Polymorphism and Adaptation of Primate Colour Vision

  • Amanda D. Melin
  • Chihiro Hiramatsu
  • Linda M. Fedigan
  • Colleen M. Schaffner
  • Filippo Aureli
  • Shoji Kawamura
Chapter

Abstract

Opsins provide an excellent model system for studying evolutionary interconnections at genetic, phenotypic and behavioural levels. Primates have evolved a unique ability for trichromatic colour vision from a dichromatic mammalian ancestor. This was accomplished via allelic differentiation (e.g. most New World monkeys) or gene duplication (e.g. Old World primates) of the middle to long-wavelength sensitive (M/LWS) opsin gene. However, questions remain regarding the behavioural adaptations of primate trichromacy. Allelic differentiation of the M/LWS opsins results in extensive colour vision variability in New World monkeys, where trichromats and dichromats are found in the same breeding population, enabling us to directly compare visual performances among different colour vision phenotypes. Thus, New World monkeys can serve as an excellent model to understand and evaluate the adaptive significance of primate trichromacy in a behavioural context. In this chapter, we summarise recent findings on colour vision evolution in vertebrates, with special emphasis on primates, and introduce our genetic and behavioural study on primate colour vision polymorphism and adaptation.

Keywords

World Monkey Colour Vision Placental Mammal Spider Monkey 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.

Notes

Acknowledgments

Our study was supported by Grants-in-Aid for Scientific Research A 19207018 and 22247036 from the Japan Society for the Promotion of Science (JSPS) and Grants-in-Aid for Scientific Research on Priority Areas “Comparative Genomics” 20017008 and “Cellular Sensor” 21026007 from the Ministry of Education, Culture, Sports, Science and Technology of Japan to S.K; a Grant-in-Aid for JSPS Fellows (15-11926) to C.H.; post-graduate scholarships and grants from the Alberta Ingenuity Fund, the Natural Sciences and Engineering Research Council of Canada, the Leakey Foundation and the Animal Behavior Society to A.D.M; the Canada Research Chairs Program and a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to L.M.F.; the Leakey Foundation and the North of England Zoological Society to F.A.; the British Academy and the University of Chester small grants scheme to C.M.S.

References

  1. Allen G (1879) The color sense: its origin and development. Trubner & Co, LondonGoogle Scholar
  2. Arrese CA, Beazley LD, Neumeyer C (2006) Behavioural evidence for marsupial trichromacy. Curr Biol 16:R193–R194PubMedGoogle Scholar
  3. Arrese CA, Hart NS, Thomas N et al (2002) Trichromacy in Australian marsupials. Curr Biol 12:657–660PubMedGoogle Scholar
  4. Bowmaker JK (2008) Evolution of vertebrate visual pigments. Vision Res 48:2022–2041PubMedGoogle Scholar
  5. Buchanan-Smith H, Smith AC, Surridge AK et al (2005) The effect of sex and color vision status on prey capture by captive and wild tamarins (Saguinus spp). Am J Primatol 66:S49Google Scholar
  6. Caine NG (2002) Seeing red: consequences of individual differences in color vision in callitrichid primates. In: Miller LE (ed) Eat or be eaten. Cambridge University Press, Cambridge, pp 58–73Google Scholar
  7. Caine NG, Mundy NI (2000) Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc R Soc Lond B 267:439–444Google Scholar
  8. Caine NG, Osorio D, Mundy NI (2010) A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity. Biol Lett 6:36–38PubMedGoogle Scholar
  9. Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate colour vision. Biol Lett 2:217–221PubMedGoogle Scholar
  10. Chapman C, Russo SE (2007) Primate seed dispersal: linking behavioural ecology and forest community structure. In: Campbell CJ, Fuentes AF, MacKinnon KC et al (eds) Primates in perspective. Oxford University Press, Oxford, pp 510–525Google 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. Collin SP, Knight MA, Davies WL et al (2003) Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13:R864–R865PubMedGoogle Scholar
  13. Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer Associates, SunderlandGoogle Scholar
  14. Cowing JA, Arrese CA, Davies WL et al (2008) Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus). Proc R Soc B 275:1491–1499PubMedGoogle Scholar
  15. Cropp S, Boinski S, Li WH (2002) Allelic variation in the squirrel monkey X-linked color vision gene: biogeographical and behavioral correlates. J Mol Evol 54:734–745PubMedGoogle Scholar
  16. 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–R163PubMedGoogle Scholar
  17. Davies WL, Carvalho LS, Tay BH et al (2009a) Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res 19:415–426PubMedGoogle Scholar
  18. Davies WL, Collin SP, Hunt DM (2009b) Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. Mol Biol Evol 26:1803–1809PubMedGoogle Scholar
  19. Deeb SS, Lindsey DT, Hibiya Y et al (1992) Genotype-phenotype relationships in human red/green color-vision defects: molecular and psychophysical studies. Am J Hum Genet 51:687–700PubMedGoogle Scholar
  20. Deeb SS (2006) Genetics of variation in human color vision and the retinal cone mosaic. Curr Opin Genet Dev 16:301–307PubMedGoogle Scholar
  21. Dominy NJ, Lucas PW (2001) Ecological importance of trichromatic vision to primates. Nature 410:363–366PubMedGoogle Scholar
  22. Dominy NJ, Lucas PW, Osorio D et al (2001) The sensory ecology of primate food perception. Evol Anthropol 10:171–186Google Scholar
  23. 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
  24. Dulai KS, Bowmaker JK, Mollon JD et al (1994) Sequence divergence, polymorphism and evolution of the middle-wave and long-wave visual pigment genes of great apes and Old World monkeys. Vision Res 34:2483–2491PubMedGoogle Scholar
  25. Ebeling W, Natoli RC, Hemmi JM (2010) Diversity of color vision: not all Australian marsupials are trichromatic. PLoS ONE 5:e14231PubMedGoogle Scholar
  26. Ebrey T, Koutalos Y (2001) Vertebrate photoreceptors. Prog Retin Eye Res 20:49–94PubMedGoogle Scholar
  27. Endler JA (2006) Disruptive and cryptic coloration. Proc R Soc B 273:2425–2426PubMedGoogle Scholar
  28. Fernandez AA, Morris MR (2007) Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis. Am Nat 170:10–20PubMedGoogle Scholar
  29. Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic Press, San DiegoGoogle Scholar
  30. Gautier-Hion A, Duplantier J-M, Quris FF et al (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324–337Google Scholar
  31. Gullan P, Cranston P (2005) The insects: an outline of entomology. Blackwell Publishing, OxfordGoogle Scholar
  32. Heesy CP, Ross CF (2004) Mosaic evolution of activity pattern, diet and color vision in haplorhine primates. In: Ross CP, Kay RF (eds) Anthropoid origins: new visions. Kluwer Academic/Plenum Press, New York, pp 665–698Google Scholar
  33. Hendrickson A, Djajadi HR, Nakamura L et al (2000) Nocturnal tarsier retina has both short and long/medium-wavelength cones in an unusual topography. J Comp Neurol 424:718–730PubMedGoogle Scholar
  34. Hiramatsu C, Tsutsui T, Matsumoto Y et al (2005) Color-vision polymorphism in wild capuchins (Cebus capucinus) and spider monkeys (Ateles geoffroyi) in Costa Rica. Am J Primatol 67:447–461PubMedGoogle Scholar
  35. Hiramatsu C, Melin AD, Aureli F et al (2008) Importance of achromatic contrast in short-range fruit foraging of primates. PLoS ONE 3:e3356PubMedGoogle Scholar
  36. Hiramatsu C, Melin AD, Aureli F et al (2009) Interplay of olfaction and vision in fruit foraging of spider monkeys. Anim Behav 77:1421–1426Google Scholar
  37. 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 27:453–464PubMedGoogle Scholar
  38. Hiwatashi T, Mikami A, Katsumura T et al (2011) Gene conversion and purifying selection shape nucleotide variation in gibbon L/M opsin genes. BMC Evol Biol 11:312PubMedGoogle Scholar
  39. Hopson JA, Crompton AW (1969) Origin of mammals. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary biology. Appleton-Century-Crofts, New YorkGoogle Scholar
  40. Hunt DM, Carvalho LS, Cowing JA et al (2007) Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem Photobiol 83:303–310PubMedGoogle Scholar
  41. Ibbotson RE, Hunt DM, Bowmaker JK et al (1992) Sequence divergence and copy number of the middle- and long-wave photopigment genes in Old World monkeys. Proc R Soc Lond B 247:145–154Google Scholar
  42. Isbell LA (2009) The fruit, the tree and the serpent: why we see so well. Harvard University Press, BostonGoogle Scholar
  43. Jacobs GH, Deegan JF II, Neitz J et al (1993) Photopigments and color vision in the nocturnal monkey, Aotus. Vision Res 33:1773–1783PubMedGoogle Scholar
  44. Jacobs GH, Deegan JF II (2001) Photopigments and colour vision in New World monkeys from the family Atelidae. Proc R Soc Lond B 268:695–702Google Scholar
  45. Jacobs GH, Williams GA (2001) The prevalence of defective color vision in Old World monkeys and apes. Col Res Appl 26 (Suppl):S123–S127Google Scholar
  46. Jacobs GH, Deegan JF II, Tan Y et al (2002) Opsin gene and photopigment polymorphism in a prosimian primate. Vision Res 42:11–18PubMedGoogle Scholar
  47. Jacobs GH, Rowe MP (2004) Evolution of vertebrate colour vision. Clin Exp Optom 87:206–216PubMedGoogle Scholar
  48. Jacobs GH (2007) New World monkeys and color. Int J Primatol 28:729–759Google Scholar
  49. Jacobs GH (2008) Primate color vision: a comparative perspective. Vis Neurosci 25:619–633PubMedGoogle Scholar
  50. Jacobs GH, Nathans J (2009) The evolution of primate color vision. Sci Am 300:56–63PubMedGoogle Scholar
  51. Julliot C (1996) Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. Am J Primatol 40:261–282Google Scholar
  52. Kelber A, Roth LS (2006) Nocturnal colour vision—not as rare as we might think. J Exp Biol 209:781–788PubMedGoogle Scholar
  53. Leighton M (1993) Modeling dietary selectivity by Bornean orangutans: evidence for integration of multiple criteria in fruit selection. Int J Primatol 14:257–313Google Scholar
  54. Leonhardt SD, Tung J, Camden JB et al (2009) Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates. Behav Ecol 20:1–12Google Scholar
  55. Lev-Yadun S, Dafni A, Flaishman MA et al (2004) Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126–1130PubMedGoogle Scholar
  56. 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 69:139–154PubMedGoogle Scholar
  57. Lucas PW, Dominy NJ, Riba-Hernández P et al (2003) Evolution and function of routine trichromatic vision in primates. Evolution 57:2636–2643PubMedGoogle Scholar
  58. McConkey KR, Aldy F, Ario A et al (2002) Selection of fruit by gibbons (Hylobates muelleri X agilis) in the rain forests of Central Borneo. Int J Primatol 23:123–145Google Scholar
  59. McConkey KR, Ario A, Aldy F et al (2003) Influence of forest seasonality on gibbon food choice in the rain forests of Barito Ulu, Central Kalimantan. Int J Primatol 24:19–32Google Scholar
  60. 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 73:205–214Google Scholar
  61. 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 62:659–670Google Scholar
  62. Melin AD, Fedigan LM, Hiramatsu C et al (2009) Fig foraging by dichromatic and trichromatic Cebus capucinus in a tropical dry forest. Int J Primatol 30:753–775Google Scholar
  63. 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
  64. Melin AD, Moritz GL, Fosbury RAE et al (2012) Commentary: why aye-ayes see blue. Am J Primatol 74:185–192PubMedGoogle Scholar
  65. Miller L (2002) Eat or be eaten. Cambridge University Press, Cambridge, p 297Google Scholar
  66. 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 222:373–399PubMedGoogle Scholar
  67. Morgan MJ, Adam A, Mollon JD (1992) Dichromats detect colour-camouflaged objects that are not detected by trichromats. Proc R Soc Lond B 248:291–295Google Scholar
  68. Mullen KT (1985) The contrast sensitivity of human colour vision to red-green and blue-yellow chromatic gratings. J Physiol 359:381–400PubMedGoogle Scholar
  69. Nei M, Zhang J, Yokoyama S (1997) Color vision of ancestral organisms of higher primates. Mol Biol Evol 14:611–618PubMedGoogle Scholar
  70. Olendorf R, Rodd FH, Punzalan D et al (2006) Frequency-dependent survival in natural guppy populations. Nature 441:633–636PubMedGoogle Scholar
  71. Onishi A, Koike S, Ida M et al (1999) Dichromatism in macaque monkeys. Nature 402:139–140PubMedGoogle Scholar
  72. Onishi A, Koike S, Ida-Hosonuma M et al (2002) Variations in long- and middle-wavelength-sensitive opsin gene loci in crab-eating monkeys. Vision Res 42:281–292PubMedGoogle Scholar
  73. Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593–599Google Scholar
  74. Osorio D, Smith AC, Vorobyev M et al (2004) Detection of fruit and the selection of primate visual pigments for color vision. Am Nat 164:696–708Google Scholar
  75. Parraga CA, Troscianko T, Tolhurst DJ (2002) Spatiochromatic properties of natural images and human vision. Curr Biol 12:483–487PubMedGoogle Scholar
  76. Perini ES, Pessoa VF, Pessoa DM (2009) Detection of fruit by the Cerrado’s marmoset (Callithrix penicillata): modeling color signals for different background scenarios and ambient light intensities. J Exp Zool Part A 311:289–302Google Scholar
  77. Perry GH, Martin RD, Verrelli BC (2007) Signatures of functional constraint at aye–aye opsin genes: the potential of adaptive color vision in a nocturnal primate. Mol Biol Evol 24:1963–1970PubMedGoogle Scholar
  78. Pisani D, Mohun SM, Harris SR et al (2006) Molecular evidence for dim-light vision in the last common ancestor of the vertebrates. Curr Biol 16:R318–R319PubMedGoogle Scholar
  79. Pokorny J, Lutze M, Cao D et al (2008) The color of night: surface color categorization by color defective observers under dim illuminations. Vis Neurosci 25:475–480PubMedGoogle Scholar
  80. Punzalan D, Rodd FH, Hughes KA (2005) Perceptual processes and the maintenance of polymorphism through frequency-dependent predation. Evol Ecol 19:303–320Google Scholar
  81. Regan BC, Julliot C, Simmen B et al (2001) Fruits, foliage and the evolution of primate colour vision. Phil Trans R Soc B 356:229–283PubMedGoogle Scholar
  82. Riba-Hernández P, Stoner KE, Lucas PW (2005) Sugar concentration of fruits and their detection via color in the Central American spider monkey (Ateles geoffroyi). Am J Primatol 67:411–423PubMedGoogle Scholar
  83. Robinson SR (1994) Early vertebrate color vision. Nature 367:121Google Scholar
  84. Saito A, Mikami A, Kawamura S et al (2005) Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in nonhuman primates. Am J Primatol 67:425–436PubMedGoogle Scholar
  85. Smith AC, Buchanan-Smith HM, Surridge AK et al (2003) The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). J Exp Biol 206:3159–3165PubMedGoogle Scholar
  86. 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 26:337–355Google Scholar
  87. Sourd C, Gautier-hion A (1986) Fruit selection by a forest guenon. J Animal Ecol 55:235–244Google Scholar
  88. Sumner P, Mollon JD (2000a) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986PubMedGoogle Scholar
  89. Sumner P, Mollon JD (2000b) Chromaticity as a signal of ripeness in fruits taken by primates. J Exp Biol 203:1987–2000PubMedGoogle Scholar
  90. Sumner P, Mollon JD (2003) Colors of primate pelage and skin: objective assessment of conspicuousness. Am J Primatol 59:67–91PubMedGoogle Scholar
  91. Surridge AK, Mundy NI (2002) Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates. Mol Ecol 11:2157–2169PubMedGoogle Scholar
  92. Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198–205Google Scholar
  93. Surridge AK, Suarez SS, Buchanan-Smith HM et al (2005) Color vision pigment frequencies in wild tamarins (Saguinus spp). Am J Primatol 67:463–470PubMedGoogle Scholar
  94. Talebi MG, Pope TR, Vogel ER et al (2006) Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae). Mol Ecol 15:551–558PubMedGoogle Scholar
  95. Tamboia T, Cipollini M, Levey D (1996) An evaluation of vertebrate seed dispersal syndromes in four species of black nightshade (Solanum sect. Solanum). Oecologia 107:522–535Google Scholar
  96. Tan Y, Li WH (1999) Trichromatic vision in prosimians. Nature 402:36PubMedGoogle Scholar
  97. Tan Y, Yoder AD, Yamashita N et al (2005) Evidence from opsin genes rejects nocturnality in ancestral primates. Proc Natl Acad Sci USA 102:14712–14716PubMedGoogle Scholar
  98. Terao K, Mikami A, Saito A et al (2005) Identification of a protanomalous chimpanzee by molecular genetic and electroretinogram analyses. Vision Res 45:1225–1235PubMedGoogle Scholar
  99. Urbani B (2002) A field observation on color selection by New World sympatric primates, Pithecia pithecia and Alouatta seniculus. Primates 43:95–101PubMedGoogle Scholar
  100. Valenta K, Fedigan LM (2009) Effects of gut passage, feces, and seed handling on latency and rate of germination in seeds consumed by capuchins (Cebus capucinus). Am J Phys Anthropol 138:486–492PubMedGoogle Scholar
  101. Valenta K, Melin AD Protein limitation explains variation in primate colour vision phenotypes. In: Garcia (ed.), Zoology. InTech (in press)Google Scholar
  102. Veilleux CC, Bolnick DA (2009) Opsin gene polymorphism predicts trichromacy in a cathemeral lemur. Am J Primatol 71:86–90PubMedGoogle Scholar
  103. Verrelli BC, Lewis CM Jr, Stone AC et al (2008) Different selective pressures shape the molecular evolution of color vision in chimpanzee and human populations. Mol Biol Evol 25:2735–2743PubMedGoogle Scholar
  104. Wakefield MJ, Anderson M, Chang E et al (2008) Cone visual pigments of monotremes: filling the phylogenetic gap. Vis Neurosci 25:257–264PubMedGoogle Scholar
  105. Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 136:790–809Google Scholar
  106. Yamashita N, Stoner KE, Riba-Hernández P et al (2005) Light levels used during feeding by primate species with different color vision phenotypes. Behav Ecol Sociobiol 58:618–629Google Scholar
  107. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Amanda D. Melin
    • 1
    • 6
  • Chihiro Hiramatsu
    • 2
  • Linda M. Fedigan
    • 1
  • Colleen M. Schaffner
    • 3
    • 4
  • Filippo Aureli
    • 4
    • 5
  • Shoji Kawamura
    • 2
  1. 1.Department of AnthropologyUniversity of CalgaryCalgaryCanada
  2. 2.Department of Integrated Biosciences, Graduate School of Frontier SciencesThe University of TokyoKashiwa, ChibaJapan
  3. 3.Psychology DepartmentUniversity of ChesterChesterUK
  4. 4.Instituto de NeuroetologiaUniversidad VeracruzanaXalapaMexico
  5. 5.Research Centre in Evolutionary Anthropology and PalaeoecologyLiverpool John Moores UniversityLiverpoolUK
  6. 6.Department of AnthropologyDartmouth CollegeHanoverUSA

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