Abstract
Color provides a reliable cue for object detection and identification during various behaviors such as foraging, mate choice, predator avoidance, and navigation. The total number of colors that a visual system can discriminate is largely dependent on the number of different spectral types of cone opsins present in the retina and the spectral separations among them. Thus, opsins provide an excellent model system to study evolutionary interconnections at genetic, phenotypic, and behavioral levels. Primates have evolved a unique ability for three-dimensional color vision (trichromacy) from the two-dimensional color vision (dichromacy) present in the majority of other mammals. This development 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, or red–green) opsin gene. However, questions remain regarding the behavioral adaptations of primate trichromacy. Allelic differentiation of the M/LWS opsins results in extensive color 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 color vision phenotypes. Thus, New World monkeys can serve as an excellent model to understand and evaluate the adaptive significance of primate trichromacy in a behavioral context. In this chapter, we summarize recent findings on color vision evolution in primates and other vertebrates and introduce our genetic and behavioral study of vision–behavior interrelationships in free-ranging sympatric capuchin and spider monkey populations in Costa Rica.
Keywords
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- λmax :
-
Wavelength of maximal absorbance
- cDNA:
-
Complementary DNA
- ERG:
-
Electroretinogram
- LCR:
-
Locus control region
- M/LWS:
-
Middle to long wavelength-sensitive
- MSP:
-
Microspectrophotometry
- PCR:
-
Polymerase chain reaction
- RH1:
-
Rhodopsin
- RH2:
-
Rhodopsin-like
- SWS1:
-
Short wavelength-sensitive type 1
- SWS2:
-
Short wavelength-sensitive type 2
References
Ahnelt PK, Kolb H (2000) The mammalian photoreceptor mosaic-adaptive design. Prog Retin Eye Res 19:711–777
Allen G (1879) The color sense: its origin and development. Trubner, London
Araujo AC, Didonet JJ, Araujo CS et al (2008) Color vision in the black howler monkey (Alouatta caraya). Vis Neurosci 25:243–248
Aureli F, Schaffner CM (2008) Spider monkeys: social structure, social relationships and social interactions. In: Campbell C (ed) Spider monkeys: behavior ecology & evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 236–265
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 USA 95:13749–13754
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
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
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 24:1163–1175
Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate color vision. Biol Lett 2:217–221
Chapman CA (1990) Association patterns of spider monkeys: the influence of ecology and sex on social organization. Behav Ecol Sociobiol 26:409–414
Chinen A, Hamaoka T, Yamada Y et al (2003) Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663–675
Collin SP, Knight MA, Davies WL et al (2003) Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13:R864–R865
Collin SP, Davies WL, Hart NS et al (2009) The evolution of early vertebrate photoreceptors. Philos Trans R Soc B 364:2925–2940
Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer Associates, Sunderland
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
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
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 68:1129–1137
Deeb SS (2006) Genetics of variation in human color vision and the retinal cone mosaic. Curr Opin Genet Dev 16:301–307
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, New York, pp 599–628
Dominy NJ, Lucas PW (2001) Ecological importance of trichromatic vision to primates. Nature (Lond) 410:363–366
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 66:829–837
Dominy NJ, Svenning JC, Li WH (2003b) Historical contingency in the evolution of primate color vision. J Hum Evol 44:25–45
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 USA 86:983–987
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
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 9:629–638
Ebrey T, Koutalos Y (2001) Vertebrate photoreceptors. Prog Retin Eye Res 20:49–94
Fedigan LM (2003) Impact of male takeovers on infant deaths, births and conceptions in Cebus capucinus at Santa Rosa, Costa Rica. Int J Primatol 24:723–741
Fedigan LM, Jack K (2001) Neotropical primates in a regenerating Costa Rican dry forest: a comparison of howler and capuchin population patterns. Int J Primatol 22:689–713
Fedigan LM, Jack K (2004) The demographic and reproductive context of male replacements in Cebus capucinus. Behaviour 141:755–775
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
Fleagle JG (1999) Primate adaptation and evolution, 2dth edn. Academic, San Diego
Foster DH, Nascimento SM (1994) Relational colour constancy from invariant cone-excitation ratios. Proc R Soc Lond B 257:115–121
Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the genus Cebus. Cambridge University Press, Cambridge
Goldsmith TH (1990) Optimization, constraint, and history in the evolution of eyes. Q Rev Biol 65:281–322
Govardovskii VI (1983) On the role of oil drops in colour vision. Vision Res 23:1739–1740
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 USA 98:8124–8127
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 22:90–93
Heesy CP, Ross CF (2001) Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics. J Hum Evol 40:111–149
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 257–283
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. Vision Res 44:2225–2231
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 67:447–461
Hiramatsu C, Melin AD, Aureli F et al (2008) Importance of achromatic contrast in short-range fruit foraging of primates. PLoS One 3:e3356
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
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
Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159
Hunt DM, Dulai KS, Cowing JA et al (1998) Molecular evolution of trichromacy in primates. Vision Res 38:3299–3306
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
Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev 68:413–471
Jacobs GH (1996) Primate photopigments and primate color vision. Proc Natl Acad Sci USA 93:577–581
Jacobs GH (1998) A perspective on color vision in platyrrhine monkeys. Vision Res 38:3307–3313
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, Dordrecht, pp 629–650
Jacobs GH (2007) New World monkeys and color. Int J Primatol 28:729–759
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
Jacobs GH, Deegan JF II (2003) Cone pigment variations in four genera of new world monkeys. Vision Res 43:227–236
Jacobs GH, Deegan JF II (2005) Polymorphic New World monkeys with more than three M/L cone types. J Opt Soc Am A 22:2072–2080
Jacobs GH, Williams GA (2001) The prevalence of defective color vision in Old World monkeys and apes. Color Res Appl 26(suppl):S123–S127
Jacobs GH, Neitz M, Deegan JF et al (1996a) Trichromatic colour vision in New World monkeys. Nature (Lond) 382:156–158
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 263:705–710
Jacobs GH, Deegan JF II, Tan Y et al (2002) Opsin gene and photopigment polymorphism in a prosimian primate. Vision Res 42:11–18
Jacobs GH, Williams GA, Cahill H et al (2007) Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 315:1723–1725
Janzen DH (2002) Tropical dry forest: Area de Conservacion Guanacaste, northwestern Costa Rica. In: Perrow M, Davey A (eds) Handbook of ecological restoration: restoration in practice. Cambridge University Press, Cambridge, pp 559–583
Kawamura S, Kubotera N (2003) Absorption spectra of reconstituted visual pigments of a nocturnal prosimian, Otolemur crassicaudatus. Gene (Amst) 321:131–135
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 58:314–321
Kawamura S, Hirai M, Takenaka O et al (2001) Genomic and spectral analyses of long to middle wavelength-sensitive visual pigments of common marmoset (Callithrix jacchus). Gene (Amst) 269:45–51
Kawamura S, Takenaka N, Hiramatsu C et al (2002) Y-chromosomal red-green opsin genes of nocturnal New World monkey. FEBS Lett 530:70–72
Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision: behavioural tests and physiological concepts. Biol Rev 78:81–118
Levine JS, MacNichol EF Jr (1982) Color vision in fishes. Sci Am 246:140–149
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
Lucas PW, Dominy NJ, Riba-Hernández P et al (2003) Evolution and function of routine trichromatic vision in primates. Evolution 57:2636–2643
Lythgoe JN (1979) The ecology of vision. Oxford University Press, Oxford
MacLeod DI, Boynton RM (1979) Chromaticity diagram showing cone excitation by stimuli of equal luminance. J Opt Soc Am 69:1183–1186
Martin PR (1998) Colour processing in the primate retina: recent progress. J Physiol 513(pt 3):631–638
Maximov VV (2000) Environmental factors which may have led to the appearance of colour vision. Philos Trans R Soc B 355:1239–1242
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
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
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
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
Mollon JD (1989) “Tho’ she kneel’d in that place where they grew…” The uses and origins of primate colour vision. J Exp Biol 146:21–38
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
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
Morley RJ (2000) Origin and evolution of tropical rain forests. Wiley, Chichester
Mullen KT (1985) The contrast sensitivity of human colour vision to red-green and blue-yellow chromatic gratings. J Physiol 359:381–400
Nagao K, Takenaka N, Hirai M et al (2005) Coupling and decoupling of evolutionary mode between X- and Y-chromosomal red-green opsin genes in owl monkeys. Gene (Amst) 352:82–91
Nathans J (1987) Molecular biology of visual pigments. Annu Rev Neurosci 10:163–194
Nathans J, Thomas D, Hogness DS (1986) Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232:193–202
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Neitz M, Neitz J, Jacobs GH (1991) Spectral tuning of pigments underlying red-green color vision. Science 252:971–974
Onishi A, Koike S, Ida M et al (1999) Dichromatism in macaque monkeys. Nature (Lond) 402:139–140
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 42:281–292
Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593–599
Parraga CA, Troscianko T, Tolhurst DJ (2002) Spatiochromatic properties of natural images and human vision. Curr Biol 12:483–487
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
Pessoa DM, Araujo MF, Tomaz C et al (2003) Colour discrimination learning in black-handed tamarin (Saguinus midas niger). Primates 44:413–418
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 43–61
Regan BC, Julliot C, Simmen B et al (1998) Frugivory and colour vision in Alouatta seniculus, a trichromatic platyrrhine monkey. Vision Res 38:3321–3327
Regan BC, Julliot C, Simmen B et al (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R Soc B 356:229–283
Riba-Hernández 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 207:2465–2470
Robinson SR (1994) Early vertebrate color vision. Nature (Lond) 367:121
Saito A, Mikami A, Hasegawa T et al (2003) Behavioral evidence of color vision deficiency in a protanomalia chimpanzee (Pan troglodytes). Primates 44:171–176
Saito CA, da Silva Fiho M, Lee BB et al (2004) Alouatta trichromatic color vision: single-unit recording from retinal ganglion cells and microspectrophotometry. Invest Ophthalmol Vis Sci 45:E (abstract 4276)
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 67:471–485
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 67:425–436
Schneider H (2000) The current status of the New World monkey phylogeny. An Acad Bras Ci 72:165–172
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 3–51
Shyue SK, Hewett-Emmett D, Sperling HG et al (1995) Adaptive evolution of color vision genes in higher primates. Science 269:1265–1267
Shyue SK, Boissinot S, Schneider H et al (1998) Molecular genetics of spectral tuning in New World monkey color vision. J Mol Evol 46:697–702
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 99:1008–1011
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 61:145–157
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 206:3159–3165
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
Stoner KE, Riba-Hernández P, Lucas PW (2005) Comparative use of color vision for frugivory by sympatric species of platyrrhines. Am J Primatol 67:399–409
Sumner P, Mollon JD (2000) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986
Sumner P, Mollon JD (2003) Colors of primate pelage and skin: objective assessment of conspicuousness. Am J Primatol 59:67–91
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
Surridge AK, Smith AC, Buchanan-Smith HM et al (2002) Single-copy nuclear DNA sequences obtained from noninvasively collected primate feces. Am J Primatol 56:185–190
Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198–205
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Talebi MG, Pope TR, Vogel ER et al (2006) Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae). Mol Ecol 15:551–558
Tan Y, Li WH (1999) Trichromatic vision in prosimians. Nature (Lond) 402:36
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
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
Terborgh J (1986) Keystone plant resources in the tropical forest. In: Soule M (ed) Conservation biology: science of scarcity and diversity. Sinauer, Sunderland, pp 330–344
Veilleux CC, Bolnick DA (2009) Opsin gene polymorphism predicts trichromacy in a cathemeral lemur. Am J Primatol 71:86–90
Verrelli BC, Tishkoff SA (2004) Signatures of selection and gene conversion associated with human color vision variation. Am J Hum Genet 75:363–375
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
Vogel ER, Neitz M, Dominy NJ (2007) Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus. Behav Ecol 18:292–297
Vorobyev M (2004) Ecology and evolution of primate colour vision. Clin Exp Optom 87:230–238
Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, Bloomfield Hills
Wang Y, Macke JP, Merbs SL et al (1992) A locus control region adjacent to the human red and green visual pigment genes. Neuron 9:429–440
Wang Y, Smallwood PM, Cowan M et al (1999) Mutually exclusive expression of human red and green visual pigment-reporter transgenes occurs at high frequency in murine cone photoreceptors. Proc Natl Acad Sci USA 96:5251–5256
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276
Yamada ES, Marshak DW, Silveira LC et al (1998) Morphology of P and M retinal ganglion cells of the bush baby. Vision Res 38:3345–3352
Yokoyama S (2000a) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419
Yokoyama S (2000b) Phylogenetic analysis and experimental approaches to study color vision in vertebrates. Methods Enzymol 315:312–325
Yokoyama S, Radlwimmer FB (1998) The “five-sites” rule and the evolution of red and green color vision in mammals. Mol Biol Evol 15:560–567
Yokoyama S, Radlwimmer FB (1999) The molecular genetics of red and green color vision in mammals. Genetics 153:919–932
Yokoyama S, Radlwimmer FB (2001) The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 158:1697–1710
Yokoyama R, Yokoyama S (1990) Convergent evolution of the red- and green-like visual pigment genes in fish, Astyanax fasciatus, and human. Proc Natl Acad Sci USA 87:9315–9318
Yokoyama S, Yang H, Starmer WT (2008) Molecular basis of spectral tuning in the red- and green-sensitive (M/LWS) pigments in vertebrates. Genetics 179:2037–2043
Zhou YH, Li WH (1996) Gene conversion and natural selection in the evolution of X-linked color vision genes in higher primates. Mol Biol Evol 13:780–783
Acknowledgments
We thank R. Blanco Segura, M.M. Chavarria, and other staff of the Área de Conservación Guanacaste for local support, and we are grateful to the Ministerio de Ambiente y Energía (MINAE) of Costa Rica for giving us permission to conduct our field study in Santa Rosa. We appreciate the help of E. Murillo Chacon, C. Sendall, K.M. Jack, S. Carnegie, L. Rebecchini, A.H. Korstjens, G. McCabe, and H. Young with collection of fecal samples and behavioral data and assistance in the field. Our field 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.; postgraduate 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.; and the British Academy and the University of Chester small grants scheme to C.M.S.
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Kawamura, S., Hiramatsu, C., Melin, A.D., Schaffner, C.M., Aureli, F., Fedigan, L.M. (2012). Polymorphic Color Vision in Primates: Evolutionary Considerations. In: Hirai, H., Imai, H., Go, Y. (eds) Post-Genome Biology of Primates. Primatology Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54011-3_7
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