Evolutionary Diversification of Visual Opsin Genes in Fish and Primates

Part of the Primatology Monographs book series (PrimMono)


Among vertebrates, fish and primates are highly polymorphic in their color vision. This diversity likely reflects the variability in light environments inhabited by these species. Gene duplications and allelic differentiation of opsin genes play an important role in the evolution of color vision in fish and primates. Studies have shown that gene duplications of opsins have occurred repeatedly during fish evolution, often accompanied by differentiation of spectral sensitivity and ­spatiotemporal expression patterns in the retina, which possibly enabled different color sensitivities between upward and downward vision. Interestingly, a similar regulatory mechanism for the expression of duplicated opsin genes, in which a single regulatory region controls the array of duplicated opsin genes, has evolved independently in fish and primates. However, this regulatory mechanism has resulted in different consequences for fish and primates: different sights by visual angles in fish and trichromatic color vision in primates. New World monkeys have the single-copy but multiallelic M/LWS opsin gene and hence exhibit an extensive intraspecific polymorphism of color vision. Behavioral observations of New World monkeys in the wild have revealed surprising findings, including that dichromatic monkeys perform better catching camouflaged insects than their trichromatic group mates and that these dichromats can be as good as trichromats when foraging for fruits. Interdisciplinary studies that emphasize a study of genes and behaviors will continue to uncover surprising variations of color vision and promote our understanding of the adaptive significance of color vision in evolution.


Color Vision Spectral Type World Monkey Visual Pigment Opsin Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



I thank the Japan Society for the Promotion of Science (Grants-in-Aid for Scientific Research A 19207018 and 22247036) and the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grants-in-Aid for Scientific Research on Priority Areas “Comparative Genomics” 20017008 and “Cellular Sensor” 21026007) for funding.


  1. Ahnelt PK, Kolb H (2000) The mammalian photoreceptor mosaic-adaptive design. Prog Retin Eye Res 19:711–777PubMedCrossRefGoogle Scholar
  2. Allen G (1879) The color sense: its origin and development. Trubner & Co, LondonGoogle Scholar
  3. Archer S, Hope A, Partridge JC (1995) The molecular basis for the green-blue sensitivity shift in the rod visual pigments of the European eel. Proc R Soc Lond B 262:289–295CrossRefGoogle Scholar
  4. Asaoka Y, Mano H, Kojima D et al (2002) Pineal expression-promoting element (PIPE), a cis-acting element, directs pineal-specific gene expression in zebrafish. Proc Natl Acad Sci USA 99:15456–15461PubMedCrossRefGoogle Scholar
  5. Caine NG, Mundy NI (2000) Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc R Soc Lond B 267:439–444CrossRefGoogle Scholar
  6. Caine NG, Surridge AK, Mundy NI (2003) Dichromatic and trichromatic Callithrix geoffroyi differ in relative foraging ability for red-green color-camouflaged and non-camouflaged food. Int J Primatol 24:1163–1175CrossRefGoogle Scholar
  7. Carleton KL, Kocher TD (2001) Cone opsin genes of African cichlid fishes: tuning spectral sensitivity by differential gene expression. Mol Biol Evol 18:1540–1550PubMedCrossRefGoogle Scholar
  8. Carleton KL, Spady TC, Streelman JT et al (2008) Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biol 6:22PubMedCrossRefGoogle Scholar
  9. Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate color vision. Biol Lett 2:217–221PubMedCrossRefGoogle Scholar
  10. Cheng CL, Novales Flamarique I (2004) Opsin expression: new mechanism for modulating colour vision. Nature 428:279PubMedCrossRefGoogle Scholar
  11. Chinen A, Hamaoka T, Yamada Y et al (2003) Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663–675PubMedGoogle Scholar
  12. Chinen A, Matsumoto Y, Kawamura S (2005a) Reconstitution of ancestral green visual pigments of zebrafish and molecular mechanism of their spectral differentiation. Mol Biol Evol 22:1001–1010PubMedCrossRefGoogle Scholar
  13. Chinen A, Matsumoto Y, Kawamura S (2005b) Spectral differentiation of blue opsins between phylogenetically close but ecologically distant goldfish and zebrafish. J Biol Chem 280:9460–9466PubMedCrossRefGoogle Scholar
  14. Collin SP, Knight MA, Davies WL et al (2003) Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13:R864–R865PubMedCrossRefGoogle Scholar
  15. Davies WL, Carvalho LS, Cowing JA et al (2007) Visual pigments of the platypus: a novel route to mammalian colour vision. Curr Biol 17:R161–R163PubMedCrossRefGoogle Scholar
  16. Davies WL, Collin SP, Hunt DM (2009) Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. Mol Biol Evol 26:1803–1809PubMedCrossRefGoogle Scholar
  17. De Araujo MF, Lima EM, Pessoa VF (2006) Modeling dichromatic and trichromatic sensitivity to the color properties of fruits eaten by squirrel monkeys (Saimiri sciureus). Am J Primatol 68:1129–1137PubMedCrossRefGoogle Scholar
  18. Deeb SS (2006) Genetics of variation in human color vision and the retinal cone mosaic. Curr Opin Genet Dev 16:301–307PubMedCrossRefGoogle Scholar
  19. Dominy NJ (2004) Color as an indicator of food quality to anthropoid primates: ecological evidence and an evolutionary scenario. In: Ross C, Kay RF (eds) Anthropoid origins. Kluwer Academic, New York, pp 599–628Google Scholar
  20. Dominy NJ, Lucas PW (2001) Ecological importance of trichromatic vision to primates. Nature 410:363–366PubMedCrossRefGoogle Scholar
  21. Dominy NJ, Garber PA, Bicca-Marques JC et al (2003a) Do female tamarins use visual cues to detect fruit rewards more successfully than do males? Anim Behav 66:829–837CrossRefGoogle Scholar
  22. Dominy NJ, Svenning JC, Li WH (2003b) Historical contingency in the evolution of primate color vision. J Hum Evol 44:25–45PubMedCrossRefGoogle Scholar
  23. Ebrey T, Koutalos Y (2001) Vertebrate photoreceptors. Prog Retin Eye Res 20:49–94PubMedCrossRefGoogle Scholar
  24. Fernandez AA, Morris MR (2007) Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis. Am Nat 170:10–20PubMedCrossRefGoogle Scholar
  25. Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic, San DiegoGoogle Scholar
  26. Foster DH, Nascimento SM (1994) Relational colour constancy from invariant cone-excitation ratios. Proc R Soc Lond B 257:115–121CrossRefGoogle Scholar
  27. Goldsmith TH (1990) Optimization, constraint, and history in the evolution of eyes. Q Rev Biol 65:281–322PubMedCrossRefGoogle Scholar
  28. Govardovskii VI (1983) On the role of oil drops in colour vision. Vision Res 23:1739–1740PubMedCrossRefGoogle Scholar
  29. Hamaoka T, Takechi M, Chinen A et al (2002) Visualization of rod photoreceptor development using GFP-transgenic zebrafish. Genesis 34:215–220PubMedCrossRefGoogle Scholar
  30. Heesy CP, Ross CF, Demes B (2007) Oculomotor stability and the functions of the postorbital bar and septum. In: Ravosa MJ, Dagosto M (eds) Primate origins: adaptations and evolution. Springer, New York, pp 257–283CrossRefGoogle Scholar
  31. Hiramatsu C, Melin AD, Aureli F et al (2008) Importance of achromatic contrast in short-range fruit foraging of primates. PLoS One 3:e3356PubMedCrossRefGoogle Scholar
  32. Hiramatsu C, Melin AD, Aureli F et al (2009) Interplay of olfaction and vision in fruit foraging of spider monkeys. Anim Behav 77:1421–1426CrossRefGoogle Scholar
  33. Hiwatashi T, Okabe Y, Tsutsui T et al (2010) An explicit signature of balancing selection for color vision variation in New World monkeys. Mol Biol Evol 27:453–464Google Scholar
  34. Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev 68:413–471PubMedCrossRefGoogle Scholar
  35. Jacobs GH (1999) Vision and behavior in primates. In: Archer SN, Djamgoz MBA, Loew ER et al (eds) Adaptive mechanisms in the ecology of vision. Kluwer Academic, Dordrecht, pp 629–650CrossRefGoogle Scholar
  36. Jacobs GH, Nathans J (2009) The evolution of primate color vision. Sci Am 300:56–63PubMedCrossRefGoogle Scholar
  37. Jacobs GH, Williams GA, Cahill H et al (2007) Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 315:1723–1725PubMedCrossRefGoogle Scholar
  38. Kasahara M, Naruse K, Sasaki S et al (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447:714–719PubMedCrossRefGoogle Scholar
  39. Kawamura S, Takeshita K, Tsujimura T et al (2005) Evolutionarily conserved and divergent regulatory sequences in the fish rod opsin promoter. Comp Biochem Physiol B 141:391–399PubMedCrossRefGoogle Scholar
  40. Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision–behavioural tests and physiological concepts. Biol Rev 78:81–118PubMedCrossRefGoogle Scholar
  41. Kennedy BN, Vihtelic TS, Checkley L et al (2001) Isolation of a zebrafish rod opsin promoter to generate a transgenic zebrafish line expressing enhanced green fluorescent protein in rod photoreceptors. J Biol Chem 276:14037–14043PubMedGoogle Scholar
  42. Levine JS, MacNichol EF Jr (1982) Color vision in fishes. Sci Am 246:140–149CrossRefGoogle Scholar
  43. Lucas PW, Darvell BW, Lee PKD et al (1998) Colour cues for leaf food selection by long-tailed macaques (Macaca fascicularis) with a new suggestion for the evolution of trichromatic colour vision. Folia Primatol 69:139–154PubMedCrossRefGoogle Scholar
  44. Lucas PW, Dominy NJ, Riba-Hernandez P et al (2003) Evolution and function of routine trichromatic vision in primates. Evolution 57:2636–2643PubMedGoogle Scholar
  45. Luo W, Williams J, Smallwood PM et al (2004) Proximal and distal sequences control UV cone pigment gene expression in transgenic zebrafish. J Biol Chem 279:19286–19293PubMedCrossRefGoogle Scholar
  46. Lythgoe JN (1979) The ecology of vision. Oxford University Press, OxfordGoogle Scholar
  47. MacLeod DI, Boynton RM (1979) Chromaticity diagram showing cone excitation by stimuli of equal luminance. J Opt Soc Am 69:1183–1186PubMedCrossRefGoogle Scholar
  48. Martin PR (1998) Colour processing in the primate retina: recent progress. J Physiol 513(Pt 3):631–638PubMedCrossRefGoogle Scholar
  49. Matsumoto Y, Fukamachi S, Mitani H et al (2006) Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene 371:268–278PubMedCrossRefGoogle Scholar
  50. Maximov VV (2000) Environmental factors which may have led to the appearance of colour vision. Philos Trans R Soc Lond B 355:1239–1242CrossRefGoogle Scholar
  51. Melin AD, Fedigan LM, Hiramatsu C et al (2007) Effects of colour vision phenotype on insect capture by a free-ranging population of white-faced capuchins (Cebus capucinus). Anim Behav 73:205–214CrossRefGoogle Scholar
  52. Melin AD, Fedigan LM, Hiramatsu C et al (2008) Polymorphic color vision in white-faced capuchins (Cebus capucinus): is there foraging niche divergence among phenotypes? Behav Ecol Sociobiol 62:659–670CrossRefGoogle Scholar
  53. Melin AD, Fedigan LM, Young HC et al (2010) Can color vision variation explain sex differences in invertebrate foraging by capuchin monkeys? Curr Zool 56:300–312Google Scholar
  54. Mollon JD, Bowmaker JK, Jacobs GH (1984) Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proc R Soc Lond B 222:373–399PubMedCrossRefGoogle Scholar
  55. Morgan MJ, Adam A, Mollon JD (1992) Dichromats detect colour-camouflaged objects that are not detected by trichromats. Proc R Soc Lond B 248:291–295CrossRefGoogle Scholar
  56. Morley RJ (2000) Origin and evolution of tropical rain forests. Wiley, ChichesterGoogle Scholar
  57. Nathans J (1987) Molecular biology of visual pigments. Annu Rev Neurosci 10:163–194PubMedCrossRefGoogle Scholar
  58. Nathans J, Thomas D, Hogness DS (1986) Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232:193–202PubMedCrossRefGoogle Scholar
  59. Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593–599CrossRefGoogle Scholar
  60. Parry JW, Carleton KL, Spady T et al (2005) Mix and match color vision: tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Curr Biol 15:1734–1739PubMedCrossRefGoogle Scholar
  61. Pokorny J, Shevell SK, Smith VC (1991) Colour appearance and colour constancy. In: Cronly-Dillon JR (ed) Vision and visual dysfunction, vol 6. MacMillan, London, pp 43–61Google Scholar
  62. Regan BC, Julliot C, Simmen B et al (1998) Frugivory and colour vision in Alouatta seniculus, a trichromatic platyrrhine monkey. Vision Res 38:3321–3327PubMedCrossRefGoogle Scholar
  63. Regan BC, Julliot C, Simmen B et al (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R Soc Lond B 356:229–283CrossRefGoogle Scholar
  64. Riba-Hernandez P, Stoner KE, Osorio D (2004) Effect of polymorphic colour vision for fruit detection in the spider monkey Ateles geoffroyi, and its implications for the maintenance of polymorphic colour vision in platyrrhine monkeys. J Exp Biol 207:2465–2470PubMedCrossRefGoogle Scholar
  65. Robinson SR (1994) Early vertebrate color vision. Nature 367:121CrossRefGoogle Scholar
  66. Saito A, Kawamura S, Mikami A et al (2005a) Demonstration of a genotype–phenotype correlation in the polymorphic color vision of a non-callitrichine New World monkey, capuchin (Cebus apella). Am J Primatol 67:471–485PubMedCrossRefGoogle Scholar
  67. Saito A, Mikami A, Kawamura S et al (2005b) Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in nonhuman primates. Am J Primatol 67:425–436PubMedCrossRefGoogle Scholar
  68. Seehausen O, Terai Y, Magalhaes IS et al (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–626PubMedCrossRefGoogle Scholar
  69. Shi Y, Yokoyama S (2003) Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA 100:8308–8313PubMedCrossRefGoogle Scholar
  70. Smallwood PM, Wang Y, Nathans J (2002) Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes. Proc Natl Acad Sci USA 99:1008–1011PubMedCrossRefGoogle Scholar
  71. Smith AC, Buchanan-Smith HM, Surridge AK et al (2003a) Leaders of progressions in wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax), with emphasis on color vision and sex. Am J Primatol 61:145–157PubMedCrossRefGoogle Scholar
  72. Smith AC, Buchanan-Smith HM, Surridge AK et al (2003b) The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). J Exp Biol 206:3159–3165PubMedCrossRefGoogle Scholar
  73. Smith AC, Buchanan-Smith HM, Surridge AK et al (2005) Factors affecting group spread within wild mixed-species troops of saddleback and mustached tamarins. Int J Primatol 26:337–355CrossRefGoogle Scholar
  74. Spady TC, Parry JW, Robinson PR et al (2006) Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Mol Biol Evol 23:1538–1547PubMedCrossRefGoogle Scholar
  75. Stoner KE, Riba-Hernandez P, Lucas PW (2005) Comparative use of color vision for frugivory by sympatric species of platyrrhines. Am J Primatol 67:399–409PubMedCrossRefGoogle Scholar
  76. Sumner P, Mollon JD (2000) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986PubMedGoogle Scholar
  77. Sumner P, Mollon JD (2003) Colors of primate pelage and skin: objective assessment of conspicuousness. Am J Primatol 59:67–91PubMedCrossRefGoogle Scholar
  78. Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198–205CrossRefGoogle Scholar
  79. Takechi M, Kawamura S (2005) Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. J Exp Biol 208:1337–1345PubMedCrossRefGoogle Scholar
  80. Takechi M, Hamaoka T, Kawamura S (2003) Fluorescence visualization of ultraviolet-sensitive cone photoreceptor development in living zebrafish. FEBS Lett 553:90–94PubMedCrossRefGoogle Scholar
  81. Takechi M, Seno S, Kawamura S (2008) Identification of cis-acting elements repressing blue opsin expression in zebrafish UV cones and pineal cells. J Biol Chem 283:31625–31632PubMedCrossRefGoogle Scholar
  82. Tan Y, Li WH (1999) Trichromatic vision in prosimians. Nature 402:436CrossRefGoogle Scholar
  83. Terai Y, Mayer WE, Klein J et al (2002) The effect of selection on a long wavelength-sensitive (LWS) opsin gene of Lake Victoria cichlid fishes. Proc Natl Acad Sci USA 99:15501–15506PubMedCrossRefGoogle Scholar
  84. Terai Y, Seehausen O, Sasaki T et al (2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biol 4:2244–2251CrossRefGoogle Scholar
  85. Terborgh J (1986) Keystone plant resources in the tropical forest. In: Soule M (ed) Conservation biology: science of scarcity and diversity. Sinauer, Sunderland, pp 330–344Google Scholar
  86. Tsujimura T, Chinen A, Kawamura S (2007) Identification of a locus control region for quadruplicated green-sensitive opsin genes in zebrafish. Proc Natl Acad Sci USA 104:12813–12818PubMedCrossRefGoogle Scholar
  87. Vogel ER, Neitz M, Dominy NJ (2007) Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus. Behav Ecol 18:292–297CrossRefGoogle Scholar
  88. Vorobyev M (2004) Ecology and evolution of primate colour vision. Clin Exp Optom 87:230–238PubMedCrossRefGoogle Scholar
  89. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, Bloomfield HillsCrossRefGoogle Scholar
  90. Wang Y, Macke JP, Merbs SL et al (1992) A locus control region adjacent to the human red and green visual pigment genes. Neuron 9:429–440PubMedCrossRefGoogle Scholar
  91. Westerfield M (1995) The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, EugeneGoogle Scholar
  92. Wittbrodt J, Shima A, Schartl M (2002) Medaka – a model organism from the far East. Nat Rev Genet 3:53–64PubMedCrossRefGoogle Scholar
  93. Yamada ES, Marshak DW, Silveira LC et al (1998) Morphology of P and M retinal ganglion cells of the bush baby. Vision Res 38:3345–3352PubMedCrossRefGoogle Scholar
  94. Yokoyama S (1997) Molecular genetic basis of adaptive selection: examples from color vision in vertebrates. Annu Rev Genet 31:315–336PubMedCrossRefGoogle Scholar
  95. Yokoyama S (2000a) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419PubMedCrossRefGoogle Scholar
  96. Yokoyama S (2000b) Phylogenetic analysis and experimental approaches to study color vision in vertebrates. Methods Enzymol 315:312–325PubMedCrossRefGoogle Scholar
  97. Yokoyama S, Radlwimmer FB, Blow NS (2000) Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change. Proc Natl Acad Sci USA 97:7366–7371PubMedCrossRefGoogle Scholar
  98. Yokoyama S, Yang H, Starmer WT (2008) Molecular basis of spectral tuning in the red- and green-sensitive (M/LWS) pigments in vertebrates. Genetics 179:2037–2043PubMedCrossRefGoogle Scholar
  99. Zhang H, Futami K, Horie N et al (2000) Molecular cloning of fresh water and deep-sea rod opsin genes from Japanese eel Anguilla japonica and expressional analyses during sexual maturation. FEBS Lett 469:39–43PubMedCrossRefGoogle Scholar

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© Springer 2011

Authors and Affiliations

  1. 1.Department of Integrated BiosciencesGraduate School of Frontier Sciences, The University of TokyoKashiwaJapan

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