Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision

Abstract

This review outlines how eyes of terrestrial vertebrates and insects meet the competing requirements of coding both spatial and spectral information. There is no unique solution to this problem. Thus, mammals and honeybees use their long-wavelength receptors for both achromatic (luminance) and colour vision, whereas flies and birds probably use separate sets of photoreceptors for the two purposes. In particular, we look at spectral tuning and diversification among 'long-wavelength' receptors (sensitivity maxima at greater than 500 nm), which play a primary role in luminance vision. Data on spectral sensitivities and phylogeny of visual photopigments can be incorporated into theoretical models to suggest how eyes are adapted to coding natural stimuli. Models indicate, for example, that animal colour vision--involving five or fewer broadly tuned receptors--is well matched to most natural spectra. We can also predict that the particular objects of interest and signal-to-noise ratios will affect the optimal eye design. Nonetheless, it remains difficult to account for the adaptive significance of features such as co-expression of photopigments in single receptors, variation in spectral sensitivities of mammalian L-cone pigments and the diversification of long-wavelength receptors that has occurred in several terrestrial lineages.

Figure 1

Vertebrate cone and insect photoreceptor spectral sensitivities, normalized to λ_max. (a), (b) Humans and honeybees have three spectral types of photoreceptor, and trichromatic colour vision. Human M and L cones, and the bee's long-wavelength receptor also provide luminance signals. (c), (d) In birds and flies, respectively, the double cone (D) and short visual fibre (SVF) signals are used for luminance, while the bird's four types of single cone and the fly's long visual fibres (LVFs) give chromatic signals. The fly photoreceptors are named according to their location in the rhabdom (R7 or R8), and by their colour pale (p) or yellow (y). The five types of fly receptor illustrated are found across most of the eye, but in specialized regions are replaced by others (Hardie 1986). Vertebrate and bee visual photoreceptors contain only a single type of photopigment, but flies also have a UV sensitive antennal pigment, which accounts for their complex spectral sensitivity (Hardie 1986; Stavenga 2004).

Figure 2

(a) Illumination spectrum of standard daylight in quantum units. Illumination spectra contain differing proportions of direct sunlight, blue skylight, and light filtered through leaves, which resembles the leaf reflectance spectrum. (b) Here, illustrated by the average from a large sample of rainforest species. Leaf spectra peak at 555 nm, and increase sharply beyond 680 nm. (c) Dependence of quantum catch on the wavelength position of the photopigment containing A1 pigments. A2 pigments, which can peak at up to 620 nm, give very similar curves. Illumination is assumed to be either standard D65 daylight (ca figure 2a) or forest light. Calculations assume the receptor views a surface whose reflectance is uniform across the spectrum, and that the absorption at the peak does not depend on λ_max. Forest light is assumed to be the product of D65 illumination with the reflectance of leaves, which is an extreme green light. Quantum catch is normalized to that for a receptor peaking at 645 nm. The quantum catch in forest light increases sharply at the peak wavelengths greater than 600 nm. Ordinarily visual pigments contain a vitamin A1 chromophore (or in some insects, a chromophore based on xanthophylls; Hardie 1986), which allow λ_max to reach about 570 nm. However, the lizards use vitamin A2 as a chromophore (Provencio et al. 1992), which gives an LWS pigment with λ_max 620 nm. A2 pigments are common in fishes and it unclear why they are rare in amniotes.

Figure 3

Effects of mixing long- (L) and short- (S) wavelength sensitive pigments on quantum catch. Dependence of the quantum catch on the ratio L : S in a cone containing a mixture of an L pigment peaking at 565 nm and an S pigment peaking at 435 nm. Calculations are for two optical densities. The solid line corresponds to a receptor with a peak absorptance of 0.4, and the dashed line a peak absorptance of 0.99. This shows that even for very long receptors (with high optical density), the quantum catch for a cone containing only L pigment exceeds that for a receptor with a mixture of visual pigments.