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Evolution of Genes for Color Vision and the Chemical Senses in Primates

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Evolution of the Human Genome I

Part of the book series: Evolutionary Studies ((EVOLUS))

Abstract

Primates are generally regarded as visually oriented mammals, trading a sense of smell for good sight. However, recent studies have questioned this simplistic view, and it is not well understood the extent to which senses have evolved interactively or in concert with each other in primates including humans. For example, the number of olfactory receptor genes is not as clearly differentiated between species with different color vision as once asserted. Among senses, receptors of stimuli for vision, olfaction, and bitter/sweet/umami tastes all belong to the G-protein-coupled receptor (GPCR) family, for which the genetic mechanism of signal perception is well understood. Thus, it is now possible to explore the evolutionary correlation among different senses in primates by studying these receptor groups for interspecies divergence, intraspecies diversity, and functional differences among variants. In this chapter, we review recent findings on these receptors and senses in humans and other primates and discuss the future directions of studies on their sensory evolution.

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References

  • Adipietro KA, Mainland JD, Matsunami H (2012) Functional evolution of mammalian odorant receptors. PLoS Genet 8:e1002821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adler E, Hoon MA, Mueller KL et al (2000) A novel family of mammalian taste receptors. Cell 100:693–702

    Article  CAS  PubMed  Google Scholar 

  • Araujo AC, Didonet JJ, Araujo CS et al (2008) Color vision in the black howler monkey (Alouatta caraya). Vis Neurosci 25:243–248

    Article  PubMed  Google Scholar 

  • Barton RA, Purvis A, Harvey PH (1995) Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Phil Trans R Soc B 348:381–392

    Article  CAS  PubMed  Google Scholar 

  • Bastir M, Rosas A, Gunz P et al (2011) Evolution of the base of the brain in highly encephalized human species. Nat Commun 2:588

    Article  PubMed  CAS  Google Scholar 

  • Bicca-Marques JC, Garber PA (2004) Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: a field experiment comparing Aotus, Callicebus, and Saguinus. Am J Primatol 62:171–187

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan TW, Tranel D, Adolphs R (2003) A specific role for the human amygdala in olfactory memory. Learn Mem 10:319–325

    Article  PubMed  PubMed Central  Google Scholar 

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  CAS  PubMed  Google Scholar 

  • Bullock TH (1982) Electroreception. Annu Rev Neurosci 5:121–170

    Article  CAS  PubMed  Google Scholar 

  • Bunce JA, Isbell LA, Grote MN et al (2011a) Color vision variation and foraging behavior in wild neotropical titi monkeys (Callicebus brunneus): possible mediating roles for spatial memory and reproductive status. Int J Primatol 32:1058–1075

    Article  Google Scholar 

  • Bunce JA, Isbell LA, Neitz M et al (2011b) Characterization of opsin gene alleles affecting color vision in a wild population of titi monkeys (Callicebus brunneus). Am J Primatol 73:189–196

    Article  CAS  PubMed  Google Scholar 

  • Bushdid C, Magnasco MO, Vosshall LB et al (2014) Humans can discriminate more than 1 trillion olfactory stimuli. Science 343:1370–1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Caine NG, Osorio D, Mundy NI (2010) A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity. Biol Lett 6:36–38

    Article  PubMed  Google Scholar 

  • Campbell MC, Ranciaro A, Froment A et al (2012) Evolution of functionally diverse alleles associated with PTC bitter taste sensitivity in Africa. Mol Biol Evol 29:1141–1153

    Article  CAS  PubMed  Google Scholar 

  • Carrigan MA, Uryasev O, Frye CB et al (2015) Hominids adapted to metabolize ethanol long before human-directed fermentation. Proc Natl Acad Sci USA 112:458–463

    Article  CAS  PubMed  Google Scholar 

  • Carvalho LS, Davies WL, Robinson PR et al (2012) Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments. Proc R Soc B 279:387–393

    Article  PubMed  Google Scholar 

  • Collin SP, Knight MA, Davies WL et al (2003) Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13:R864–R865

    Article  CAS  PubMed  Google Scholar 

  • 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 54:734–745

    Article  CAS  PubMed  Google Scholar 

  • Davies WI, Collin SP, Hunt DM (2012) Molecular ecology and adaptation of visual photopigments in craniates. Mol Ecol 21:3121–3158

    Article  CAS  PubMed  Google Scholar 

  • 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 77:66–75

    Article  PubMed  Google Scholar 

  • Deeb SS (2005) The molecular basis of variation in human color vision. Clin Genet 67:369–377

    Article  CAS  PubMed  Google Scholar 

  • Deeb SS (2006) Genetics of variation in human color vision and the retinal cone mosaic. Curr Opin Genet Dev 16:301–307

    Article  CAS  PubMed  Google Scholar 

  • DeMaria S, Ngai J (2010) The cell biology of smell. J Cell Biol 191:443–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dominy NJ, Lucas PW (2001) Ecological importance of trichromatic vision to primates. Nature 410:363–366

    Article  CAS  PubMed  Google Scholar 

  • Dominy NJ, Lucas PW, Osorio D et al (2001) The sensory ecology of primate food perception. Evol Anthropol 10:171–186

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dominy NJ, Svenning JC, Li W-H (2003b) Historical contingency in the evolution of primate color vision. J Hum Evol 44:25–45

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 34:2483–2491

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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:e84872

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Fleagle JG (2013) Primate adaptation and evolution, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Fortes-Marco L, Lanuza E, Martinez-Garcia F (2013) Of pheromones and kairomones: what receptors mediate innate emotional responses? Anat Rec 296:1346–1363

    Article  CAS  Google Scholar 

  • Garrett EC (2015) Was there a sensory trade-off in primate evolution? The vomeronasal groove as a means of understanding the vomeronasal system in the fossil record. The Graduate Center, City University of New York, New York

    Google Scholar 

  • Gelis L, Wolf S, Hatt H et al (2012) Prediction of a ligand-binding niche within a human olfactory receptor by combining site-directed mutagenesis with dynamic homology modeling. Angew Chem Int Ed 51:1274–1278

    Article  CAS  Google Scholar 

  • Gilad Y, Przeworski M, Lancet D (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol 2:e5

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilad Y, Wiebe V, Przeworski M et al (2007) Correction: loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates (vol 2, pg 120, 2004). PLoS Biol 5:e148

    Article  PubMed Central  Google Scholar 

  • Go Y, Niimura Y (2008) Similar numbers but different repertoires of olfactory receptor genes in humans and chimpanzees. Mol Biol Evol 25:1897–1907

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Hasin Y, Olender T, Khen M et al (2008) High-resolution copy-number variation map reflects human olfactory receptor diversity and evolution. PLoS Genet 4:e1000249

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hasin-Brumshtein Y, Lancet D, Olender T (2009) Human olfaction: from genomic variation to phenotypic diversity. Trends Genet 25:178–184

    Article  CAS  PubMed  Google Scholar 

  • Hayakawa T, Sugawara T, Go Y, Udono T, Hirai H, Imai H (2012) Eco-geographical diversification of bitter taste receptor genes (TAS2Rs) among subspecies of chimpanzees (Pan troglodytes). PLoS One 7:e43277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 45:60–67

    Article  CAS  PubMed  Google Scholar 

  • 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 23:411–417

    Article  PubMed  Google Scholar 

  • Hayden S, Bekaert M, Crider TA et al (2010) Ecological adaptation determines functional mammalian olfactory subgenomes. Genome Res 20:1–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Heritage S (2014) Modeling olfactory bulb evolution through primate phylogeny. PLoS One 9:e113904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heymann EW (2006) The neglected sense-olfaction in primate behavior, ecology, and evolution. Am J Primatol 68:519–524

    Article  PubMed  Google Scholar 

  • 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 44:2225–2231

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hiramatsu C, Melin AD, Aureli F et al (2008) Importance of achromatic contrast in short-range fruit foraging of primates. PLoS One 3:e3356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoon MA, Adler E, Lindemeier J et al (1999) Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96:541–551

    Article  CAS  PubMed  Google Scholar 

  • Hudson R (1999) From molecule to mind: the role of experience in shaping olfactory function. J Comp Physiol A 185:297–304

    Article  CAS  PubMed  Google Scholar 

  • Hughes GM, Teeling EC, Higgins DG (2014) Loss of olfactory receptor function in hominin evolution. PLoS One 9:e84714

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev 68:413–471

    Article  CAS  PubMed  Google Scholar 

  • Jacobs GH (2007) New World monkeys and color. Int J Primatol 28:729–759

    Article  Google Scholar 

  • 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 30:39–53

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jacobs GH, Nathans J (2009) The evolution of primate color vision. Sci Am 300:56–63

    Article  PubMed  Google Scholar 

  • Jacobs GH, Williams GA (2001) The prevalence of defective color vision in Old World monkeys and apes. Col Res Appl 26. (Suppl.):S123–S127

    Article  Google Scholar 

  • Jacobs GH, Neitz M, Deegan JF et al (1996) Trichromatic colour vision in New World monkeys. Nature 382:156–158

    Article  CAS  PubMed  Google Scholar 

  • Jameson KA, Highnote SM, Wasserman LM (2001) Richer color experience in observers with multiple photopigment opsin genes. Psychon Bull Rev 8:244–261

    Article  CAS  PubMed  Google Scholar 

  • Jiang P, Josue J, Li X et al (2012) Major taste loss in carnivorous mammals. Proc Natl Acad Sci USA 109:4956–4961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones G, Teeling EC, Rossiter SJ (2013) From the ultrasonic to the infrared: molecular evolution and the sensory biology of bats. Front Physiol 4:117

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamilar JM, Heesy CP, Bradley BJ (2013) Did trichromatic color vision and red hair color coevolve in primates? Am J Primatol 75:740–751

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 93–120

    Chapter  Google Scholar 

  • Keller A, Zhuang H, Chi Q et al (2007) Genetic variation in a human odorant receptor alters odour perception. Nature 449:468–472

    Article  CAS  PubMed  Google Scholar 

  • Kim UK, Wooding S, Riaz N et al (2006) Variation in the human TAS1R taste receptor genes. Chem Senses 31:599–611

    Article  CAS  PubMed  Google Scholar 

  • Klailova M, Lee PC (2014) Wild Western lowland gorillas signal selectively using odor. PLoS One 9:e99554

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuang S, Zhang T (2014) Smelling directions: olfaction modulates ambiguous visual motion perception. Sci Rep 4:5796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambert D (1987) The Cambridge guide to prehistoric man. Cambridge University Press, Cambridge

    Google Scholar 

  • Laska M, Seibt A, Weber A (2000) ‘Microsmatic’ primates revisited: olfactory sensitivity in the squirrel monkey. Chem Senses 25:47–53

    Article  CAS  PubMed  Google Scholar 

  • Laska M, Freist P, Krause S (2007) Which senses play a role in nonhuman primate food selection? A comparison between squirrel monkeys and spider monkeys. Am J Primatol 69:282–294

    Article  PubMed  Google Scholar 

  • 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 69:757–765

    Article  CAS  PubMed  Google Scholar 

  • Li X, Staszewski L, Xu H et al (2002) Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99:4692–4696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Garcia F, Martinez-Ricos J, Agustin-Pavon C et al (2009) Refining the dual olfactory hypothesis: pheromone reward and odour experience. Behav Brain Res 200:277–286

    Article  CAS  PubMed  Google Scholar 

  • Matsui A, Go Y, Niimura Y (2010) Degeneration of olfactory receptor gene repertories in primates: no direct link to full trichromatic vision. Mol Biol Evol 27:1192–1200

    Article  CAS  PubMed  Google Scholar 

  • 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 23:1799–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 35:71–87

    Article  PubMed  Google Scholar 

  • McRae JF, Jaeger SR, Bava CM et al (2013) Identification of regions associated with variation in sensitivity to food-related odors in the human genome. Curr Biol 23:1596–1600

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Melin AD, Moritz GL, Fosbury RAE et al (2012) Why aye-ayes see blue. Am J Primatol 74:185–192

    Article  PubMed  Google Scholar 

  • 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 87:87–96

    Article  Google Scholar 

  • 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 280:20130189

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 35:258–287

    Article  Google Scholar 

  • Menashe I, Abaffy T, Hasin Y et al (2007) Genetic elucidation of human hyperosmia to isovaleric acid. PLoS Biol 5:e284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meyerhof W, Batram C, Kuhn C et al (2010) The molecular receptive ranges of human TAS2R bitter taste receptors. Chem Senses 35:157–170

    Article  CAS  PubMed  Google Scholar 

  • Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278

    Article  CAS  PubMed  Google Scholar 

  • Muniz JAPC, de Athaide LM, Gomes BD et al (2014) Ganglion cell and displaced amacrine cell density distribution in the retina of the howler monkey (Alouatta caraya). PLoS One 9:e115291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nathans J, Hogness DS (1983) Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell 34:807–814

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9:951–963

    Article  CAS  PubMed  Google Scholar 

  • Neville KR, Haberly LB (2004) Olfactory cortex. In: Shepherd GM (ed) The synaptic organization of the brain, 5th edn. Oxford University Press, New York, pp 415–454

    Chapter  Google Scholar 

  • Niimura Y, Nei M (2005) Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proc Natl Acad Sci USA 102:6039–6044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niimura Y, Nei M (2007) Extensive gains and losses of olfactory receptor genes in mammalian evolution. PLoS One 2:e708

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Niimura Y, Matsui A, Touhara K (2014) Extreme expansion of the olfactory receptor gene repertoire in African elephants and evolutionary dynamics of orthologous gene groups in 13 placental mammals. Genome Res 24:1485–1496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nozawa M, Kawahara Y, Nei M (2007) Genomic drift and copy number variation of sensory receptor genes in humans. Proc Natl Acad Sci USA 104:20421–20426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olender T, Waszak SM, Viavant M et al (2012) Personal receptor repertoires: olfaction as a model. BMC Genomics 13:414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onishi A, Koike S, Ida M et al (1999) Dichromatism in macaque monkeys. Nature 402:139–140

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Parraga CA, Troscianko T, Tolhurst DJ (2002) Spatiochromatic properties of natural images and human vision. Curr Biol 12:483–487

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pessoa DM, Maia R, de Albuquerque Ajuz RC et al (2014) The adaptive value of primate color vision for predator detection. Am J Primatol 76:721–729

    Article  PubMed  Google Scholar 

  • Peterlin Z, Firestein S, Rogers ME (2014) The state of the art of odorant receptor deorphanization: a report from the orphanage. J Gen Physiol 143:527–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ressler KJ, Sullivan SL, Buck LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597–609

    Article  CAS  PubMed  Google Scholar 

  • Rowe MP, Jacobs GH (2007) Naturalistic color discriminations in polymorphic platyrrhine monkeys: effects of stimulus luminance and duration examined with functional substitution. Vis Neurosci 24:17–23

    Article  PubMed  Google Scholar 

  • Rushmore J, Leonhardt SD, Drea CM (2012) Sight or scent: lemur sensory reliance in detecting food quality varies with feeding ecology. PLoS One 7:e41558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Saito H, Chi Q, Zhuang H et al (2009) Odor coding by a mammalian receptor repertoire. Sci Signal 2:ra9

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Shepherd GM (2004) The human sense of smell: are we better than we think? PLoS Biol 2:E146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shichida Y, Imai H (1998) Visual pigment: G-protein-coupled receptor for light signals. Cell Mol Life Sci 54:1299–1315

    Article  CAS  PubMed  Google Scholar 

  • Shigemura N, Shirosaki S, Sanematsu K et al (2009) Genetic and molecular basis of individual differences in human umami taste perception. PLoS One 4:e6717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Siemers BM, Goerlitz HR, Robsomanitrandrasana E et al (2007) Sensory basis of food detection in wild Microcebus murinus. Int J Primatol 28:291–304

    Article  Google Scholar 

  • Silveira LCL, Saito CA, da Silva FM et al (2014) Alouatta trichromatic color vision: cone spectra and physiological responses studied with microspectrophotometry and single unit retinal electrophysiology. PLoS One 9:e113321

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith AC, Buchanan-Smith HM, Surridge AK et al (2003) 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

    Article  PubMed  Google Scholar 

  • Smith TD, Bhatnagar KP, Tuladhar P et al (2004) Distribution of olfactory epithelium in the primate nasal cavity: are microsmia and macrosmia valid morphological concepts? Anat Rec A 281A:1173–1181

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Smith TD, Rossie JB, Bhatnagar KP (2007) Evolution of the nose and nasal skeleton in primates. Evol Anthropol 16:132–146

    Article  Google Scholar 

  • Smith AC, Surridge AK, Prescott MJ et al (2012) Effect of colour vision status on insect prey capture efficiency of captive and wild tamarins (Saguinus spp.) Anim Behav 83:479–486

    Article  Google Scholar 

  • Sugawara T, Go Y, Udono T et al (2011) Diversification of bitter taste receptor gene family in western chimpanzees. Mol Biol Evol 28:921–931

    Article  CAS  PubMed  Google Scholar 

  • Sumner P, Mollon JD (2000) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986

    CAS  PubMed  Google Scholar 

  • Sumner P, Mollon JD (2003) Colors of primate pelage and skin: objective assessment of conspicuousness. Am J Primatol 59:67–91

    Article  PubMed  Google Scholar 

  • Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198–205

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Sugawara T, Matsui A et al (2010) Identification of non-taster Japanese macaques for a specific bitter taste. Primates 51:285–289

    Article  PubMed  Google Scholar 

  • Suzuki-Hashido N, Hayakawa T, Matsui A et al (2015) Rapid expansion of phenylthiocarbamide non-tasters among Japanese macaques. PLoS One 10:e0132016

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Talebi MG, Pope TR, Vogel ER et al (2006) Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae). Mol Ecol 15:551–558

    Article  CAS  PubMed  Google Scholar 

  • Tan Y, Li W-H (1999) Trichromatic vision in prosimians. Nature 402:36

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terao K, Mikami A, Saito A et al (2005) Identification of a protanomalous chimpanzee by molecular genetic and electroretinogram analyses. Vis Res 45:1225–1235

    Article  PubMed  Google Scholar 

  • Toda Y, Okada S, Misaka T (2011) Establishment of a new cell-based assay to measure the activity of sweeteners in fluorescent food extracts. J Agric Food Chem 59:12131–12138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toda Y, Nakagita T, Hayakawa T et al (2013) Two distinct determinants of ligand specificity in T1R1/T1R3 (the umami taste receptor). J Biol Chem 288:36863–36877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Touhara K, Vosshall LB (2009) Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 71:307–332

    Article  CAS  PubMed  Google Scholar 

  • Touhara K, Sengoku S, Inaki K et al (1999) Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc Natl Acad Sci USA 96:4040–4045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valenta K, Burke RJ, Styler SA et al (2013) Colour and odour drive fruit selection and seed dispersal by mouse lemurs. Sci Rep 3:2424

    Article  PubMed  PubMed Central  Google Scholar 

  • Valenta K, Brown KA, Melin AD et al (2015) It's not easy being blue: are there olfactory and visual trade-offs in plant signalling? PLoS One 10:e0131725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vassar R, Ngai J, Axel R (1993) Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309–318

    Article  CAS  PubMed  Google Scholar 

  • Veilleux CC, Bolnick DA (2009) Opsin gene polymorphism predicts trichromacy in a cathemeral lemur. Am J Primatol 71:86–90

    Article  CAS  PubMed  Google Scholar 

  • Veilleux CC, Cummings ME (2012) Nocturnal light environments and species ecology: implications for nocturnal color vision in forests. J Exp Biol 215:4085–4096

    Article  PubMed  Google Scholar 

  • 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 30:1420–1437

    Article  CAS  PubMed  Google Scholar 

  • Verrelli BC, Tishkoff SA (2004) Signatures of selection and gene conversion associated with human color vision variation. Am J Hum Genet 75:363–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vorobyev M (2004) Ecology and evolution of primate colour vision. Clin Exp Optom 87:230–238

    Article  PubMed  Google Scholar 

  • Wald G (1968) Molecular basis of visual excitation. Science 162:230–239

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Thomas SD, Zhang J (2004) Relaxation of selective constraint and loss of function in the evolution of human bitter taste receptor genes. Hum Mol Genet 13:2671–2678

    Article  CAS  PubMed  Google Scholar 

  • Wildman DE, Jameson NM, Opazo JC et al (2009) A fully resolved genus level phylogeny of neotropical primates (Platyrrhini). Mol Phylogenet Evol 53:694–702

    Article  CAS  PubMed  Google Scholar 

  • Winderickx J, Lindsey DT, Sanocki E et al (1992) Polymorphism in red photopigment underlies variation in colour matching. Nature 356:431–433

    Article  CAS  PubMed  Google Scholar 

  • 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 2:1413–1421

    Article  CAS  PubMed  Google Scholar 

  • Wooding S, Bufe B, Grassi C et al (2006) Independent evolution of bitter-taste sensitivity in humans and chimpanzees. Nature 440:930–934

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S (2000a) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S (2000b) Phylogenetic analysis and experimental approaches to study color vision in vertebrates. Methods Enzymol 315:312–325

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Young JM, Shykind BM, Lane RP et al (2003) Odorant receptor expressed sequence tags demonstrate olfactory expression of over 400 genes, extensive alternate splicing and unequal expression levels. Genome Biol 4:R71

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Yang JR, Xu H et al (2010) Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo. Mol Biol Evol 27:2669–2673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Wang B, Pan Q et al (2014) Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history. Nat Genet 46:1303–1310

    Article  CAS  PubMed  Google Scholar 

  • Zhuang H, Matsunami H (2008) Evaluating cell-surface expression and measuring activation of mammalian odorant receptors in heterologous cells. Nat Protoc 3:1402–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuang HY, Chien MS, Matsunami H (2009) Dynamic functional evolution of an odorant receptor for sex-steroid-derived odors in primates. Proc Natl Acad Sci USA 106:21247–21251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, Japan

    Shoji Kawamura

  2. Department of Anthropology and Archaeology, Department of Medical Genetics, University of Calgary, Calgary, AB, Canada

    Amanda D. Melin

  3. Alberta Children’s Hospital Research Institute, University of Calgary, Calgary, AB, Canada

    Amanda D. Melin

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  1. Shoji Kawamura
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  2. Amanda D. Melin
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Correspondence to Shoji Kawamura or Amanda D. Melin .

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Editors and Affiliations

  1. Division of Population Genetics, National Institute of Genetics, Mishima, Japan

    Naruya Saitou

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Kawamura, S., Melin, A.D. (2017). Evolution of Genes for Color Vision and the Chemical Senses in Primates. In: Saitou, N. (eds) Evolution of the Human Genome I. Evolutionary Studies. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56603-8_10

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