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Cone pigment polymorphism in New World monkeys: Are all pigments created equal?

Published online by Cambridge University Press:  05 April 2005

MICKEY P. ROWE
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara
GERALD H. JACOBS
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara

Abstract

Most platyrrhine monkeys have a triallelic M/L opsin gene polymorphism that underlies significant individual variations in color vision. A survey of the frequencies of these polymorphic genes suggests that the three alleles occur with equal frequency among squirrel monkeys (subfamily Cebinae), but are not equally frequent in a number of species from the subfamily Callitrichinae. This departure from equal frequency in the Callitrichids should slightly increase the ratio of dichromats to trichromats in the population and significantly alter the relative representation of the three possible dichromatic and trichromatic phenotypes. A particular feature of the inequality is that it leads to a relative increase in the number of trichromats whose M/L pigments have the largest possible spectral separation. To assess whether these trichromatic phenotypes are equally well equipped to make relevant visual discriminations, psychophysical experiments were run on human observers. A technique involving the functional substitution of photopigments was used to simulate the discrimination between fruits among a background of leaves. The goal of the simulation was to reproduce in the cones of human observers excitations equivalent to those produced in monkey cones as the animals view fruit. Three different viewing conditions were examined involving variations in the relative luminances of fruit and leaves and the spectrum of the illuminant. In all cases, performance was best for simulated trichromacies including M/L pigments with the largest spectral separation. Thus, the inequality of opsin gene frequency in Callitrichid monkeys may reflect adaptive pressures.

Type
Research Article
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

Boissinot, S., Tan, Y., Shyue, S.K., Schneider, H., Sampaio, I., Neiswanger, K., Hewett-Emmett, D., & Li, W.H. (1998). Origins and antiquity of X-linked triallelic color vision systems in New World monkeys. Proceedings of the National Academy of Sciences of the U.S.A. 95, 1374913754.Google Scholar
Brainard, D.H. (1997). The psychophysics toolbox. Spatial Vision 10, 433436.Google Scholar
Brettel, H., Viénot, F., & Mollon, J.D. (1997). Computerized simulation of color appearance for dichromats. Journal of the Optical Society of America A 14, 26472655.Google Scholar
Caine, N.G. & Mundy, N.I. (2000). Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proceedings of the Royal Society B (London) 267, 439444.Google Scholar
Caine, N.G., Surridge, A.K., & Mundy, N.I. (2003). Dichromatic and trichromatic Callithrix geoffroyi differ in relative foraging ability for red–green color-comouflaged and noncamouflaged food. International Journal of Primatology 24, 11631175.Google Scholar
Carroll, J., Murphy, C., Neitz, M., Ver Hoeve, J., & Neitz, J. (2001). Photopigment basis for dichromatic color vision in the horse. Journal of Vision 1. 8087, http://journalofvision.org/1/2/2/, DOI 10.1167/1.2.2.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. Journal of Molecular Evolution 54, 734745.Google Scholar
Dominy, N.J., Garber, P.A., Bicca-Marques, C., Azevedo-Lopes, M.A.P. de O. (2003). Do female tamarins use visual cues to detect fruit rewards more successfully than do males? Animal Behaviour 66, 829837.Google Scholar
Endler, J.A. (1993). The color of light in forests and its implications. Ecological Monographs 63, 127.Google Scholar
Jacobs, G.H. (1984). Within-species variations in visual capacity among squirrel monkeys (Saimiri sciureus): Color vision. Vision Research 24, 12671277.Google Scholar
Jacobs, G.H. (1998). A perspective on color vision in platyrrhine monkeys. Vision Research 38, 33073313.Google Scholar
Jacobs, G.H. & Deegan, J.F. II (2003). Cone pigment variations in four genera of New World monkeys. Vision Research 43, 227236.Google Scholar
Jacobs, G.H. & Neitz, J. (1987). Inheritance of color vision in a New World monkey (Saimiri sciureus). Proceedings of the National Academy of Sciences of the U.S.A. 84, 25452549.Google Scholar
Jacobs, G.H., Neitz, J., & Crognale, M. (1987). Color vision polymorphism and its photopigment basis in a callitrichid monkey (Saguinus fuscicollis). Vision Research 27, 20892100.Google Scholar
Jacobs, G.H., Neitz, J., & Neitz, M. (1993). Genetic basis of polymorphism in the color vision of platyrrhine monkeys. Vision Research 33, 269274.Google Scholar
Kinzey, W.G. (1997). Synopsis of New World Primates. In New World Primates: Ecology, Evolution, and Behavior, ed. Kinzey, W.G., pp. 169324. New York: Walter de Gruyter, Inc.
Mollon, J.D., Bowmaker, J.K., & Jacobs, G.H. (1984). Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proceedings of the Royal Society B (London) 222, 373399.Google Scholar
Pelli, D.G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision 10, 437442.Google Scholar
Pokorny, J. & Smith, V.C. (1977). Evaluation of single-pigment shift model of anomalous trichromacy. Journal of the Optical Society of America 67, 11961209.Google Scholar
Pokorny, J., Smith, V.C., Verriest, G., & Pinkers, A.J.L.G. (1979). Congenital and Acquired Color Vision Defects. New York: Grune and Stratton.
Regan, B.C., Julliot, C., Simmen, B., Viénot, F., Charles-Dominique, P., & Mollon, J.D. (2001). Fruits, foliage and the evolution of primate colour vision. Philosophical Transactions of the Royal Society B (London) 356, 229283.Google Scholar
Shyue, S.-K., D.Hewett-Emmett, D., Sperling, H.G., Hunt, D.M., Bowmaker, J.K., Mollon, J.D., & Li, W.H. (1995). Adaptive evolution of color vision genes in higher primates. Science 269, 12651267.Google Scholar
Smith, A.C., Buchanan-Smith, H.M., Surridge, A.K., Osorio, D., & Mundy, N.I. (2003). The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). Journal of Experimental Biology 206, 31593165.Google Scholar
Smith, V.C. & Pokorny, J. (1975). Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Research 15, 161171.Google Scholar
Surridge, A.K. & Mundy, N.I. (2002). Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates. Molecular Ecology 11, 21572169.Google Scholar
Tovée, M.J., Bowmaker, J.K., & Mollon, J.D. (1992). The relationship between cone pigments and behavioural sensitivity in a New World monkey (Callithrix jacchus jacchus). Vision Research 32, 867878.Google Scholar
Travis, D.S., Bowmaker, J.K., & Mollon, J.D. (1988). Polymorphism of visual pigments in a callitrichid monkey (Callithrix jacchus jacchus). Vision Research 28, 481490.Google Scholar
Vorobyev, M., Gumbert, A., Kunze, J., Giurfa, M., & Menzel, R. (1997). Flowers through insect eyes. Israel Journal of Plant Sciences 45, 93101.Google Scholar
Vorobyev, M., Marshall, J., Osorio, D., de Ibarra, N.H., & Menzel, R. (2001). Colourful objects through animal eyes. Color Research and Application 26 (SUPPS), S214S217.Google Scholar
Williams, A.J., Hunt, D.M., Bowmaker, J.K., & Mollon, J.D. (1992). The polymorphic photopigments of the marmoset: Spectral tuning and genetic basis. EMBO Journal 11, 20392045.Google Scholar