Colour Vision in New World Monkeys and the Single-Locus X-Chromosome Theory

The disabilities experienced by colour-blind people show us the biological advantages of colour vision in detecting targets, in segregating the visual field and in identifying particular objects or states. Human dichromats have especial difficulty in detecting coloured fruit against dappled foliage that varies randomly in luminosity; it is suggested that yellow and orange tropical fruits have co-evolved with the trichromatic colour vision of Old World monkeys. It is argued that the colour vision of man and of the Old World monkeys depends on two subsystems that remain parallel and independent at early stages of the visual pathway. The primordial subsystem, which is shared with most mammals, depends on a comparison of the rates of quantum catch in the short- and middle-wave cones; this system exists almost exclusively for colour vision, although the chromatic signals carry with them a local sign that allows them to sustain several of the functions of spatiochromatic vision. The second subsystem arose from the phylogenetically recent duplication of a gene on the X-chromosome, and depends on a comparison of the rates of quantum catch in the long- and middle-wave receptors. At the early stages of the visual pathway, this chromatic information is carried by a channel that is also sensitive to spatial contrast. The New World monkeys have taken a different route to trichromacy: in species that are basically dichromatic, heterozygous females gain trichromacy as a result of X-chromosome inactivation, which ensures that different photopigments are expressed in two subsets of retinal photoreceptor.

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Trichromatic colour vision in New World monkeys

Nature ◽

10.1038/382156a0 ◽

1996 ◽

Vol 382 (6587) ◽

pp. 156-158 ◽

Cited By ~ 177

Author(s):

Gerald H. Jacobs ◽

Maureen Neitz ◽

Jess F. Deegan ◽

Jay Neitz

Keyword(s):

Colour Vision ◽

New World ◽

New World Monkeys

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Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari ( Cacajao calvus )

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.0067 ◽

2016 ◽

Vol 283 (1828) ◽

pp. 20160067 ◽

Cited By ~ 11

Author(s):

Josmael Corso ◽

Mark Bowler ◽

Eckhard W. Heymann ◽

Christian Roos ◽

Nicholas I. Mundy

Keyword(s):

Colour Vision ◽

New World ◽

Balancing Selection ◽

Vision System ◽

Alternative Hypothesis ◽

World Monkey ◽

New World Monkeys ◽

Facial Skin ◽

Predator Detection ◽

Functional Alleles

Colour vision is highly variable in New World monkeys (NWMs). Evidence for the adaptive basis of colour vision in this group has largely centred on environmental features such as foraging benefits for differently coloured foods or predator detection, whereas selection on colour vision for sociosexual communication is an alternative hypothesis that has received little attention. The colour vision of uakaris ( Cacajao ) is of particular interest because these monkeys have the most dramatic red facial skin of any primate, as well as a unique fission/fusion social system and a specialist diet of seeds. Here, we investigate colour vision in a wild population of the bald uakari, C. calvus , by genotyping the X-linked opsin locus. We document the presence of a polymorphic colour vision system with an unprecedented number of functional alleles (six), including a novel allele with a predicted maximum spectral sensitivity of 555 nm. This supports the presence of strong balancing selection on different alleles at this locus. We consider different hypotheses to explain this selection. One possibility is that trichromacy functions in sexual selection, enabling females to choose high-quality males on the basis of red facial coloration. In support of this, there is some evidence that health affects facial coloration in uakaris, as well as a high prevalence of blood-borne parasitism in wild uakari populations. Alternatively, the low proportion of heterozygous female trichromats in the population may indicate selection on different dichromatic phenotypes, which might be related to cryptic food coloration. We have uncovered unexpected diversity in the last major lineage of NWMs to be assayed for colour vision, which will provide an interesting system to dissect adaptation of polymorphic trichromacy.

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