Colour Vision Genetics Learned from New World Monkeys in Santa Rosa, Costa Rica

  • Shoji KawamuraEmail author
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


By the mid-1980s, it was known that colour vision was polymorphic in New World monkeys due to allelic variation of the L/M opsin gene. However, until the early 2000s, it was unknown whether this polymorphism existed within social groups of wild monkeys, other than mixed-species troops of tamarins. In 2003, I embarked on a collaborative project with Linda Fedigan and colleagues in Santa Rosa National Park. We collected faecal samples from white-faced capuchin monkeys (Cebus capucinus) and black-handed spider monkeys (Ateles geoffroyi) that were individually identified by researchers. The major findings of our genetic studies were (1) the confirmation of the allelic polymorphism of the L/M opsin within social groups of each of the two species, (2) the discovery of a novel spectral tuning mechanism in ateline L/M alleles, (3) population genetic evidence for balancing selection on the L/M opsin alleles in the two species, (4) unequal allele frequencies of L/M opsins and (5) the discovery of hybrid L/M opsins in sympatric howler monkeys. Of equal importance has been the ecological side of our colour vision study. In this chapter I summarize basic knowledge on colour vision and visual opsin genes in primates and then describe the contribution of our studies in Santa Rosa to our understanding of primate colour vision evolution.


Colour vision Opsin Capuchin monkeys Spider monkeys Polymorphism 



I cannot express my gratitude with words to Professor Linda Marie Fedigan. I simply thank my luck that I encountered Linda during my search for a field primatologist collaborator in the early 2000s. Without her assistance, guidance and cooperation, my research would have taken a very different path and reached no better place. I also thank from the bottom of my heart the many friends and excellent collaborators who I got to know through Linda, especially Amanda Melin and Chihiro Hiramatsu, for making the research so productive. I also greatly appreciate excellent suggestions in revising the manuscript from anonymous reviewers and the editors, Dr. Urs Kalbitzer and Dr. Katharine Jack.


  1. Arrese CA, Hart NS, Thomas N et al (2002) Trichromacy in Australian marsupials. Curr Biol 12:657–660PubMedGoogle Scholar
  2. Balding DJ, Nichols RA, Hunt DM (1992) Detecting gene conversion: primate visual pigment genes. Proc R Soc B 249:275–280PubMedGoogle Scholar
  3. Boissinot S, Tan Y, Shyue SK et al (1998) Origins and antiquity of X-linked triallelic color vision systems in New World monkeys. Proc Natl Acad Sci U S A 95:13749–13754PubMedPubMedCentralGoogle Scholar
  4. Bosten JM, Robinson JD, Jordan G et al (2005) Multidimensional scaling reveals a color dimension unique to ‘color deficient’ observers. Curr Biol 15:R950–R952PubMedGoogle Scholar
  5. Bowmaker JK, Jacobs GH, Mollon JD (1987) Polymorphism of photopigments in the squirrel monkey: a sixth phenotype. Proc R Soc Lond B 231:383–390PubMedGoogle Scholar
  6. Carvalho LS, Davies WL, Robinson PR et al (2012) Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments. Proc R Soc B 279:387–393PubMedGoogle Scholar
  7. Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate colour vision. Biol Lett 2:217–221PubMedPubMedCentralGoogle Scholar
  8. 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
  9. Collin SP, Davies WL, Hart NS et al (2009) The evolution of early vertebrate photoreceptors. Phil Trans R Soc B 364:2925–2940PubMedGoogle Scholar
  10. Corso J, Bowler M, Heymann EW et al (2016) Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari (Cacajao calvus). Proc R Soc B 283:20160067PubMedGoogle Scholar
  11. Cropp S, Boinski S, Li W-H (2002) Allelic variation in the squirrel monkey X-linked color vision gene: biogeographical and behavioral correlates. J Mol Evol 54:734–745PubMedGoogle Scholar
  12. 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
  13. 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 19:415–426PubMedPubMedCentralGoogle Scholar
  14. 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
  15. Davies WI, Collin SP, Hunt DM (2012) Molecular ecology and adaptation of visual photopigments in craniates. Mol Ecol 21:3121–3158PubMedGoogle Scholar
  16. de Lima EM, Pessoa DM, Sena L et al (2015) Polymorphic color vision in captive Uta Hick’s cuxius, or bearded sakis (Chiropotes utahickae). Am J Primatol 77:66–75PubMedGoogle Scholar
  17. Deeb SS (2005) The molecular basis of variation in human color vision. Clin Genet 67:369–377PubMedGoogle Scholar
  18. Deeb SS (2006) Genetics of variation in human color vision and the retinal cone mosaic. Curr Opin Genet Dev 16:301–307PubMedGoogle Scholar
  19. Deeb SS, Jorgensen AL, Battisti L et al (1994) Sequence divergence of the red and green visual pigments in great apes and humans. Proc Natl Acad Sci U S A 91:7262–7266PubMedPubMedCentralGoogle Scholar
  20. Deegan JF II, Jacobs GH (1996) Spectral sensitivity and photopigments of a nocturnal prosimian, the bushbaby (Otolemur crassicaudatus). Am J Primatol 40:55–66Google Scholar
  21. Dominy NJ, Svenning JC, Li W-H (2003) Historical contingency in the evolution of primate color vision. J Hum Evol 44:25–45PubMedGoogle Scholar
  22. Drummond-Borg M, Deeb SS, Motulsky AG (1989) Molecular patterns of X chromosome-linked color vision genes among 134 men of European ancestry. Proc Natl Acad Sci U S A 86:983–987PubMedPubMedCentralGoogle Scholar
  23. 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. Vis Res 34:2483–2491PubMedGoogle Scholar
  24. Dulai KS, von Dornum M, Mollon JD et al (1999) The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome Res 9:629–638PubMedGoogle Scholar
  25. Ebeling W, Natoli RC, Hemmi JM (2010) Diversity of color vision: not all Australian marsupials are trichromatic. PLoS One 5:e14231PubMedPubMedCentralGoogle Scholar
  26. Fedigan LM, Melin AD, Addicott JF et al (2014) The heterozygote superiority hypothesis for polymorphic color vision is not supported by long-term fitness data from wild neotropical monkeys. PLoS One 9:e84872PubMedPubMedCentralGoogle Scholar
  27. 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
  28. Fleagle JG (2013) Primate adaptation and evolution, 3rd edn. Academic Press, San DiegoGoogle Scholar
  29. Hanazawa A, Mikami A, Sulistyo Angelika P et al (2001) Electroretinogram analysis of relative spectral sensitivity in genetically identified dichromatic macaques. Proc Natl Acad Sci U S A 98:8124–8127PubMedPubMedCentralGoogle Scholar
  30. Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associates, SunderlandGoogle Scholar
  31. Hayashi T, Motulsky AG, Deeb SS (1999) Position of a ‘green-red’ hybrid gene in the visual pigment array determines colour-vision phenotype. Nat Genet 22:90–93PubMedGoogle Scholar
  32. Hayashi S, Ueyama H, Tanabe S et al (2001) Number and variations of the red and green visual pigment genes in Japanese men with normal color vision. Jpn J Ophthalmol 45:60–67PubMedGoogle Scholar
  33. Hayashi T, Kubo A, Takeuchi T et al (2006) Novel form of a single X-linked visual pigment gene in a unique dichromatic color-vision defect. Vis Neurosci 23:411–417PubMedGoogle Scholar
  34. Heesy CP, Ross CF (2001) Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics. J Hum Evol 40:111–149PubMedGoogle Scholar
  35. 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 257–283Google Scholar
  36. Hiramatsu C, Radlwimmer FB, Yokoyama S et al (2004) Mutagenesis and reconstitution of middle-to-long-wave-sensitive visual pigments of New World monkeys for testing the tuning effect of residues at sites 229 and 233. Vis Res 44:2225–2231PubMedGoogle Scholar
  37. 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
  38. Hiramatsu C, Melin AD, Aureli F et al (2008) Importance of achromatic contrast in short-range fruit foraging of primates. PLoS One 3:e3356PubMedPubMedCentralGoogle Scholar
  39. 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
  40. Hiramatsu C, Melin AD, Allen WL et al (2017) Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals. Proc R Soc B 284:20162458Google Scholar
  41. 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
  42. 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 11:312PubMedPubMedCentralGoogle Scholar
  43. Hood SM, Mollon JD, Purves L et al (2006) Color discrimination in carriers of color deficiency. Vis Res 46:2894–2900PubMedGoogle Scholar
  44. 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
  45. Jacobs GH (1984) Within-species variations in visual capacity among squirrel monkeys (Saimiri sciureus): color vision. Vis Res 24:1267–1277PubMedGoogle Scholar
  46. Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev 68:413–471PubMedGoogle Scholar
  47. Jacobs GH (2007) New World monkeys and color. Int J Primatol 28:729–759Google Scholar
  48. Jacobs GH (2013) Losses of functional opsin genes, short-wavelength cone photopigments, and color vision-A significant trend in the evolution of mammalian vision. Vis Neurosci 30:39–53PubMedGoogle Scholar
  49. Jacobs GH, Deegan JF 2nd (2003) Photopigment polymorphism in prosimians and the origins of primate trichromacy. In: Mollon JD, Pokorny J, Knoblanch K (eds) Normal and defective colour vision. Oxford University Press, Oxford, pp 14–20Google Scholar
  50. 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
  51. Jacobs GH, Deegan JF II (2005) Polymorphic New World monkeys with more than three M/L cone types. J Opt Soc Am A 22:2072–2080Google Scholar
  52. Jacobs GH, Nathans J (2009) The evolution of primate color vision. Sci Am 300:56–63PubMedGoogle Scholar
  53. 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
  54. Jacobs GH, Deegan JF II, Neitz J et al (1993) Photopigments and color vision in the nocturnal monkey, Aotus. Vis Res 33:1773–1783PubMedGoogle Scholar
  55. Jacobs GH, Neitz M, Deegan JF et al (1996a) Trichromatic colour vision in New World monkeys. Nature 382:156–158PubMedGoogle Scholar
  56. Jacobs GH, Neitz M, Neitz J (1996b) Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proc R Soc Lond B 263:705–710Google Scholar
  57. Jacobs GH, Deegan JF II, Tan Y et al (2002) Opsin gene and photopigment polymorphism in a prosimian primate. Vis Res 42:11–18PubMedGoogle Scholar
  58. Jacobs RL, MacFie TS, Spriggs AN et al (2017) Novel opsin gene variation in large-bodied, diurnal lemurs. Biol Lett 13:20170050PubMedPubMedCentralGoogle Scholar
  59. Jameson KA, Highnote SM, Wasserman LM (2001) Richer color experience in observers with multiple photopigment opsin genes. Psychon Bull Rev 8:244–261PubMedGoogle Scholar
  60. Jorgensen AL, Deeb SS, Motulsky AG (1990) Molecular genetics of X chromosome-linked color vision among populations of African and Japanese ancestry: high frequency of a shortened red pigment gene among Afro-Americans. Proc Natl Acad Sci U S A 87:6512–6516PubMedPubMedCentralGoogle Scholar
  61. Kamilar JM, Heesy CP, Bradley BJ (2013) Did trichromatic color vision and red hair color coevolve in primates? Am J Primatol 75:740–751PubMedGoogle Scholar
  62. Kawamura S, Kubotera N (2004) Ancestral loss of short wave-sensitive cone visual pigment in lorisiform prosimians, contrasting with its strict conservation in other prosimians. J Mol Evol 58:314–321PubMedGoogle Scholar
  63. Kawamura S, Hiramatsu C, Melin AD et al (2012) Polymorphic color vision in primates: evolutionary considerations. In: Hirai H, Imai H, Go Y (eds) Post-genome biology of primates. Springer, Tokyo, pp 93–120Google Scholar
  64. Lambert D (1987) The Cambridge guide to prehistoric man. Cambridge University Press, CambridgeGoogle Scholar
  65. Levenson DH, Fernandez-Duque E, Evans S et al (2007) Mutational changes in S-cone opsin genes common to both nocturnal and cathemeral Aotus monkeys. Am J Primatol 69:757–765PubMedGoogle Scholar
  66. Matsumoto Y, Hiramatsu C, Matsushita Y et al (2014) Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys. Mol Ecol 23:1799–1812PubMedPubMedCentralGoogle Scholar
  67. Matsushita Y, Oota H, Welker BJ et al (2014) Color vision variation as evidenced by hybrid L/M opsin genes in wild populations of trichromatic Alouatta New World monkeys. Int J Primatol 35:71–87PubMedGoogle Scholar
  68. 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
  69. 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
  70. 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
  71. Melin AD, Moritz GL, Fosbury RAE et al (2012) Why aye-ayes see blue. Am J Primatol 74:185–192PubMedGoogle Scholar
  72. Melin AD, Kline DW, Hickey C et al (2013a) Food search through the eyes of a monkey: a functional substitution approach for assessing the ecology of primate color vision. Vis Res 87:87–96Google Scholar
  73. Melin AD, Matsushita Y, Moritz GL et al (2013b) Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates. Proc R Soc B 280:20130189PubMedGoogle Scholar
  74. Melin AD, Hiramatsu C, Parr NA et al (2014) The behavioral ecology of color vision: considering fruit conspicuity, detection distance and dietary importance. Int J Primatol 35:258–287Google Scholar
  75. Melin AD, Chiou KL, Walco ER et al (2017a) Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator). Proc Natl Acad Sci U S A 114:10402–10407PubMedPubMedCentralGoogle Scholar
  76. Melin AD, Khetpal V, Matsushita Y et al (2017b) Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory. Ecol Evol 7:1421–1434PubMedPubMedCentralGoogle Scholar
  77. 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
  78. 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
  79. Moritz GL, Ong PS, Perry GH et al (2017) Functional preservation and variation in the cone opsin genes of nocturnal tarsiers. Phil Trans R Soc B 372:20160075Google Scholar
  80. Nathans J, Thomas D, Hogness DS (1986) Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232:193–202PubMedGoogle Scholar
  81. Onishi A, Koike S, Ida M et al (1999) Dichromatism in macaque monkeys. Nature 402:139–140PubMedGoogle Scholar
  82. Onishi A, Koike S, Ida-Hosonuma M et al (2002) Variations in long- and middle-wavelength-sensitive opsin gene loci in crab-eating monkeys. Vis Res 42:281–292PubMedGoogle Scholar
  83. Osorio D, Smith AC, Vorobyev M et al (2004) Detection of fruit and the selection of primate visual pigments for color vision. Am Nat 164:696–708PubMedGoogle Scholar
  84. Pearce E, Dunbar R (2012) Latitudinal variation in light levels drives human visual system size. Biol Lett 8:90–93PubMedGoogle Scholar
  85. 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
  86. 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
  87. Reimchen TE (1987) Human color vision deficiencies and atmospheric twilight. Soc Biol 34:1–11PubMedGoogle Scholar
  88. Rowe MP, Jacobs GH (2004) Cone pigment polymorphism in New World monkeys: are all pigments created equal? Vis Neurosci 21:217–222PubMedGoogle Scholar
  89. Rowe MP, Jacobs GH (2007) Naturalistic color discriminations in polymorphic platyrrhine monkeys: effects of stimulus luminance and duration examined with functional substitution. Vis Neurosci 24:17–23PubMedGoogle Scholar
  90. Saito A, Mikami A, Hasegawa T et al (2003) Behavioral evidence of color vision deficiency in a protanomalia chimpanzee (Pan troglodytes). Primates 44:171–176PubMedGoogle Scholar
  91. 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 67:471–485PubMedGoogle Scholar
  92. 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 67:425–436PubMedGoogle Scholar
  93. Schneider H (2000) The current status of the New World monkey phylogeny. An Acad Bras Ci 72:165–172Google Scholar
  94. Sharpe LT, Stockman A, Jagle H et al (1999) Opsin genes, cone photopigments, color vision, and color blindness. In: Gegenfurtner KR, Sharpe LT (eds) Color vision: from genes to perception. Cambridge University Press, Cambridge, pp 3–51Google Scholar
  95. Sharpe LT, de Luca E, Hansen T et al (2006) Advantages and disadvantages of human dichromacy. J Vis 6:213–223PubMedGoogle Scholar
  96. Shyue SK, Li L, Chang BH et al (1994) Intronic gene conversion in the evolution of human X-linked color vision genes. Mol Biol Evol 11:548–551PubMedGoogle Scholar
  97. 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 61:145–157PubMedGoogle Scholar
  98. 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 206:3159–3165PubMedGoogle Scholar
  99. Soares JGM, Fiorani M, Araujo EA et al (2010) Cone photopigment variations in Cebus apella monkeys evidenced by electroretinogram measurements and genetic analysis. Vis Res 50:99–106PubMedGoogle Scholar
  100. 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
  101. Surridge AK, Smith AC, Buchanan-Smith HM et al (2002) Single-copy nuclear DNA sequences obtained from noninvasively collected primate feces. Am J Primatol 56:185–190PubMedGoogle Scholar
  102. Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198–205Google Scholar
  103. 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
  104. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  105. 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
  106. Tan Y, Li W-H (1999) Trichromatic vision in prosimians. Nature 402:36PubMedGoogle Scholar
  107. Tan Y, Yoder AD, Yamashita N et al (2005) Evidence from opsin genes rejects nocturnality in ancestral primates. Proc Natl Acad Sci U S A 102:14712–14716PubMedPubMedCentralGoogle Scholar
  108. Terao K, Mikami A, Saito A et al (2005) Identification of a protanomalous chimpanzee by molecular genetic and electroretinogram analyses. Vis Res 45:1225–1235PubMedGoogle Scholar
  109. Valenta K, Edwards M, Rafaliarison RR et al (2016) Visual ecology of true lemurs suggests a cathemeral origin for the primate cone opsin polymorphism. Funct Ecol 30:932–942Google Scholar
  110. Veilleux CC, Bolnick DA (2009) Opsin gene polymorphism predicts trichromacy in a cathemeral lemur. Am J Primatol 71:86–90PubMedGoogle Scholar
  111. Veilleux CC, Cummings ME (2012) Nocturnal light environments and species ecology: implications for nocturnal color vision in forests. J Exp Biol 215:4085–4096PubMedGoogle Scholar
  112. Veilleux CC, Louis EE Jr, Bolnick DA (2013) Nocturnal light environments influence color vision and signatures of selection on the OPN1SW opsin gene in nocturnal lemurs. Mol Biol Evol 30:1420–1437PubMedGoogle Scholar
  113. Veilleux CC, Scarry CJ, Di Fiore A et al (2016) Group benefit associated with polymorphic trichromacy in a Malagasy primate (Propithecus verreauxi). Sci Rep 6:38418PubMedPubMedCentralGoogle Scholar
  114. Verhulst S, Maes FW (1998) Scotopic vision in colour-blinds. Vis Res 38:3387–3390PubMedGoogle Scholar
  115. Verrelli BC, Tishkoff SA (2004) Signatures of selection and gene conversion associated with human color vision variation. Am J Hum Genet 75:363–375PubMedPubMedCentralGoogle Scholar
  116. 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 25:2735–2743PubMedPubMedCentralGoogle Scholar
  117. Vorobyev M (2004) Ecology and evolution of primate colour vision. Clin Exp Optom 87:230–238PubMedGoogle Scholar
  118. Wakefield MJ, Anderson M, Chang E et al (2008) Cone visual pigments of monotremes: filling the phylogenetic gap. Vis Neurosci 25:257–264PubMedGoogle Scholar
  119. Wikler KC, Rakic P (1990) Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. J Neurosci 10:3390–3401PubMedGoogle Scholar
  120. Wildman DE, Jameson NM, Opazo JC et al (2009) A fully resolved genus level phylogeny of neotropical primates (Platyrrhini). Mol Phylogenet Evol 53:694–702PubMedGoogle Scholar
  121. Winderickx J, Lindsey DT, Sanocki E et al (1992) Polymorphism in red photopigment underlies variation in colour matching. Nature 356:431–433PubMedGoogle Scholar
  122. Winderickx J, Battisti L, Hibiya Y et al (1993) Haplotype diversity in the human red and green opsin genes: evidence for frequent sequence exchange in exon 3. Hum Mol Genet 2:1413–1421PubMedGoogle Scholar
  123. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419PubMedGoogle Scholar
  124. Yokoyama S, Radlwimmer FB (1998) The “five-sites” rule and the evolution of red and green color vision in mammals. Mol Biol Evol 15:560–567PubMedGoogle Scholar
  125. Yokoyama S, Radlwimmer FB (1999) The molecular genetics of red and green color vision in mammals. Genetics 153:919–932PubMedPubMedCentralGoogle Scholar
  126. Yokoyama S, Radlwimmer FB (2001) The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 158:1697–1710PubMedPubMedCentralGoogle Scholar
  127. Yokoyama S, Yang H, Starmer WT (2008) Molecular basis of spectral tuning in the red- and green-sensitive (M/LWS) pigments in vertebrates. Genetics 179:2037–2043PubMedPubMedCentralGoogle Scholar
  128. Zhao Z, Hewett-Emmett D, Li W-H (1998) Frequent gene conversion between human red and green opsin genes. J Mol Evol 46:494–496PubMedGoogle Scholar
  129. Zhou YH, Li W-H (1996) Gene conversion and natural selection in the evolution of X-linked color vision genes in higher primates. Mol Biol Evol 13:780–783PubMedGoogle Scholar

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Authors and Affiliations

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

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