Evolution of color vision in primates

Baboon

The evolution of color vision in primates is unique 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 all mammals, with the exception of some primates and marsupials,[2] 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 short-, medium-, and long wavelengths.[3] In nearly all species of platyrrhines (New World monkeys) males and homozygotic females are dichromats, while heterozygotic females are trichromats, a condition known as allelic or polymorphic trichromacy. Among platyrrhines, the exceptions are Alouatta and Aotus, both of which are uniform (consistent) trichromats.[4][5]

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 for L and M opsin pigments.[6]

In contrast, platyrrhines have only a single, polymorphic X chromosome M/L opsin gene locus.[6] 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.[7]

Proximate Causation 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.[8] 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.[9]

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.[10][11] 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%).[9] 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.[12]

Ultimate Causation Hypotheses

Fruit Theory

This theory encompasses the idea that this trait became favorable in the increased ability to find ripe fruit against a mature leaf background. Research has found that the spectral separation between the L and the M cones is closely proportional to the optimal detection of fruit against foliage.[13] 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.[14]

While the “fruit theory” holds much data to support its reasoning,[13][14][15][16] recent research has gone on to disprove this theory. Studies have suggested that the cone pigments found in dichromats can actually distinguish the color differences between fruit and the foliage surrounding it. Furthermore, the survival benefits favoring the selection for this trait are not completely necessary as many trichromatic primates live in environments where fruits have similar color tones in relation to the surrounding foliage and yet studies have shown that these primates obtain the same proportion of fruit compared to their dichromatic relatives.

Young Leaf Theory

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][17] 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.[17]

Long-Distance Foliage Hypothesis

This hypothesis suggests that trichromacy has evolved to adapt to distinguishing objects from the background foliage in long distance viewing. This hypothesis is based upon the fact that there is a larger variety of background S/(L+M) and luminance values under long-distance viewing.[16]

Short-Distance Foliage Hypothesis

This hypothesis suggests that trichromacy has evolved to show higher sensitivity to low spatial frequencies. 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."[18]

Evolution of Olfactory Systems

The sense of smell may have been a contributing factor in selection of color vision. Studies suggest that the loss of olfactory receptor genes may coincide with the evolved trait of full trichromatic vision.[19] In other words, as sense of smell deteriorated, and thus the ability to identify the most vital nutritional sources, the necessity for advancement in other senses increased and the likelihood for trichromatic color vision mutations to remain selected for became higher. 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 shown that the concentration of olfactory receptors is directly related to color vision acquisition. Interestingly, 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.[20]

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.

Health of Offspring

Trichromacy may also be evolutionarily favorable in offspring health (and therefore increasing fitness) through mate choice. M and L cone pigments maximize sensitivities for discriminating blood oxygen saturation through skin reflectance.[21] Therefore, the formation of trichromatic color vision in certain primate species may have been beneficial in modulating health of others, thus increasing the likelihood for trichromatic color vision to dominate a specie’s phenotypes as the fitness of offspring increases with parental health.

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,[22] 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][17]

See also

References

  1. ↑ 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 2781854Freely accessible. PMID 19720656.
  2. ↑ Arrese, C. A.; Runham, P. B; 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 1599861Freely accessible. PMID 15888411.
  3. ↑ Weiner, Irving B. (2003). Handbook of Psychology, Biological Psychology. John Wiley & Sons. p. 64. ISBN 978-0-471-38403-8. Retrieved 19 January 2015. Some 90 species of catarrhine primates...
  4. 1 2 3 4 5 Surridge, A. K.; 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.
  5. ↑ Backhaus, Werner G. K.; Kliegl, Reinhold; Werner, John S. (1 January 1998). Color Vision: Perspectives from Different Disciplines. Walter de Gruyter. p. 89. ISBN 978-3-11-080698-4. Retrieved 19 January 2015.
  6. 1 2 3 Nathans, J.; 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.
  7. 1 2 3 4 5 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., 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.
  8. ↑ Neitz, M.; J. Neitz (1991). "Spectral tuning of pigments underlying red-green color vision". Science. 252 (5008): 971–974. doi:10.1126/science.1903559. PMID 1903559.
  9. 1 2 Hunt, D. M.; 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.
  10. ↑ Hillis, D. M. (1996). "Inferring complex phytogenies". Nature. 383 (6596): 130–131. doi:10.1038/383130a0. PMID 8774876.
  11. ↑ Shyue, S. K.; 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.
  12. ↑ Mollon, J. D.; 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.
  13. 1 2 Osorio, D. (1996). "Colour vision as an adaptation to frugivory in primates". Royal Society of London: Biological Sciences.
  14. 1 2 Regan, B. (1998). "Frugivory and colour vision in Alouatta seniculus, a trichromatic platyrrhine monkey". Vision Research. doi:10.1016/S0042-6989(97)00462-8.
  15. ↑ Allen, G. (1879). The colour-sense: Its origin and development: An essay in comparative psychology. Boston.
  16. 1 2 Sumner, P. (2000). "Catarrhine photopigments are optimized for detecting targets against a foliage background". Journal of Experimental Biology.
  17. 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 (44): 25–45. doi:10.1016/S0047-2484(02)00167-7.
  18. ↑ Párraga, C. A. (2002). "Spatiochromatic properties of natural images and human vision". Current Biology.
  19. ↑ Gilad, Y. (2004). "Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates". PLoS Biology.
  20. ↑ Webb, D. M. (2004). "Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys". Molecular Biology and Evolution.
  21. ↑ Changizi, M. (2006). "Bare skin, blood and the evolution of primate colour vision". Biology Letters.
  22. ↑ 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.

Further reading

Shozo Yokoyama; Jinyi Xing; Yang Liu; Davide Faggionato; Ahmet Altun; William T. Starmer (December 18, 2014). "Epistatic Adaptive Evolution of Human Color Vision". PLoS Genetics. 10 (12). doi:10.1371/journal.pgen.1004884. 

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