Evolution of Red-green Visual Pigment Genes and Color Vision of New World Monkeys

Abstract

Most New World (NW) monkeys exhibit extensive intra-specific variations in color vision, where males are dichromatic (red-green colorblind) and females are either dichromatic or trichromatic. This is explained by a model that the red-green visual pigment genes of NW monkeys exist as a single-locus gene with three allelic variations residing on X-chromosome (“tri-allelic single-locus X-chromosome model”). In this study we investigated genomic organization of red-green visual pigment genes of common marmoset (Callithrix jacchus) and owl monkey (Aotus trivirgatus). By fluorescence in situ hybridization (FISH), we directly localized the pigment gene at a locus on X-chromosome of common marmoset. The study on the marmoset provided direct and conclusive evidences for the “tri-allelic single-locus X-chromosome model” on the genetic basis of marmoset color vision.
By using in vitro pigment regeneration method, we determined exact peak absorption spectrum (λmax) of all three allelic pigments, red, yellow, and green, of the marmoset, to be 561, 553, and 539nm, respectively, and green pigment of owl monkey to be 539nm, which were precise to within ±1nm. These values were virtually identical to predicted values based on amino acid sequence at five critical sites: 180, 197, 277, 285, 308.
Interestingly, the nocturnal owl monkey was found to possess multiple green pseudogenes. The phylogenetic analysis indicated that duplications of the green genes occurred in owl monkey lineage and were independent from that in the howler monkey, the only known NW monkey having red and green genes on separate loci. By Southern hybridization, we found one male capuchin monkey (Cebus apella) that appeared to have two red-green-like visual pigment genes. The results obtained from studies on owl monkey and capuchin suggest that the evolution of color vision in NW monkey is more complicated than ever considered.