Evolution of colour vision in mammals

Abstract

Colour vision allows animals to reliably distinguish differences in the distributions of spectral energies reaching the eye. Although not universal, a capacity for colour vision is sufficiently widespread across the animal kingdom to provide prima facie evidence of its importance as a tool for analysing and interpreting the visual environment. The basic biological mechanisms on which vertebrate colour vision ultimately rests, the cone opsin genes and the photopigments they specify, are highly conserved. Within that constraint, however, the utilization of these basic elements varies in striking ways in that they appear, disappear and emerge in altered form during the course of evolution. These changes, along with other alterations in the visual system, have led to profound variations in the nature and salience of colour vision among the vertebrates. This article concerns the evolution of colour vision among the mammals, viewing that process in the context of relevant biological mechanisms, of variations in mammalian colour vision, and of the utility of colour vision.

Figure 1.

Vertebrate photopigment opsins are products of five opsin gene families (top). In each of these families, gene sequence variations yield photopigments whose λ_max values are drawn from the spectral ranges indicated by the extent of the horizontal lines. The ranges shown are those appropriate for pigments constructed using an 11-cis-retinal chromophore. All of the cone photopigments of eutherian mammals come from two of these gene families, SWS1 and LWS. It can be inferred from gene sequence comparisons that the two types of cone photopigments found in ancestral members of this group had spectral sensitivities given by the curves at the bottom.

Figure 2.

A vertebrate phylogeny illustrating the distribution of the four cone opsin gene families. All four families (SWS1, SWS2, Rh2, LWS) originated early in vertebrate evolution. Of contemporary mammals, monotremes have opsins drawn from the SWS2 and LWS families; these animals also have a non-functional SWS1 opsin gene (asterisk). All eutherian cone pigments are drawn from two families—SWS1 and LWS. Contemporary marsupials have gene representatives from the SWS1 and LWS families and, possibly, from the Rh2 gene family. See the text for further discussion.

Figure 3.

Variations in primate cone photopigment arrangements. (a) All catarrhine primates and the platyrrhine howler monkey have three classes of cone pigments that support trichromatic colour vision. (b) Many platyrrhine monkeys have polymorphic colour vision in which all male monkeys and homozygous females get any of three M/L-cone pigments (dashed lines) which in conjunction with the S pigment supports dichromatic colour vision. Female platyrrhine monkeys that are heterozygous have any pair of the M/L pigments and they are trichromatic. (c) The platyrrhine Aotus monkey and a number of strepsirrhine primates have only a single cone photopigment and thus lack a colour vision capacity. (d) Some strepsirrhine monkeys have two types of cone photopigment and dichromatic colour vision.