinely trichromatic; only a small population of platyrrhines are trichromats.cite journal | author = Surridge, A. K., and D. Osorio | year = 2003 | title = Evolution and selection of trichromatic vision in primates | journal = Trends in Ecol. and Evol. | volume = 18 | pages = 198-205]

Mechanism of color vision

There are underlying genetic differences between the catarrhines and platyrrhines that results in the former having routine trichromacy and the latter having non-routine trichromacy. Catarrhines have an S opsin encoded by an autosomal gene on chromosome 7. Their M and L opsins are encoded by adjacent genes on the X chromosome.cite journal | author = Nathans, J., and D Thomas | year = 1986 | title = Molecular genetics of human color vision: the genes encoding blue, green and red pigments | journal = Science | volume = 232 | pages = 193–203]

Platyrrhines share an S photopigment encoded by an autosomal gene with catarrhines, however; they have only a single X chromosome M/L opsin gene locus. The entire male platyrrhine population is dichromatic because it can only receive either the M or L photopigment in addition to their S photopigment. However, the X chromosome gene locus is polymorphic with two or three alleles, rendering some heterozygous platyrrhine females with trichromatic vision.cite journal | author = Lucas, P. W., and N. J. Dominy | year = 2003 | title = Evolution and function of routine trichromatic vision in primates | journal = Evolution | volume = 57 |pages = 2636-2643]

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.cite journal | author = Neitz, M., and J. Neitz | year = 1991 | title = Spectral tuning of pigments underlying red-green color vision | journal = Science | volume = 252 | pages = 971-974] There are two popular hypotheses that explain the evolution of the primate vision differences from this common origin.

Polymorphism

The first 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.cite journal | author = Hunt, D. M., and K. S. Dulai | year = 1998 | title = Molecular evolution of trichromacy in primates | journal = Vision Research | volume = 38 | pages = 3299-3306]

This hypothesis proposes that soon after the platyrrhine/catarrhine divergence, a heterozygous female led to male and female offspring with separate M and L opsins on the X-chromosome. 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 routine trichromacy arose early in primate evolution and was subsequently lost in some primate taxa. Use of the “molecular clocks” ideology, which is a technique geneticists use to determine an evolutionary sequence of events. It deduces elapsed time from a number of minor differences in DNA sequences. [cite journal |author=Hillis, D. M. |year=1996 |title=Inferring complex phytogenies |journal=Nature |volume=383 |pages=130-131] 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%). Based on this data, some researchers believe that gene duplication preceded the polymorphism seen in extant New World primates. These scientists argue that New World primates could have lost or gained alleles based on selective pressures of the environment. They also propose 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.

Nucleotide sequencing

Nucleotide sequencing of New World and Old World primate species can offer clues as to which hypothesis is likely to be correct. Sequences for the marmoset and squirrel monkeys, two New World primate species, have been determined. The sequencing data of their L/M opsin gene demonstrates their level of interspecies sequence divergence.cite journal | author = Shyue, S. K., and D. Hewett-Emmett | year = 1995 | title = Adaptive evolution of color vision genes in higher primates | journal = Science | volume = 269 | pages = 1265-1267] The divergence for marmoset and squirrel monkeys is on the order of 2-4%, which is considerably smaller than the divergence for Old World primate genes (6.1%). Hence, the New World primate color vision alleles are likely to have arisen after Old World gene duplication.

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.cite book | author = Mollon, J. D., and O. Estevez | year = 1990 | title = The two subsystems of colour vision and their role in wavelength discrimination. Found in: Vision—Coding and Efficiency | publisher = Cambridge University Press | location = Cambridge, UK | pages = 119-131]

New World monkeys

These two conflicting forces (homogenization and polymorphism) suggest that a balancing selection for trichromacy is present in the form of heterozygote advantage. 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.cite journal | author = Osorio, D., and M. Vorobyev | year = 1996 | title = Colour vision as an adaptation to frugivory in primates | journal = Proc. R. Soc. Lond | volume = 263 | pages = 593-599] 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.cite journal | author = Tovee, M. J., and J. K. Bowmaker | year = 1991 | title = The relationship between cone pigments and behavioral sensitivity in a New World monkey ("Callithrix jacchus jacchus") | journal = Vision Res. | volume = 32 | pages = 867-878]

"Aotus" and "Alouatta"

There are two noteworthy genera within the New World primates that suggest how different environments, and of course, different selective pressures, can make routine-trichromacy or even a lack of color vision more advantageous than non-routine trichromacy. For example, the night monkeys ("Aotus") have lost their S photopigments and polymorphic M/L opsin gene. These nocturnal anthropoids cannot perceive color, however; it is likely this is an adaptation for night time frugivory and folivory discrimination. On the opposite spectrum, howler monkeys ("Alouatta") have reinvented routine trichromatism through a 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. Howler monkeys are perhaps the most folivorous of the New World monkeys. Fruits make up a relatively small portion of their diet [cite book|title=Primate Ecology and Social Structure, Volume 2: New World Monkeys|edition=Revised First Edition|author=Robert W. Sussman|page=133|year=2003|isbn=0-536-74364-9] , and the type of leaves they consume (young, nutritive, and digestible), are detectable only by a red-green signal. Field work exploring the dietary preferences of howler monkeys suggest that routine trichromacy was environmentally selected for.

References