The Evolution and Physiology of Human Color Vision

Abstract

Nothing in biology makes sense except in light of evolution.—T. Dobzhansky Color vision is the process by which an organism extracts information regarding the wavelength composition of a visual stimulus (Figure 1). In its simplest form—exemplified by the wavelength-dependent phototactic responses of halobacteria—color vision is based on the relative abundances of two isoforms of a sensory pigment (25Hoff W.D Jung K.H Spudich J.L Molecular mechanism of photosignaling by archaeal sensory rhodopsins.Annu. Rev. Biophys. Biomol. Struct. 1997; 26: 223-258Crossref PubMed Scopus (284) Google Scholar). One isoform preferentially absorbs long wavelength light and mediates a photoattractant response, and the second isoform preferentially absorbs short wavelength light and mediates a photorepellant response. Light absorption photoconverts the first isoform into the second, and the second into the first. Thus, the steady-state ratio of pigment isoforms provides a measure of the spectral composition of the ambient light. The halobacterial system contains the two cardinal elements of every color vision system: (1) two or more sensory pigments with different spectral sensitivities (although in most organisms these are distinct chromoproteins rather than isoforms of a single chromoprotein), and (2) a mechanism for monitoring the relative number of photons captured by the different pigments. In higher eukaryotes, this system has evolved so that, in general, each pigment resides within a distinct class of photoreceptor cells, and therefore the ratios of photoexcitation of the different pigments can be determined by assessing the ratios of activation of different photoreceptor cells. Visual pigments are G protein–coupled receptors in which a seven-transmembrane segment protein is covalently linked to a chromophore, 11-cis retinal. Studies of the visual pigment complement and color vision ability of different vertebrates reveal an ancient and nearly universal color vision system in which one visual pigment has an absorption maximum at <500 nm and a second visual pigment has an absorption maximum at >500 nm (47Mollon J.D “Tho she kneel'd in that place where they grew…”—the uses and origins of primate colour vision.J. Exp. Biol. 1989; 146: 21-38PubMed Google Scholar, 100Yokoyama S Molecular genetic basis of adaptive selection examples from color vision in vertebrates.Annu. Rev. Genet. 1997; 31: 315-336Crossref PubMed Scopus (82) Google Scholar). Rhodopsin, a third and equally ancient pigment, has an absorption maximum at ∼500 nm and plays little or no role in color vision. In general, the pigments mediating color vision reside in cone photoreceptors and are used only under bright light conditions, whereas rhodopsin resides in rod photoreceptors and is used under dim light conditions. Present-day vertebrates vary enormously in the sophistication of their color vision, the density and spatial distribution of cone classes, and the number and absorption maxima of their cone pigments (Figure 2; 38Lythgoe J.N The Ecology of Vision. Clarendon Press, Oxford1979Google Scholar, 30Jacobs G.H Comparative Color Vision. Academic Press, New York1981Google Scholar, 31Jacobs G.H The distribution and nature of colour vision among the mammals.Biol. Rev. 1993; 68: 413-471Crossref PubMed Google Scholar, 100Yokoyama S Molecular genetic basis of adaptive selection examples from color vision in vertebrates.Annu. Rev. Genet. 1997; 31: 315-336Crossref PubMed Scopus (82) Google Scholar). At one extreme, most mammals have only three pigments: the two ancestral cone pigments and rhodopsin. At the other evolutionary extreme, chickens possess six pigments: four cone pigments, one rhodopsin, and a pineal visual pigment, pinopsin. As seen in the dendrogram in Figure 2, the chicken green pigment was derived from a duplication within the rhodopsin branch. In this evolutionary comparison, humans and their closest primate relatives represent an intermediate level of complexity. Humans have four visual pigments: a single member of the <500 nm family of cone pigments (the blue or short-wave pigment, with an absorption maximum at ∼425 nm), two highly homologous members of the >500 nm family (the green or middle-wave pigment, and red or long-wave pigment, with absorption maxima at ∼530 and ∼560 nm, respectively), and rhodopsin. The presence of only a single gene encoding a >500 nm pigment in almost all New World primates, and in all nonprimate mammals studied to date, places the red/green visual pigment gene duplication in the Old World primate lineage at ∼30–40 million years ago, shortly after the geologic split between Africa and South America (31Jacobs G.H The distribution and nature of colour vision among the mammals.Biol. Rev. 1993; 68: 413-471Crossref PubMed Google Scholar). Current molecular genetic evidence suggests that howler monkeys, the only of New World primate with two >500 nm pigment have a gene duplication that is of the one within the Old World primate