Sensing in Nature pp 156-172

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 739) | Cite as

The Evolution of Vertebrate Color Vision

  • Gerald H. Jacobs

Abstract

Color vision is conventionally defined as the ability of animals to reliably discriminate among objects and lights based solely on differences in their spectral properties. Although the nature of color vision varies widely in different animals, a large majority of all vertebrate species possess some color vision and that fact attests to the adaptive importance this capacity holds as a tool for analyzing the environment. In recent years dramatic advances have been made in our understanding of the nature of vertebrate color vision and of the evolution of the biological mechanisms underlying this capacity. In this chapter I review and comment on these advances.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Olson JM. Photosynthesis in the Archean era. Photosyn Res 2006; 88:109–117.PubMedCrossRefGoogle Scholar
  2. 2.
    Hoashi M, Bevacqua DC, Otake T et al. Primary heamatite formation in an oxygenated sea 3.46 billion years ago. Nature Geosci 2009; 2:301–306.CrossRefGoogle Scholar
  3. 3.
    Green BR. Was “molecular opportunism” a factor in evolution of photosynthetic light-harvesting systems? Proc Natl Acad Sci USA 2001; 98:2119–2121.PubMedCrossRefGoogle Scholar
  4. 4.
    Hardin CL. Color for Philosophers. Indianapolis: Hackett Publishing Company, 1988.Google Scholar
  5. 5.
    Newton I. Optics: Dover, 1952 edition, 1730.Google Scholar
  6. 6.
    Jacobs GH. The distribution and nature of colour vision among the mammals. Biol Rev 1993; 68:413–471.PubMedCrossRefGoogle Scholar
  7. 7.
    Kelber A, Vorobyev M, Osorio D. Animal colour vision—behavioural tests and physiological concepts. Biol Rev 2003; 78:81–118.PubMedCrossRefGoogle Scholar
  8. 8.
    Skorupski P, Chittka L. Is colour cognitive? Opt Laser Tech 2011; 43:251–260.CrossRefGoogle Scholar
  9. 9.
    Jacobs GH, Rowe MP. Evolution of vertebrate colour vision. Clin Exptl Optom 2004; 87:206–216.CrossRefGoogle Scholar
  10. 10.
    Neitz J, Carroll J, Neitz M. Color vision: almost reason enough for having eyes. Opt Photon News 2001; 12:26–33.CrossRefGoogle Scholar
  11. 11.
    Lythgoe JN. The Ecology of Vision. New York: Oxford University Press, 1979:244.Google Scholar
  12. 12.
    Jacobs GH. Comparative Color Vision. New York: Academic Press, 1981.Google Scholar
  13. 13.
    Mollon JD. “Tho she kneel’d in that place where they grew.” The uses and origins of primate colour vision. J Exptl Bio 1989; 146:21–38.Google Scholar
  14. 14.
    Wensel TG. Signal transducing membrane complexes of photoreceptor outer segments. Vis Res 2008; 48:2052–2061.PubMedCrossRefGoogle Scholar
  15. 15.
    Solomon SG, Lennie P. The machinery of colour vision. Nat Neurosci Rev 2007; 8:276–286.CrossRefGoogle Scholar
  16. 16.
    Nathans J, Hogness DS. Isolation, sequence analysis and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell 1983; 34:807–814.PubMedCrossRefGoogle Scholar
  17. 17.
    Yokoyama S. Evolution of dim-light and color vision pigments. Annual Review of Genom Hum Genet 2009; 9:259–282.CrossRefGoogle Scholar
  18. 18.
    Yokoyama S, Radlwimmer FB. The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 2001; 158:1697–1710.PubMedGoogle Scholar
  19. 19.
    Carroll J, Jacobs GH. Mammalian photopigments. In: Masland RH, Albright TD, eds. The Senses: A Comprehensive Reference. New York: Elsevier, 2008; 247–268.CrossRefGoogle Scholar
  20. 20.
    Dartnall HJA. Identity and distribution of visual pigments in the animal kingdom. In: Davson H, ed. The Visual Process. New York: Academic Press, 1962; 367–425.Google Scholar
  21. 21.
    Bowmaker JK. Evolution of vertebrate visual pigments. Vis Res 2008; 48:2022–2041.PubMedCrossRefGoogle Scholar
  22. 22.
    Douglas RH, Marshall NJ. A review of vertebrate and invertebrate ocular filters. In: Archer SN, Djamgoz MBA, Loew ER et al, eds. Adaptive Mechanisms in the Ecology of Vision. Dordrecht: Kluwer Academic Publishers, 1999; 95–162.Google Scholar
  23. 23.
    Vorobyev M. Coloured oil droplets enhance colour discrimination. Proc Roy Soc Lond B 2003; 270: 1255–1261.CrossRefGoogle Scholar
  24. 24.
    Lamb TD, Collin SP, Pugh ENJ. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye-cup. Nat Rev Neurosci 2007; 8:960–975.PubMedCrossRefGoogle Scholar
  25. 25.
    Collin SP, Knight MA, Davies WL et al. Ancient colour vision: multiple opsin genes in ancestral vertebrates. Curr Biol 2003; 13:R864–R865.PubMedCrossRefGoogle Scholar
  26. 26.
    Collin S, Davies W, Hunt D. The evolution of early vertebrate photoreceptors. Phil Trans Roy Soc Lond B 2009; 364:2925–2940.CrossRefGoogle Scholar
  27. 27.
    Maximov VV. Environmental factors which may have led to the appearance of colour vision. Phil Trans Roy Soc Lond B 2000; 355:1239–1242.CrossRefGoogle Scholar
  28. 28.
    Kuraku S, Meyer A, Kuratani S. Timing of genome duplications relative to the origin of vertebrates: did cyclostomes diverge before or after? Mol Biol Evol 2009; 26:47–59.PubMedCrossRefGoogle Scholar
  29. 29.
    Parry JWL, Carleton KL, Spady T et al. Mix and match color vision: tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Curr Biol 2005; 15:1734–1739.PubMedCrossRefGoogle Scholar
  30. 30.
    Barlow HB. What causes trichromacy? A theoretical analysis using comb-filtered spectra. Vis Res 1982; 22:635–643.PubMedCrossRefGoogle Scholar
  31. 31.
    Osorio D, Bossomaier TRJ. Human cone pigment spectral sensitivities and the reflectances of natural surfaces. Biol Cyber 1992; 67:217–222.CrossRefGoogle Scholar
  32. 32.
    Howard J, Blakeslee B, Laughlin SB. The intracellular pupil mechanism and photoreceptor signal-noise ratio in the fly Lucilla cuprina. Proc Roy Soc Lond B 1987; 231:415–435.CrossRefGoogle Scholar
  33. 33.
    Niven JE, Laughlin SB. Energy limitation as a selective pressure on the evolution of sensory systems. J Exptl Biol 2008; 211:1792–1804.CrossRefGoogle Scholar
  34. 34.
    Mollon JD, Estevez O, Cavonius CR. The two subsystems of colour vision and their roles in wavelength discrimination. In: Blakemore C, ed. Vision: Coding and Efficiency. Cambridge: Cambridge University Press, 1990:119–131.Google Scholar
  35. 35.
    Hunt DM, Carvalho LS, Cowing JA et al. Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem Photobiol 2007; 83:303–310.PubMedCrossRefGoogle Scholar
  36. 36.
    Hunt D, Carvalho LS, Cowing JA et al. Evolution and spectral tuning of visual pigments in birds and mammals. Phil Trans Roy Soc Lond B 2009; 364:2941–2955.CrossRefGoogle Scholar
  37. 37.
    Sterling P. How retinal circuits optimize the transfer of visual information. In: Chalupa LM, Werner JS, eds. The Visual Neurosciences. Boston: MIT Press, 2004:234–259.Google Scholar
  38. 38.
    Okano T, Kojima D, Fukada Y et al. Primary structures of chicken visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc Natl Acad Sci USA 1992; 89:5932–5936.PubMedCrossRefGoogle Scholar
  39. 39.
    Makous W. Scotopic Vision. In: Chalupa LM, Werner JS, eds. The Visual Neurosciences. Cambridge: MIT Press, 2004:838–850.Google Scholar
  40. 40.
    LaVail MM. Survival of some photoreceptors in albino rats following long-term exposure to continuous light. Invest Ophthal Vis Sci 1976; 15:64–70.Google Scholar
  41. 41.
    Muller B, Peichl L. Topography of cones and rods in the tree shrew retina. J Comp Neurol 1989; 282:581–594.PubMedCrossRefGoogle Scholar
  42. 42.
    Steiper ME, Ruvolo M. New World monkey phylogeny based on X-linked G6PD DNA sequences. Mol Phylogenet Evol 2003; 27:121–130.PubMedCrossRefGoogle Scholar
  43. 43.
    Finlay BL. The developing and evolving retina: using time to organize form. Br Res 2007; 1192:5–16.CrossRefGoogle Scholar
  44. 44.
    Dyer MA, Martins R, Filho MS et al. Developmental sources of conservation and variation in the evolution of the primate eye. Proc Natl Acad Sci USA 2009; 106:8963–8968.PubMedCrossRefGoogle Scholar
  45. 45.
    Yokoyama S. Molecular evolution of color vision in vertebrates. Gene 2002; 300:69–78.PubMedCrossRefGoogle Scholar
  46. 46.
    Lamb TD, Pugh ENJ, Collin SP. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye-cup. Nat Rev Neurosci 2007; 8:960–975.PubMedCrossRefGoogle Scholar
  47. 47.
    Yokoyama S. Evolution of dim-light and color vision pigments. Ann Rev Genom Hum Genet 2008; 9:259–282.CrossRefGoogle Scholar
  48. 48.
    Hunt DM, Carvalho LS, Cowing JA et al. Evolution and spectral tuning of visual pigments in birds and mammals. Phil Trans Roy Soc Lond B 2009; 364:2941–2956.CrossRefGoogle Scholar
  49. 49.
    Collin SP, Davies WL, Hart NS et al. The evolution of early vertebrate photoreceptors. Phil Trans Roy Soc Lond B 2009; 364:2925–2940.CrossRefGoogle Scholar
  50. 50.
    Jacobs GH. Evolution of colour vision in mammals. Phil Trans Roy Soc Lond B 2009; 364:2957–2967.CrossRefGoogle Scholar
  51. 51.
    Kemp TS. The Origin and Evolution of Mammals. Oxford, UK: Oxford University Press, 2005.Google Scholar
  52. 52.
    Davies WL, Caravalho LS, Cowing JA et al. Visual pigments of the platypus: a novel route to mammalian colour vision. Curr Biol 2007; 17:B161–B163.CrossRefGoogle Scholar
  53. 53.
    Wakefield MJ, Anderson M, Chang E et al. Cone visual pigments of monotremes: filling the phylogenetic gap. Vis Neurosci 2008; 25:257–264.PubMedCrossRefGoogle Scholar
  54. 54.
    Hemmi JM. Dichromatic colour vision in an Australian marsupial, the tammar wallaby. J Comp Physiol A 1999; 185:509–515.PubMedCrossRefGoogle Scholar
  55. 55.
    Hemmi JM, Maddess T, Mark RF. Spectral sensitivity of photoreceptors in an Australian marsupial, the tammar wallaby (Macropus eugenii). Vis Res 2000; 40:591–599.PubMedCrossRefGoogle Scholar
  56. 56.
    Arrese CA, Hart NS, Thomas N et al. Trichromacy in Australian marsupials. Curr Biol 2002; 12:657–660.PubMedCrossRefGoogle Scholar
  57. 57.
    Arrese CA, Beazley LD, Neumeyer C. Behavioural evidence of marsupial trichromacy. Curr Biol 2006; 16:R193–R194.PubMedCrossRefGoogle Scholar
  58. 58.
    Cowing JA, Arrese CA, Davies WL et al. Cone visual pigmens in two marsuial species: the fat-tailed dunnart (Sminthopsis crassicaudatus) and the honey possum (Tarsipes rostratus). Proc Roy Soc Lond B 2008; 275:1491–1499.CrossRefGoogle Scholar
  59. 59.
    Hunt DM, Wilkie SE, Bowmaker JK et al. Vision in the ultraviolet. Cell Mol Life Sci 2001; 58:1583–1598.PubMedCrossRefGoogle Scholar
  60. 60.
    Yokoyama S, Yang H, Starmer WT. Molecular basis of spectral tuning in the red-and green-sensitive (M/LWS) pigments in vertebrates. Genetics 2008; 179:2037–2041.PubMedCrossRefGoogle Scholar
  61. 61.
    Chiao C-C, Vorobyev M, Cronin TW et al. Spectral tuning of dichromats to natural scenes. Vis Res 2000; 40:3257–3271.PubMedCrossRefGoogle Scholar
  62. 62.
    Jacobs GH, Deegan JF II, Neitz JA et al. Photopigments and color vision in the nocturnal monkey, Aotus. Vis Res 1993; 33:1773–1783.CrossRefGoogle Scholar
  63. 63.
    Deegan JF II, Jacobs GH. Spectral sensitivity and photopigments of a nocturnal prosimian, the bushbaby (Otolemur crassicaudatus). Amer J Primatol 1996; 40:55–66.CrossRefGoogle Scholar
  64. 64.
    Jacobs GH, Neitz M, Neitz J. Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proc Roy Soc Lond B 1996; 263:705–710.CrossRefGoogle Scholar
  65. 65.
    Peichl L. Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec A 2005; 287A:1001–1012.CrossRefGoogle Scholar
  66. 66.
    Levenson DH, Dizon A. Genetic evidence for the ancestral loss of SWS cone pigments in mysticetee and odontocete cetaceans. Proc Roy Soc Lond B 2003; 270:673–679.CrossRefGoogle Scholar
  67. 67.
    Levenson DH, Ponganis PJ, Crognale MA et al. Visual pigments of marine carnivores: pinnipeds, polar bear and sea otter. J Comp Physiol A 2006; 192:833–843.CrossRefGoogle Scholar
  68. 68.
    Go Y, Satta Y, Takenaka O et al. Lineage-specific loss of function of bitter taste receptor genes in humans and nonhuman primates. Genetics 2005; 176:313–326.CrossRefGoogle Scholar
  69. 69.
    Jacobs GH. Recent progress in understanding mammalian color vision. Ophthal Physiol Optics 2010: 30(5):422–34.CrossRefGoogle Scholar
  70. 70.
    Steiper ME, Young MM. Primate molecular divergence dates. Molr Phylogenet Evol 2006; 41:384–394.CrossRefGoogle Scholar
  71. 71.
    Martin RD, Ross CF. The evolutionary and ecological context of primate vision. In: Kremers J, ed. The Primate Visual System: A Comparative Approach. West Sussex: John Wiley and Sons, Ltd., 2005.Google Scholar
  72. 72.
    Nathans J. Molecular biology of visual pigments. Ann Rev Neurosci 1987; 10:163–194.PubMedCrossRefGoogle Scholar
  73. 73.
    Nathans J, Piantanida TP, Eddy RL et al. Molecular genetics of inherited variation in color vision. Science 1986; 233:203–210.CrossRefGoogle Scholar
  74. 74.
    Jacobs GH. Primate color vision: a comparative perspective. Vis Neurosci 2007; 25:619–633.CrossRefGoogle Scholar
  75. 75.
    Jacobs GH, Williams GA. The prevalence of defective color vision in Old World monkeys and apes. Color Res Appl 2001; 26:S123–S127.CrossRefGoogle Scholar
  76. 76.
    Jacobs GH. New World monkeys and color. Internat J Primatol 2007; 28:729–759.CrossRefGoogle Scholar
  77. 77.
    Jacobs GH, Neitz J. Inheritance of color vision in a New World monkey (Saimiri sciureus). Proc Natl Acad Sci USA 1987; 84:2545–2549.PubMedCrossRefGoogle Scholar
  78. 78.
    Mollon JD, Bowmaker JK, Jacobs GH. Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proc Roy Soc Lond B 1984; 222:373–399.CrossRefGoogle Scholar
  79. 79.
    Surridge AK, Osorio D, Mundy NI. Evolution and selection of trichromatic vision in primates. Trends Ecol Evolut 2003; 18:198–206.CrossRefGoogle Scholar
  80. 80.
    Jacobs GH, Deegan JF II. Photopigments and colour vision in New World monkeys from the family Atelidae. Proc Roy Soc Lond B 2001; 268:695–702.CrossRefGoogle Scholar
  81. 81.
    Jacobs GH, Neitz M, Deegan JF et al. Trichromatic colour vision in New World monkeys. Nature 1996; 382:156–158.PubMedCrossRefGoogle Scholar
  82. 82.
    Hunt DM, Dulai KS, Cowing JA et al. Molecular evolution of trichromacy in primates. Visi Res 1998; 38:3299–3306.CrossRefGoogle Scholar
  83. 83.
    Jacobs GH, Deegan II JF. Photopigments underlying color vision in ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus). Amer J Primatol 1993; 30:243–256.CrossRefGoogle Scholar
  84. 84.
    Tan Y, Li W-H. Trichromatic vision in prosimians. Nature 1999; 402:36.PubMedCrossRefGoogle Scholar
  85. 85.
    Jacobs GH, Deegan JF II, Tan Y et al. Opsin gene and photopigment polymorphism in a prosimian primate. Vis Res 2002; 42:11–18.PubMedCrossRefGoogle Scholar
  86. 86.
    Land MF, Nilsson D-E. Animal Eyes. New York: Oxford University Press, 2002.Google Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2012

Authors and Affiliations

  • Gerald H. Jacobs
    • 1
  1. 1.Department of PsychologyUniversity of CaliforniaSanta BarbaraUSA

Personalised recommendations