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The evolution and function of colour vision in primates

Primates have the best colour vision of all mammals, but there is variation among species, which is attributable to the number of colour vision photopigments (opsins) produced in cone photoreceptor cells in the retina. Remarkably, most New World monkeys have intraspecific variation, with all males and some females having dichromatic colour vision while some females have trichromatic colour vision. Trichromacy gives enhanced colour discrimination in the red-green part of the spectrum, and hence, for example, ability to discriminate the green line of dots among the red dots in the Ishihara plate (shown to the right). The genetic basis of colour vision in primates is well-established, but many questions remain about the selective benefits of trichromacy, and the mechanism for maintenance of polymorphism in New world monkeys.

One question concerns the nature of the selective advantage of trichromacy in female New World monkeys. Together with Nancy Caine at California State University, San Marcos, we have shown that trichromatic marmosets have better foraging ability than dichromats for orange food against a green background. With Andrew Smith and Hannah Buchanan-Smith at Stirling University we have shown that trichromatic tamarins have enhanced foraging ability for food targets of similar colour to that of a favored fruit in their natural habitat in Amazonia. Together, these results suggest that trichromatic marmosets and tamarins may have better foraging ability than dichromats for ripe red/yellow fruit against a foliage background in the wild.

A considerable puzzle is why, if trichromatic marmosets have a foraging advantage for ripe fruit, all marmosets are not trichromats. One much discussed possibility is that dichromats may have an advantage over trichromats under certain conditions, and thus the polymorphism is maintained by frequency-dependent selection. One task in which human dichromats (red-green colour blinds) outperform trichromats is in detecting red-green colour camouflaged objects. This has potential relevance for detection of camouflaged predators and prey in the wild, and is currently under investigation.

References

Surridge, A. K., Suárez, S. S., Buchanan-Smith, H. M. and N. I. Mundy (2005) Non-random
association of opsin alleles in wild groups of red-bellied tamarins (Saguinus labiatus) and maintenance of the colour vision polymorphism. Biology Letters 1, 465-468.

Surridge, A. K., Suárez, S. S., Buchanan-Smith, H. M., Smith, A. C. and N. I. Mundy (2005)
Colour vision pigment frequencies in wild tamarins (Saguinus spp.). American Journal of Primatology 67, 473 - 470.

Smith, A. C., Buchanan-Smith, H. M., Surridge, A. K. and N. I. Mundy (2005) Factors affecting group spread within wild mixed-species troops of saddleback (Saguinus fuscicollis) and moustached tamarins (S. mystax). International Journal of Primatology 25, 337 - 355.

Smith, A.C., Buchanan-Smith, H.M., Surridge, A.K. Osorio, D. and N. I. Mundy. (2003) The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). Journal of Experimental Biology 206, 3159 - 3165.

Caine, N. G., Surridge, A. K., and N. I. Mundy. (2003) Dichromatic and trichromatic Callithrix geoffroyi differ in relative foraging ability for red-green color-camouflaged and non-camouflaged food. International Journal of Primatology 24, 1163 - 1175.

Smith, A.C., Buchanan-Smith, H.M., Surridge, A.K. and N. I. Mundy. (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. American Journal of Primatology 61, 145 – 157.

Surridge, A. K., Osorio, D. and N. I. Mundy. (2003) Evolution and selection of trichromatic vision in primates. Trends in Ecology and Evolution 18, 198-205.

Surridge, A. K. and N. I. Mundy. (2002) Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates. Molecular Ecology 11, 2157-2169.

Surridge, A. K., Smith, A. C., Buchanan-Smith, H. M. and N. I. Mundy. (2002) Single-copy nuclear DNA sequences obtained from non-invasively collected primate feces. American Journal of Primatology 56, 185-190.

Caine, N. G. and N. I. Mundy (2000) Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proceedings of the Royal Society, Series B. 267, 439 – 444.