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.

Ultraviolet-sensitive vision in long-lived birds

“…In the four Orders containing species with UVS pigments (Passeriformes, Struthioniformes, Ciconiiformes, Psittaciformes), some species have VS rather than UVS pigments, but this is not found in the Psittaciformes where both the species (budgerigar; African grey) examined so far have UVS pigments. The molecular mechanism for the generation of UVS pigments differs in non-avian vertebrates [11], thereby reinforcing the conclusion that avian UVS pigments have a separate and more recent origin [17].…”

“…Cone photoreceptors contain coloured oil droplets in the distal regions of their inner segments that are spectrally matched to the visual pigment and act to absorb all wavelengths shorter than a droplet-specific cut-off wavelength [10,11]; short wavelength absorption in the single cones arises from carotenoids, the concentration of which is resistant to dietary manipulation [12]. In all species, the short wavelength-sensitive visual pigment is specified by the short wavelength-sensitive type 1 (SWS1) gene class; the ancestral form of this gene almost certainly specified a UVS pigment with peak sensitivity (l max ) below 390 nm [2].…”

Mapping behavioural evolution onto brain evolution: the strategic roles of conserved organization in individuals and species

“…Vertebrate colour vision contrasts the output of two to five very broadly tuned photoreceptors that cover the visible spectrum to code the reflectance characteristics of objects and environments with relative independence from the spectrum of light illuminating them. A typical mammal has two photopigments for diurnal vision (opsins), and most anthropoid primates have three [7][8][9]. The opsin molecule, composed of amino acids, is a rough cylinder to which a short-chain molecule, 11-cis retinal, is attached, like a tab on a cola can.…”

What is comparable in comparative cognition?

“…For example, red sensitivity has evolved several times in insect colour vision [43], and in Lepidoptera this has repeatedly occurred by gene duplication of a 'green' sensitive opsin and subsequent spectral sensitivity shift to longer wavelengths by the same amino acid substitutions [44]. Numerous vertebrate lineages also show adaptive duplications or losses of visual pigment genes, as well as more subtle spectral tuning of their protein products via (sometimes parallel) amino acid substitutions [45][46][47]. In mammals, at least, the nervous systems appears well-preconfigured to instantly add a novel sensory dimension to its perception without evolutionary lag-time to adjust postreceptor neural circuitry [48], perhaps by means of general purpose decorrelation mechanisms [49].…”