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wavelength (nm) C

Figure 14-3. Continued wavelength (nm) C

Figure 14-3. Continued combinations of opsins and filtering pigments that allow for six classes of spectral peak sensitivities (Pichaud, Briscoe et al. 1999).

Opsins responding to similar light frequencies are typically closely related in protein structure and, presumably, evolutionary history (Figure 14-3A) (Yokoyama 2000). However, through gene duplication, a number of cone opsins evolved, and today there is great variety among vertebrates and invertebrates in their cone and rod cell arrangements, relative number, type number, and wiring to the central nervous system. Both vertebrate and invertebrate opsin sequence relationships suggest that rhodopsin evolved from green-sensitive ancestry.

Many amino acids vary among opsins, but a relatively small number of key amino acids appear to account for most of the variation in spectral sensitivity, at least in the repeated evolution of red-green sensitivity differences that have been studied in detail (Yokoyama 2000;Yokoyama and Yokoyama 2000). Current reconstructions based on teleost fish, amphibian, reptile, bird, and mammalian data suggest that the ancestral vertebrate had five opsins, rhodopsin plus four cone types, probably indicating tetrachromatic vision (Bowmaker 1998). The latter include, opsins sensitive to red, green, blue, and ultraviolet parts of the spectrum, along with a pineal opsin (see below) (Bowmaker 1998; Yokoyama 2000; Yokoyama and Yokoyama 2000). The gene phylogeny suggests that only the long (red-green) and the shortest (blue) wavelength opsins were present in stem mammals, giving them dichromatic vision, with a relative sparseness of cones in their retinas that may indicate that their early evolution was as nocturnal species. Invertebrates have rhodopsin-green and blue-UV gene classes and may only have had the two in their stem ancestors. Clearly, terms such as "tetrachromatic" are misnomers in that with four different peak sensitivities the organism can actually parse a wide range of colors, not just the four—just as we can see the entire color range with our three (red, blue, green) opsins.

For foraging and social signaling, some vertebrates such as birds use UV light as well as the broad spectrum of visible light. This is a potentially important fact in assessing the value of protective coloration as an adaptation against bird predation because the usual hypotheses have been based on what human investigators can see. A famous example is the case of industrial melanism, in which the rapid evolution of protection in peppered moths was said to have occurred because moths that matched the color of lichens on tree trunks on which the moths rested were not seen (or eaten!) by bird predators. Visible moths were eaten, and their unfortunate wing-color alleles disappeared along with them. However, the UV sensitivity of bird vision may have rendered moths less effectively disguised than they appear to our human eyes (Grant 1999; Weiss 2002c).

In the retina, cones tend to cluster in hexagonal groupings, surrounded by rods, but with a greater overall concentration of cones near the center and of rods near the periphery of the retina. Rod cells predominate in vertebrates that live in dim light. Interestingly, it appears that a given cone cell as a rule expresses only one type of opsin, although this may be less tightly regulated in species other than primates (Wang et al. 1999). Some primates, including humans, have two closely linked opsins on their X chromosome, that arose by gene duplication. Today, these respond to red and green ranges of the spectrum. The expression of only a single gene in a cluster is another example of cis allelic exclusion previously seen in immune, globin, and olfactory genes. Which of the tandem X-linked opsin genes is expressed in a given cone cell may involve competitive binding of regulatory proteins (Wang, Smallwood et al. 1999). This selection occurs probabilistically, so that both genes are expressed in sufficient numbers of cone cells.

X-inactivation in females ensures that only one chromosome's genes are used for red and green in any given cell and introduces some variation between each retina and among areas within the same retina. Exclusion does not occur in blue cones, which express both copies of the gene (blue opsin is autosomal and hence diploid). How blue vs. red-green trans exclusion occurs so that a given cone expresses only one or the other, when the two are on different chromosomes, is not known. In fact, some species do express both blue and green opsins in the same receptor cell (Glosmann and Ahnelt 2002).

Other genes are involved in a variety of "nonvisual" animal light perception phenomena. Among these are light-sensitive melanopsins found in frog skin and mammal retinal ganglia, which help regulate circadian (day-night) rhythm and pupil reflex and others. These genes are widespread in nature, and at least some are part of the opsin gene family. However, melanopsins in vertebrates appear more closely related to those in their invertebrate relatives; for example, in situ, their chro-mophore conformation is reversible and does not require helper cells as in vertebrate retinal photoreceptors. Vertebrates use genes in the P (pineal) subgroup to regulate diurnal cycling mechanism through the retinohypothalamic tract. A net of melanopsin-expressing cells in the inner mammalian retina may serve this function independent of the outer retinal photoreceptor cells (rods and cones) (e.g., Grant 1999; Provencio et al. 2000; Provencio et al. 2002). Blind subterranean mole rats appear to use this mechanism for circadian rhythms despite having degenerate eyes (Hannibal et al. 2002). Blind humans and experimentally blinded rodents may retain light-responsive nonvisual functionality. Insects with eyes removed can also perceive light intensity through a rudimentary "dermal" light sense (Steven 1963).

The Evolution of Color Vision

It is tempting to relate color sensitivities to aspects of the environment that may have provided the adaptive darwinian basis of organisms by selection; environmental lighting conditions, the color of food sources, mates and conspecifics, and the like have been suggested as the selective forces (e.g., Mollon 1989; Treisman 1999; Yokoyama 2000). For example, vertebrates living in dim light often mainly have long-wave (blue) sensitive cone pigments as well as rods. Selection based on visual cues, both to favor seeing ability and to favor being seen or not, depending on the circumstances, can be strong and rapid. Adaptation to wavelength sensitivity is often referred to as spectral "tuning" by natural selection (we also saw this notion in regard to olfaction). It is, however, more difficult to evaluate specifically the range and nature of what an organism can actually see, than to evaluate the specific nature of an opsin protein.

The tandem nature of human red and green pigment genes provides an interesting test case in regard to color vision. A male has only a single X, and all red- or green-expressing opsins use the respective alleles on that single chromosome. Because of X-inactivation, even a female, who has two X chromosomes, will only express one of her two red or green opsins in any given cone. This adds an element of stochastic variation among females (and between the left and right eyes of a given female) in their red-green sensitivity. Generally, this has subtle effects at most.

Mutant opsins are reasonably common. Because blue opsin is autosomal (chromosome 7), both males and females have two copies of the blue opsin, and blue color blindness is rare in either sex: even if one allele is defective, the chances are small that the other will be as well. However, red or green color blindness is not unusual in males; they only have a single red and green opsin, so that if either gene is defective there is no normal allele to "cover" for it. It is relatively unlikely that a female will inherit two dysfunctional red or green opsins. (In Hardy-Weinberg terms, if p is the defective allele frequency, her chance of having two such alleles is p2, typically a very small value, and similar to the situation for the autosomal blue opsin. Even though a female only expresses genes from one of her X chromosomes in any specific retinal cell, roughly half of her cones will express her functional allele. This may affect her color sensitivity somewhat, but she will not be color blind.). By contrast, a fraction p of males will inherit the defective allele, but having only that single X have no covering protection.

Color blindness is considered a kind of disorder but that is a human subjective judgment. There is generally considerable variation in the color sensitivities of opsins. The red and green opsin genes are closely linked, and mutation, recombination, and/or inaccurate replication produces a variety of copied, disrupted, or fused opsins, with substantial variation in the resulting peak sensitivities that can be explained by the nature of the mutation (Figure 14-4) (Neitz et al. 1996; Neitz et al.

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