Evolution and spectral tuning of visual pigments in birds and mammals

Abstract

Variation in the types and spectral characteristics of visual pigments is a common mechanism for the adaptation of the vertebrate visual system to prevailing light conditions. The extent of this diversity in mammals and birds is discussed in detail in this review, alongside an in-depth consideration of the molecular changes involved. In mammals, a nocturnal stage in early evolution is thought to underlie the reduction in the number of classes of cone visual pigment genes from four to only two, with the secondary loss of one of these genes in many monochromatic nocturnal and marine species. The trichromacy seen in many primates arises from either a polymorphism or duplication of one of these genes. In contrast, birds have retained the four ancestral cone visual pigment genes, with a generally conserved expression in either single or double cone classes. The loss of sensitivity to ultraviolet (UV) irradiation is a feature of both mammalian and avian visual evolution, with UV sensitivity retained among mammals by only a subset of rodents and marsupials. Where it is found in birds, it is not ancestral but newly acquired.

Figure 1.

Retention and loss of rod and cone opsin classes in mammals. The origin of the L and M variants of the LWS gene in Old World primates and one species of New World primate by gene duplication is shown.

Figure 2.

Schematic of a visual pigment molecule showing the arrangement of helices around the chromophore retinal. The numbering is based on mammalian rod opsin. Lysine 296 (yellow) is the binding site of retinal, and glutamate 113 (yellow) provides the SB counterion. Adjacent residues within the helices are identified by linking lines. All sites mentioned in the text are numbered and colour coded with opsin class: LWS, red; RH2, green; SWS2, blue; SWS1, violet; RH1, black. Split colours indicate sites involved in tuning in more than one opsin class. Note how sites tend to cluster around either the SB linkage or the ionone ring of retinal. TM, transmembrane; CL, cytoplasmic loop; EC, extracellular loop.

Figure 3.

Absorbance difference spectra for in vitro regenerated wild-type and mutant SWS1 pigments. Note that substitution at site 86 is sufficient to shift the bovine VS pigment into the UV (a) and the UVS goldfish pigment into the violet region (b). Adapted from Cowing et al. (2002b).

Figure 4.

Mammalian phylogeny showing the presence of UVS and VS SWS1 pigments. Violet lines indicate the retention of UV sensitivity and blue lines a shift to violet sensitivity. The evolutionary position of substitutions at site 86 is indicated by their placement on the tree. Note that except for the primates, the retention of Phe86 is always associated with the retention of UV sensitivity. Dagger symbol denotes pseudogene.

Figure 5.

Schematic of the complement of single and double cone and rod photoreceptors in the avian retina as exemplified by many diurnal passerine species. Depending on the species, the SWS1 pigments have λ_max values either in the UV (360–380 nm) or in the violet (400–420 nm) region of the spectrum. Modified and redrawn from Bowmaker (2008).

Figure 6.

Phylogenetic relationships showing the presence of VS and UVS SWS1 pigments in avian species so far examined. Blue lines are lineages with VS pigments and violet lines with UVS pigments. The ancestral avian VS pigment was most probably Ser86 and Ser90. Substitutions at these sites are shown on the respective branches. Re-drawn from Hunt et al. (2007).