Polymorphism and adaptation of primate colour vision

Evolutionary Biology: Mechanisms and Trends

Volumn , Issue , 2013, Pages 225-241

  Melin, Amanda D ^a,f   Hiramatsu, Chihiro ^b   Fedigan, Linda M ^a   Schaffner, Colleen M ^c,d   Aureli, Filippo ^d,e   Kawamura, Shoji ^g  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF CHESTER   (United Kingdom)

^d UNIVERSIDAD VERACRUZANA   (Mexico)

^e LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^f Dartmouth College   (United States)

^g KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893815643     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-30425-5_13     Document Type: Chapter

References (107)

1. Allen G. (1879). The color sense: its origin and development. Trubner & Co, London
2. Arrese CA, Beazley LD, Neumeyer C. (2006). Behavioural evidence for marsupial trichromacy. Curr Biol 16:R193-R194
3. Arrese CA, Hart NS, Thomas N et al. (2002). Trichromacy in Australian marsupials. Curr Biol 12:657-660
4. Bowmaker JK. (2008). Evolution of vertebrate visual pigments. Vision Res 48:2022-2041
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:S49
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 58-73
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 267:439-444
8. Caine NG, Osorio D, Mundy NI. (2010). A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity. Biol Lett 6:36-38
9. Changizi MA, Zhang Q, Shimojo S. (2006). Bare skin, blood and the evolution of primate colour vision. Biol Lett 2:217-221
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 510-525
11. Chinen A, Hamaoka T, Yamada Y et al. (2003). Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663-675
12. Collin SP, Knight MA, Davies WL et al. (2003). Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13:R864-R865
13. Conner JK, Hartl DL. (2004). A primer of ecological genetics. Sinauer Associates, Sunderland
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 275:1491-1499
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 54:734-745
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-R163
17. Davies WL, Carvalho LS, Tay BH et al. (2009). Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res 19:415-426
18. Davies WL, Collin SP, Hunt DM. (2009). Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. Mol Biol Evol 26:1803-1809
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: 687-700
20. Deeb SS. (2006). Genetics of variation in human color vision and the retinal cone mosaic. Curr Opin Genet Dev 16:301-307
21. Dominy NJ, Lucas PW. (2001). Ecological importance of trichromatic vision to primates. Nature 410:363-366
22. Dominy NJ, Lucas PW, Osorio D et al. (2001). The sensory ecology of primate food perception. Evol Anthropol 10:171-186
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 599-628
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 34:2483-2491
25. Ebeling W, Natoli RC, Hemmi JM. (2010). Diversity of color vision: not all Australian marsupials are trichromatic. PLoS ONE 5:e14231
26. Ebrey T, Koutalos Y. (2001). Vertebrate photoreceptors. Prog Retin Eye Res 20:49-94
27. Endler JA. (2006). Disruptive and cryptic coloration. Proc R Soc B 273:2425-2426
28. Fernandez AA, Morris MR. (2007). Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis. Am Nat 170:10-20
29. Fleagle JG. (1999). Primate adaptation and evolution, 2nd edn. Academic Press, San Diego
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 65:324-337
31. Gullan P, Cranston P. (2005). The insects: an outline of entomology. Blackwell Publishing, Oxford
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 665-698
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 424:718-730
34. Hiramatsu C, Tsutsui T, Matsumoto Y et al. (2005). Color-vision polymorphism in wild capuchins (Cebus capucinus) and spidermonkeys (Ateles geoffroyi) inCostaRica.AmJ Primatol 67:447-461
35. Hiramatsu C, Melin AD, Aureli F et al. (2008). Importance of achromatic contrast in short-range fruit foraging of primates. PLoS ONE 3:e3356
36. Hiramatsu C, Melin AD, Aureli F et al. (2009). Interplay of olfaction and vision in fruit foraging of spider monkeys. Anim Behav 77:1421-1426
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 27:453-464
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 11:312
39. Hopson JA, Crompton AW. (1969). Origin of mammals. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary biology. Appleton-Century-Crofts, New York
40. Hunt DM, Carvalho LS, Cowing JA et al. (2007). Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem Photobiol 83:303-310
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 247:145-154
42. Isbell LA. (2009). The fruit, the tree and the serpent: why we see so well. Harvard University Press, Boston
43. Jacobs GH, Deegan JF II, Neitz J et al. (1993). Photopigments and color vision in the nocturnal monkey, Aotus. Vision Res 33:1773-1783
44. Jacobs GH, Deegan JF II. (2001). Photopigments and colour vision in New World monkeys from the family Atelidae. Proc R Soc Lond B 268:695-702
45. Jacobs GH, Williams GA. (2001). The prevalence of defective color vision in Old World monkeys and apes. Col Res Appl 26 (Suppl):S123-S127
46. Jacobs GH, Deegan JF II, Tan Y et al. (2002). Opsin gene and photopigment polymorphism in a prosimian primate. Vision Res 42:11-18
47. Jacobs GH, Rowe MP. (2004). Evolution of vertebrate colour vision. Clin Exp Optom 87:206-216
48. Jacobs GH. (2007). New World monkeys and color. Int J Primatol 28:729-759
49. Jacobs GH. (2008). Primate color vision: a comparative perspective. Vis Neurosci 25:619-633
50. Jacobs GH, Nathans J. (2009). The evolution of primate color vision. Sci Am 300:56-63
51. Julliot C. (1996). Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. Am J Primatol 40:261-282
52. Kelber A, Roth LS. (2006). Nocturnal colour vision-not as rare as we might think. J Exp Biol 209:781-788
53. Leighton M. (1993). Modeling dietary selectivity by Bornean orangutans: evidence for integration of multiple criteria in fruit selection. Int J Primatol 14:257-313
54. Leonhardt SD, Tung J, Camden JB et al. (2009). Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates. Behav Ecol 20:1-12
55. Lev-Yadun S, Dafni A, Flaishman MA et al. (2004). Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126-1130
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 69:139-154
57. Lucas PW, Dominy NJ, Riba-Hernandez P et al. (2003). Evolution and function of routine trichromatic vision in primates. Evolution 57:2636-2643
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 23:123-145
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 24:19-32
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 73:205-214
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 62:659-670
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 30:753-775
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 56:300-312
64. Melin AD, Moritz GL, Fosbury RAE et al. (2012). Commentary: why aye-Ayes see blue. Am J Primatol 74:185-192
65. Miller L. (2002). Eat or be eaten. Cambridge University Press, Cambridge, p 297
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 222:373-399
67. Morgan MJ, Adam A, Mollon JD. (1992). Dichromats detect colour-camouflaged objects that are not detected by trichromats. Proc R Soc Lond B 248:291-295
68. Mullen KT. (1985). The contrast sensitivity of human colour vision to red-green and blue-yellow chromatic gratings. J Physiol 359:381-400
69. Nei M, Zhang J, Yokoyama S. (1997). Color vision of ancestral organisms of higher primates. Mol Biol Evol 14:611-618
70. Olendorf R, Rodd FH, Punzalan D et al. (2006). Frequency-dependent survival in natural guppy populations. Nature 441:633-636
71. Onishi A, Koike S, Ida M et al. (1999). Dichromatism in macaque monkeys. Nature 402:139-140
72. Onishi A, Koike S, Ida-Hosonuma M et al. (2002). Variations in long-And middle-wavelengthsensitive opsin gene loci in crab-eating monkeys. Vision Res 42:281-292
73. Osorio D, Vorobyev M. (1996). Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593-599
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 164:696-708
75. Parraga CA, Troscianko T, Tolhurst DJ. (2002). Spatiochromatic properties of natural images and human vision. Curr Biol 12:483-487
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 311:289-302
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 24:1963-1970
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-R319
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 25:475-480
80. Punzalan D, Rodd FH, Hughes KA. (2005). Perceptual processes and the maintenance of polymorphism through frequency-dependent predation. Evol Ecol 19:303-320
81. Regan BC, Julliot C, Simmen B et al. (2001). Fruits, foliage and the evolution of primate colour vision. Phil Trans R Soc B 356:229-283
82. Riba-Hernandez P, Stoner KE, LucasPW. (2005). Sugar concentration offruits and their detection via color in the Central American spider monkey (Ateles geoffroyi). Am J Primatol 67:411-423
83. Robinson SR. (1994). Early vertebrate color vision. Nature 367:121
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 67:425-436
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 206:3159-3165
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 26:337-355
87. Sourd C, Gautier-hion A. (1986). Fruit selection by a forest guenon. J Animal Ecol 55:235-244
88. Sumner P, Mollon JD. (2000). Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963-1986
89. Sumner P, Mollon JD. (2000). Chromaticity as a signal of ripeness in fruits taken by primates. J Exp Biol 203:1987-2000
90. Sumner P, Mollon JD. (2003). Colors of primate pelage and skin: objective assessment of conspicuousness. Am J Primatol 59:67-91
91. Surridge AK, Mundy NI. (2002). Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates. Mol Ecol 11:2157-2169
92. Surridge AK, Osorio D, Mundy NI. (2003). Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198-205
93. Surridge AK, Suarez SS, Buchanan-Smith HM et al. (2005). Color vision pigment frequencies in wild tamarins (Saguinus spp). Am J Primatol 67:463-470
94. Talebi MG, Pope TR, Vogel ER et al. (2006). Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae). Mol Ecol 15:551-558
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 107:522-535
96. Tan Y, Li WH. (1999). Trichromatic vision in prosimians. Nature 402:36
97. Tan Y, Yoder AD, Yamashita N et al. (2005). Evidence from opsin genes rejects nocturnality in ancestral primates. Proc Natl Acad Sci USA 102:14712-14716
98. Terao K, Mikami A, Saito A et al. (2005). Identification of a protanomalous chimpanzee by molecular genetic and electroretinogram analyses. Vision Res 45:1225-1235
99. Urbani B. (2002). A field observation on color selection by New World sympatric primates, Pithecia pithecia and Alouatta seniculus. Primates 43:95-101
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 138:486-492
101. Valenta K, Melin AD Protein limitation explains variation in primate colour vision phenotypes. In: Garcia (ed.), Zoology. InTech (in press)
102. Veilleux CC, Bolnick DA. (2009). Opsin gene polymorphism predicts trichromacy in a cathemeral lemur. Am J Primatol 71:86-90
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 25:2735-2743
104. Wakefield MJ, Anderson M, Chang E et al. (2008). Cone visual pigments of monotremes: filling the phylogenetic gap. Vis Neurosci 25:257-264
105. Willson MF, Whelan CJ. (1990). The evolution of fruit color in fleshy-fruited plants. Am Nat 136:790-809
106. Yamashita N, Stoner KE, Riba-Hernandez P et al. (2005). Light levels used during feeding by primate species with different color vision phenotypes. Behav Ecol Sociobiol 58:618-629
107. Yokoyama S. (2000). Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385-419