Evolution of color vision in primates
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 dinosaurs. Most teleost fish, reptiles and birds are therefore tetrachromatic while all mammals, with the exception of some primates and marsupials, are strictly dichromats.
Primates achieve trichromacy through color photoreceptors (cone cells), 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 monkeys and apes) are routine trichromats, meaning both males and females possess three opsins (pigments) sensitive to 430 nm, 530 nm, and 560 nm wavelengths. In contrast, with the exception of Alouatta and Aotus, all platyrrhines (New World monkeys) 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 gene 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 alleles, rendering heterozygous platyrrhine females with trichromatic vision, and homozygous females with dichromatic vision.
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.
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. 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.
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. 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.
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. 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 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. 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, 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.
- Jacobs, G. H. (2009). "Evolution of colour vision in mammals". Phil. Trans. R. Soc. B 364 (1531): 2957–2967. doi:10.1098/rstb.2009.0039. PMC 2781854. PMID 19720656.
- Arrese, C. A. et al. (2005). "Cone topography and spectral sensitivity in two potentially trichromatic marsupials, the quokka (Setonix brachyurus) and quenda (Isoodon obesulus)". Proc. Biol. Sci. 272 (1565): 791–796. doi:10.1098/rspb.2004.3009. PMC 1599861. PMID 15888411.
- Bowmaker, J. K., and S. Astell (1991). "Photosensitive and photostable pigments in the retinae of Old World monkeys". J Exp Biol. 156: 1–19. PMID 2051127.
- Surridge, A. K., and D. Osorio (2003). "Evolution and selection of trichromatic vision in primates". Trends in Ecol. And Evol. 18 (4): 198–205. doi:10.1016/S0169-5347(03)00012-0.
- Nathans, J., and D Thomas (1986). "Molecular genetics of human color vision: the genes encoding blue, green and red pigments". Science 232 (4747): 193–203. doi:10.1126/science.2937147. PMID 2937147.
- Lucas, P. W., Dominy, N. J., Riba-Hernandez, P., Stoner, K. E., Yamashita, N., Loría-Calderón, E., Petersen-Pereira, W., Rojas-Durán, Salas-Pena, R., Solis-Madrigal, S,. Osorio, D., and B. W. Darvell (2003). "Evolution and function of routine trichromatic vision in primates". Evolution 57 (11): 2636–2643. doi:10.1554/03-168. PMID 14686538.
- Neitz, M., and J. Neitz (1991). "Spectral tuning of pigments underlying red-green color vision". Science 252 (5008): 971–974. doi:10.1126/science.1903559. PMID 1903559.
- Hunt, D. M., and K. S. Dulai (1998). "Molecular evolution of trichromacy in primates". Vision Research 38 (21): 3299–3306. doi:10.1016/S0042-6989(97)00443-4. PMID 9893841.
- Hillis, D. M. (1996). "Inferring complex phytogenies". Nature 383 (6596): 130–131. doi:10.1038/383130a0. PMID 8774876.
- Shyue, S. K. and D. Hewett-Emmett (1995). "Adaptive evolution of color vision genes in higher primates". Science 269 (5228): 1265–1267. doi:10.1126/science.7652574. PMID 7652574.
- Mollon, J. D., and O. Estevez (1990). The two subsystems of colour vision and their role in wavelength discrimination. Found in: Vision—Coding and Efficiency. Cambridge, UK: Cambridge University Press. pp. 119–131.
- Osorio, D., and M. Vorobyev (1996). "Colour vision as an adaptation to frugivory in primates". Proc. R. Soc. Lond 263 (1370): 593–599. doi:10.1098/rspb.1996.0089. PMID 8677259.
- Saito, A., A. Mikami, S. Kawamura, Y. Ueno, C. Hiramatsu, K. A. Widayati, B. Suryobroto (2005). "Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in nonhuman primates". American Journal of Primatology 67 (4): 425–436. doi:10.1002/ajp.20197. PMID 16342068.
- Tovee, M. J., and J. K. Bowmaker (1991). "The relationship between cone pigments and behavioral sensitivity in a New World monkey (Callithrix jacchus jacchus)". Vision Res. 32 (5): 867–878. doi:10.1016/0042-6989(92)90029-I. PMID 1604855.
- 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 0-536-74364-9.
- Dominy, N. J., Svenning, J., and W. Li (2003). "Historical contingency in the evolution of primate color vision". Journal of Human Evolution 44 (44): 25–45. doi:10.1016/S0047-2484(02)00167-7.