Evolution of vertebrate visual pigments

Abstract

Unlike most other mammals, primates are trichromatic with three cone pigments, an SWS1 pigment and two variants of the LWS pigments. In Old World primates, two different forms of the LWS gene are present, which have arisen by duplication of an ancestral gene (Figure 4Figure 4). These variants show close identity with each other and encode L and M pigments with λmax values of around 563 nm and 532 nm, respectively.As all Old World primates show this duplication, it must have occurred at the base of the catarrhine lineage around 30 million years ago. The duplicate genes form an array on the X chromosome, with additional duplicate copies of the M gene common in humans. The array is bounded on the upstream side by a so-called locus control region (LCR), the presence of which is critical for the expression of either gene. The spectral difference between the L and M pigments is largely determined by amino acid changes at only three sites (164, 261 and 269, Figure 1Figure 1).Red/green colour vision is much more variable in New World primates. Most New World species exhibit a trichromacy that is based on only two opsin genes, an autosomal SWS1 gene as in Old World primates, and a polymorphic X-linked LWS gene with multiple allelic forms that encode pigments with differing λmax values lying between about 535 and 565 nm. Platyrrhines thus lack the routine trichromacy of Old World primates, as male monkeys can combine the SWS1 gene with just one of the different allelic forms of the LWS X-linked gene and are therefore dichromats. In contrast, those females that inherit a different form of the LWS gene from each parent have the bonus of trichromatic vision, because X-inactivation will ensure that only one allele is expressed per cell.A major exception to this polymorphism-based trichromacy in New World primates is found in the howler monkey. In this species, separate L and M genes are present (Figure 4Figure 4), and expressed in separate cone populations with trichromacy present in both males and females. The duplication of the LWS gene differs from that in Old World primates and appears to be limited to the howler monkey, as it is not present in two closely related species, the spider monkey and the woolly monkey, which both possess a polymorphic LWS gene.Trichromatic colour vision in monkeys probably evolved from an ancestral dichromacy present within the arboreal environment of early primates, where the driving force was the ability to distinguish the redness of ripe fruits or reddish young leaves from a green background of foliage of highly variable luminance.Nevertheless, the complement of just three cone pigments in Old World monkeys may be considered somewhat limited in comparison to the complexity of cone pigments available to many lower vertebrates. The basic tetrachromatic system that evolved very early in vertebrate evolution has been adapted to a great range of photic environments, perhaps reaching its most advanced forms in diurnal birds and shallow water teleosts. In these species, spectral sensitivities range from the ultraviolet to the far red and in the case of some teleost fish, gene duplications have provided a wide palette of spectrally distinct pigments from which to differentially tune their colour vision.