The Evolution of Color Vision
Copyright © 1992-1997 by Mickey Rowe
ob Bales brought up an interesting topic in a recent post (well, it was recent when I started writing this). The topic is "evolution and color vision". Bob is apparently under some misconceptions either about color vision, or at least what evolutionary theory might predict about it. In a series of four posts beginning with this one, I want to ramble on and on about some of the background you might want to know if you were going to make some meaningful statements about evolution and color vision.
I'm going to start by describing a tiny fraction of what's well known about the molecular biology and biochemistry involved in visual transduction. If you're familiar with the topic, you may want to skip to the last couple of paragraphs in this post where I get to some data illuminating the evolutionary origins of the visual pigments. In followup posts I'm going to describe a bit of comparative psychology of color vision (to buttress the point that color vision systems are not all the same). In a third post I'm going to discuss some comparative anatomy, with a focus on the visual systems of mammals. I intend to demonstrate how comparative anatomy makes sense in light of what the fossil record tells us about the history of mammalian evolution. Finally, in a fourth post I will outline some of the steps that would be required in order for an organism to acquire color vision, with a discussion of how reasonable it is to suppose that such systems could evolve multiple times.
I no longer have access to Bob's post, but as I recall he was making some sort of statement that the distribution of current species which have color vision is at odds with what an evolutionary biologist would expect.
Let's dissect this claim with a little bit of thought and a look at some data. In the first place, I got the distinct impression from Bob's post that he thought "animals with color vision" should form a monophyletic group. This is absurd. In this context, saying that an animal has color vision is like saying an animal has a tail. Suggesting that two animals (say bees and humans) should be considered more closely related to each other than two others (say cats and humans) on the basis of the extent of their capacity for making color discriminations is similar to suggesting that two animals (say salamanders and lobsters) should be considered more closely related to each other than two others (say salamanders and frogs) just on the basis of which animals have tails. I'm not going to leave this discussion at this point, but I'll postpone the rest of it for my second post while I begin with some basics.
What does it mean to say that an animal has color vision? The term color vision is used in different contexts with somewhat different meanings, but from our own perspective of what it means to see in color, the best definition would go something like:
An animal has color vision if it has the capability of discriminating lights (scattered light as well as light sources) on the basis of the lights' spectral content, even when those lights are of equal subjective brightness.
The front end requirement for such a system is that the animal must have at least two different spectral classes of receptor, where each class is defined by the sensitivity of the receptor to light as a function of wavelength. This often leads to a looser definition of color vision: an animal is declared to have color vision if it has at least two spectral classes of photoreceptor operating at the same time.
Although there are a variety of ways in which different receptor classes could be constructed, it seems that extant organisms use only one.
The first step in the transduction of light energy to a neural signal is the light-induced isomerization (change of shape) of a chromophore, specifically a vitamin A derivative. Each chromophore is bound to a membrane protein called an opsin. The main function of the opsin is to change shape after light absorption triggers the isomerization of the chromophore: the opsin is an enzyme that is activated by the chromophore's isomerization. However, because of the linkage between the opsin and the chromophore, the opsin also serves to tune the wavelength dependence of the light induced isomerization reaction in the chromophore. That is, the chromophore's sensitivity to light at a given wavelength is established in part by the opsin--different opsins (i.e. opsins with different amino acid sequences) bound to identical chromophores will have different absorption probabilities at each wavelength. The result is that photoreceptors which express the gene for only one type of opsin will form a different class than photoreceptors that express a gene coding for a different opsin. Although there are other mechanisms that animals could use to differentiate photoreceptor classes (most notably some animals use more than one chromophore, and many vertebrates have colored oil droplets that screen individual receptors) it seems that the expression of only one of their possible opsin coding genes in each receptor is the mechanism that all animals use.
Now we have to throw in a slight wrinkle. In a vast majority of vertebrates, there are two different sets of photoreceptors, one that operates during the day and another that operates in the dark. Most people are probably familiar with the distinction between rods and cones--rods mediate night vision, cones day. At night when the number of photons around is low, visual systems don't go to such fancy lengths to discriminate the light's spectral content, so there is generally only one class of rod in any given animal (at least some frogs are exceptions to this rule). For all intents and purposes, none of us have color vision when we're dark adapted. Thus with respect to vertebrates, the discussion of photoreceptor classes above was more specifically a discussion of cone classes.
Here we'll get to some interesting stuff by looking at the opsins for which we have the most data. DNA and peptide sequences for various opsins have been determined. In 1990, all of the then known amino acid sequences were compared in order to infer a phylogeny for the opsin molecules. These sequenced proteins consisted of four different opsins from drosophila, one from octopus, four from human (one rod, three cone) and one rod opsin each from chicken, sheep, cow, and mouse. All of the opsins have similar sequences, but any good evolutionary biologist could tell you that some should be more similar to each other than to others. Would anybody like to draw their guess at the phylogeny determined for these thirteen proteins? (Hint, it appears that all opsins derive from a very ancient protein, since it has homologs in bacteria as well as in both invertebrates and vertebrates. (I've recently stumbled onto a reference that claims that vertebrate rhodopsin and bacteriorhodopsin are not part of the same gene family. I'll reserve judgement until I've read more than just the abstract of the paper. E-mail me if you would like to see the reference yourself.) Amongst vertebrates, the rod opsin seems to be the most conserved; cone opsins have arisen principally by duplication and subsequent mutation of the rod opsin gene.) Suffice it to say that these known opsins are not distributed in a mix and match fashion as one might guess a designer would have distributed them. If you'd like to see the phylogeny, you can look up the Goldsmith paper listed in the fourth post in this series. Alternatively I guess I could make an ASCII representation of it.
It should also be noted that many humans carry more than one copy of the middle wavelength-sensitive cone opsin. As this is grist for the evolution of color vision mill, we're literally ripe for the addition of a fourth cone class. (This probably won't happen, though, because people with a fourth cone class will be constantly trying to readjust the color on television sets. As a result of that such people will be highly selected against in bars the world over :-)
Since 1990, a few other opsins have been sequenced, specifically opsins from a variety of monkeys. I don't know as that they've been compared with the others, but I'm willing to predict where they should fit into the picture. It's nice to have a theory that lets you do that. (Since I wrote this last paragraph, I've seen another phylogeny that I think had more than twice as many opsin sequences as my best current reference. As far as I know, that work is still in press, and I no longer have access to it. From what I saw, though, the creationists have even more reason to fold their hand on this one now than they did two years ago...)
Prior to the advent of some nifty techniques in molecular biology, people had to use less direct methods of classifying photoreceptors. Among these methods are: direct measurement of the absorptive properties of individual receptors, measurement of the electrical responses of cells to monochromatic lights, and the conditioning of learned behaviors. Thus even without molecular biology, we knew (and know) a lot about the pigments underlying color vision systems.
Based on this sort of information, it's clear that most vertebrates have at least two cone classes. In fact, many birds, turtles and fish have four or five. Many invertebrates are similarly well endowed, and last I heard, the mantis shrimp was the winner of the contest of who has the largest number of photoreceptor classes. Given that coral reef animals and tropical birds often appear very colorful to us, it's not surprising that they have well developed systems of color vision. That different animals have different numbers of receptor classes already tells us that color vision systems are not all equivalent (as Bob might have us believe). If we restrict ourselves to animals which have the same number of receptor classes, might we expect that their color vision systems are equivalent?
The answer is a resounding no. Let's compare the color vision systems of two animals that both have three photopic (e.g. active under bright illumination) photoreceptor classes. One is the human, the other is the honey bee (specifically the worker--I don't know how the other castes are endowed). Does anybody here think that what a bee sees when it looks at a rainbow has the same appearance as what we see? We'll ignore optical polarization (which the bee is sensitive to and we're not) and focus on what we can infer about "color" based on, among other things, our knowledge of the bee's receptor classes. To begin with, at the inside of the rainbow where the violet-appearing light fades off to invisibility for us, the bee will still see more rainbow. On the outside, where we see red, the bee would see nothing for although bees have an ability to see what for us is UV, we have the ability to see what bees might call infrared.
Now picture that rainbow: what you see appears to have discrete bands of color. Don't for a minute think that those bands arise from there being anything discrete about the radiation emanating from that patch of sky. If you measured the radiation with a spectrophotometer, you'd find that the wavelength of maximum intensity as a function of the radial distance across the rainbow would decrease smoothly and monotonically from the outside to the inside of the bow. The apparent discreteness is an artifact of our photopigments (chromophore + opsin) and the neural processing of our photoreceptors' outputs. The bee too would probably see discrete bands (We can't ever really know how the world appears to a bee, but given what we can infer from doable experiments -- I actually chose the bee in part because its color vision has been studied about as much as any other animal's, excluding the human's -- the supposition that it would see discrete "color" bands from a rainbow is reasonable.) However, just as the outer and inner borders would be in different locations for us and bees (as described in the preceding paragraph), the borders of each "color" would be placed differently by the bee as well.
I can't claim that we have a good handle on why different animals have different visual pigments. There are some cases that are well understood--most notably it was predicted some 20 years before verification that marine fish that live just above the aphotic zone would have only one pigment, and that that one pigment would have a maximal sensitivity down around 450 nm (for us light at this wavelength would appear blue). It makes sense that if there isn't much light around, an animal's photoreceptors will be adapted to respond most strongly to the wavelengths of light most readily available. Bioluminescent fish and insects also tend to have pigments that are adapted for maximal sensitivity to the wavelengths of light emitted by their photophores (the molecules responsible for the emission of light e.g. from the abdomens of fireflies). The specifics of what selective advantage other pigments in other environments might convey are still somewhat mysterious (See the Lythgoe and Partridge paper listed in the fourth post of this series for a discussion of the topic).
One thing is clear, however. The best known predictor of what sort of pigments will be expressed by any given animal, is the pigments expressed by its nearest living relatives. To an evolutionary biologist this makes a lot of sense, of course.
There are a lot of other differences (or similarities) between manifestations of color vision systems in different animals. I've chosen to stick to a discussion of pigments here partly for simplicity, and partly because the straightforwardness of analyzing retinal receptors makes this the facet of color vision about which the most data is available. The point of this post is to say that it makes no sense to use the presence or absence of color vision in determining a phylogeny. If you want to be serious about asking what color vision and evolution have to say about each other, you have to ask specific questions about what sort of color vision different animals have.
In Bob's post, it was suggested that among mammals, color vision is more or less exclusive to primates. This isn't quite correct. In fact there are many other mammals with color vision. For example, diurnal squirrels and tree shrews have each been demonstrated to have at least two photoreceptor classes, and behavioral studies indicate that each meets the strict definition of color vision (the first definition in the first post of this series). Recent finds have also indicated that some rodents are sensitive to ultraviolet light, suggesting that they have a previously unknown class of photoreceptor. However, color vision systems do appear less frequently and with less complexity (i.e. with fewer photoreceptor classes) amongst species of mammals relative to species of most other classes of animal. To understand why this might be so, let's examine the history of mammalian evolution as evidenced by the fossil record, and conciliate that information with some comparative anatomy.
The lineage of animals which joins reptiles and mammals is often touted here as an excellent example of a transitional series. One detail that might seem surprising to people is that this transition occurred at the beginning of the Mesozoic era--the same time during which other reptiles were transitioning into dinosaurs. It's not quite right to say that mammals replaced dinosaurs at the beginning of the Cenozoic era, because mammals existed alongside of dinosaurs during the dinosaurs' entire "reign". However, during the Mesozoic era, dinosaurs and other reptilian cousins (e.g. pterosaurs, plesiosaurs and ichthyosaurs) were an extremely diverse group which occupied most of the available niches. The bush of life had only a small twig representing the lineages that would later branch out into all of the mammalian forms currently extant. Mesozoic mammals were small rodent-like creatures that were most probably nocturnal.
Note that the last paragraph is based only upon what we can glean from the fossil record. If current species arise from the descent with modification of pre-existing species, one might predict that the above inferred history of mammals would leave clues in contemporary mammalian anatomy. Oddly enough such clues exist.
You may recall from the first post in this series that pretty much all animals are "color-blind" in the dark. Consequently, if an animal is only active at night a color vision system would be of little use, much as eyes are of little use to cave fish, moles and other animals which live in the absence of light. So if modern mammals are just descendents of the animals whose fossilized remains are found in Mesozoic strata, you would expect that this would be reflected in the makeup of their retinas. Lo and behold, this expectation is born out quite well.
First off, comparative anatomy indicates that most mammals don't have well developed color vision systems not because their line didn't get around to developing it, but more likely because after our ancestors evolved color vision it became superfluous and was lost. The color vision of primates is not strictly homologous to the color vision of fish, birds, turtles, etc. Much of the machinery used for primate color vision arose independently long after similar systems developed (without being lost) in other vertebrate lineages. At this point the wary creationist might say, "Aha! So primate color vision doesn't fit into the mammalian scheme, and could be construed as evidence of a creator--in developing primates, the creator used a feature similar to what he'd used in those other so-called 'lineages'". I urge anyone who might think this to look more deeply into comparative anatomy. I will only briefly describe a few relevant features here.
Color vision is mediated by cones, so named because of the shape of the receptive part of the cells. If the history of mammalian evolution described above were correct, you would expect to find significant differences between mammalian cones and the cones of other vertebrates. (The initial definition of "cone" vs. "rod" photoreceptors has some kinks, because it is apparent (based on criteria other than the shape of the receptive part of the cell) that some photoreceptors that appear on first glance to be homologous are actually analogous. For example, the "rods" of nocturnal geckos (a type of lizard) are most likely homologous to the cones of other animals--geckos did the opposite of mammals. In their development, geckos went through a strictly diurnal phase, and hence lost some of the adaptations for nocturnal vision. They subsequently became nocturnal again, and thus their cones faced some of the same adaptive pressures faced by the rods of other vertebrates.) Whether or not you expect it, this is exactly what has been found. There are several features that are quite common to the cones of non-mammalian vertebrates, but that are completely lacking in mammals. (As most of you might guess, there are exceptions to the "complete lack" of the characters I'm about to describe. I'll leave it as an exercise to the reader as to which animals are exceptions. I'll tell anyone who guesses and provides with their guess a rationale for why they guessed what they did. That is, if you understand and accept evolution, you would predict that if there are exceptions, they will be found in particular animals. If you don't understand or don't accept descent with modification as the origin of current species, I really would like to know what sort of reasoning you might use to guess at the exceptions.)
Many vertebrates have oil droplets at the bases of the light sensitive parts of their photoreceptors. These oil droplets often have pigments in them that absorb (i.e. filter out) some of the light that would otherwise stimulate the cell. What this does is to modify the spectral sensitivity of the photoreceptor bearing that droplet. This feature is not found in mammals.
Many vertebrates have double cones--two cones that are joined along their long axes by tight junctions, gap junctions or both. Nearly all classes of vertebrates have some variety of this form of receptor in their retinas. This feature is not found in mammals.
The photoreceptors of many vertebrates perform a sort of circadian dance. During the day, the rods are extended on long stalks so that their sensitive parts are buried in a layer of pigmented epithelium. This epithelium shields the rods so that very little light reaches them from the sides, and the cones basically shield them from axially propagating light. At night the cones are extended out into the pigmented epithelium, and the rods are contracted back to where the cones were during the day. This feature is not found in mammals.
The conclusion that might be drawn from the above is that there are many features of ancestral retinal anatomy that were retained in most classes of vertebrates, but lost in mammals. Elaborate color vision is just one such feature. The phylogenies of the opsin molecules that I discussed in the first post of this series suggest that mammals have always retained two cone pigments (a survey in 1981 indicated that there aren't any vertebrates with only one cone pigment), but any mammals that, like us, have more than two pigments (re)gained the third relatively recently (for us probably around 63 million years ago). [For those from sci.bio, this was why I was suggesting that squirrels might be trichromatic--I'm not willing to climb out on that limb now. Our short wave-sensitive or "blue" cone is probably homologous to the UV cone of other (i.e. non-squirrel) rodents. One of the inferred pigments in the dichromatic squirrels has about the same absorption spectrum as our short wave cone, so there isn't any reason to suppose that the squirrel has a third. That is, it is reasonable to conclude on current evidence that the UV sensitive rodents have the same cone classes as the squirrels, only their short wave pigment has been shifted to absorb even shorter wavelengths than those of most other mammals.]
How to See Red
In this final segment I'd like to address some of the probable steps required in the formation of a color vision system. I do this in an attempt to circumvent an argument via lack of imagination about the improbability of such a system arising more than once. The generation or elaboration of color vision systems is not a terribly complicated process (at least at the periphery).
Let's presume that we're starting with an organism that already has an eye of some sort. The first step towards a color vision system is the need for at least two visual pigments. It should be obvious that the addition of a pigment would be of immediate advantage even if the new pigment was expressed in the same cells as the older pigment(s). The reason is that there are some wavelengths of light where the new pigment will respond more strongly than the old, so the addition of a pigment will increase the animal's sensitivity over those wavelengths.
The next step (conceptually anyways--it may be that this and the first step typically occur simultaneously) is the sequestration of the new pigment into a discrete population of photoreceptors. (By discrete, I don't mean spatially. I just mean that each photoreceptor should express only one opsin.) The advantage that this provides comes in the form of visual contrast. The lowest level of visual information processing is the recognition that something is different about a given region of space--i.e. that there is food or a predator "over there". To perform this function in habitats that are rich in light of particular wavelengths (the short wave "blues" underwater, or the mid wave "greens" of the tropical rainforest) it's best to have at least two pigments, one matched to the dominant wavelengths and one offset from those wavelengths. With the matched pigment, non-reflective objects have high contrast as dark areas on a bright background. With the offset pigment, reflective objects will apear bright against a darker background. Except in some extreme conditions (i.e. just above the aphotic zone for marine environments) the background probably isn't constant enough for that simplistic analysis to hold, but it's easy to imagine that if an animal has more photoreceptor classes it has a greater chance that one of them will allow for the visibility of a given target under a given set of background conditions.
(Note that it's not yet clear how the expression of photopigments is regulated in individual cells, but because of its accessibility, the retina is frequently used in studies of developmental neuroanatomy. Experiments with transgenic animals have already given us some key pieces of information about the regulatory mechanisms that determine what sort of photoreceptor a retinal precursor cell will become. Immuno- histochemistry has also been used to show that the fate of a cell, i.e. what sort of cell it will become, is established long before morphological differentiation is apparent. This is a hot area where the rest of this century is sure to see incredible advances in our knowledge base.)
The next step is the development of neural wiring in the retina that segregates the signals from one population of cells from those of the other(s). (Oddly enough this isn't necessary for the previous advantage, although as I'll describe below, there is good reason to suppose that these two steps occur simultaneously as a result of the mechanisms of neural development.) The advantage of this is that it allows the animal's retina to "draw" contours around an object (i.e. to place "color" boundaries on the visual scene).
The last phase in the development of color vision is the arrangement of wiring in the brain that allows an animal to segregate and classify objects according to their "color" (i.e. according to how well the object stimulates the different receptor classes). The advantage of this adaptation is that it allows the animal to classify objects according to "color". For example, it has been argued (although to me this is a just so story and may not be correct) that color vision and the expression of pigments in fruit co-evolved. That is, it is to the plants' advantage to have its fruit remain un-eaten until the seeds are ready for dispersal, so the color change in ripening fruit is a signal that the plants are sending to the animals. In turn the animal gets the greatest benefit from eating the ripened fruit, so it is to the animals' advantage to recognize when the fruit is ripe. The sort of comparison necessary for discriminating ripe from unripe fruit is easy if, for example, objects which reflect a lot more long than short wavelength visible radiation bring about a particular quality of sensation (e.g. what we call "red").
The point of the above was to make explicit that even if an animal were to develop color vision in steps, it's not hard to imagine a sequence of steps in which each step confers some advantage which would cause that step to be selected for. However, there's a beauty in the way that nervous systems are constructed which might lead you to expect that rudimentary color vision can arise in a "color blind" animal in only one or two steps.
The addition of a new pigment arises from a gene duplication followed by mutation of one (or both) of the copies. As indicated in the first part of this series, it seems pretty clear from gene sequence data that this is exactly how new pigments have arisen in us, fruit flies and a couple of other primates. By inference it seems likely that this is a widespread occurrence.
I'll end now with a brief foray into neurobiology. Animal nervous systems, particularly the nervous systems of vertebrates are not "hard-wired" at birth (or hatch or the end of metamorphosis...). Decisions about which nerve cells should be connected to which other nerve cells are made during a long space of time prior to adulthood, and in some animals (though usually to a much more limited extent) even during adulthood. Genetics seem to specify (in unknown ways) some of the gross features of connectivity--for example in mammals the axons of ganglion cells in the eye mostly grow through the optic nerve to a particular group of cells in the thalamus. However, the fine distinctions about, for instance, which ganglion cells connect to which cells in the thalamus are made initially by the formation of a lot of random connections. Many of these connections are then pruned back so that each ganglion cell stimulates only a small subset of the cells it initially connected with. The "rules" governing the pruning back are largely based on correlations in the activity of different cells--if two cells in the retina are generally active at the same time, then they will probably end up being connected to the same cells in the thalamus.
This activity-dependent pruning of connections appears to be the way that "maps" are created in higher brain areas. The best indicator of whether or not two cells in the retina will be simultaneously active, is how close they are to each other in space. Cells in the thalamus thus form a map of cells in the retina according to their activity, and hence their connectivity. Now it's easy to imagine that another determinant of whether or not two cells will be active at the same time is whether or not they are connected to cells which express the same pigment (within the retina, the same rules are followed in the creation of connections, so ganglion cells will preferentially be connected to cells which express the same pigment). So in the thalamus and other brain regions, there will be maps of the different receptor types within the maps of retinal location.
Of course neural development is a lot more complicated than I've described here, but the take home message is that the way that nervous systems develop in growing animals makes it easy to incorporate changes at the periphery. It has to be that way, or our nervous systems would not be able to cope with changes which occur in our muscles and sense organs as a result of growth.
If I've been at all clear, you'll see that once an animal has different photoreceptor classes the rest of the nervous system is already prepared to take advantage of them. An interesting case study in this regard is new world monkeys. In at least one species, two of their opsin genes are (like our mid- and long- wave sensitive opsins) on the X chromosome. The monkeys' expression patterns are different from ours, however, and it turns out that for one (or two depending on how you think about it) class of photoreceptor, the females can express the genes on each X chromosome. The males naturally only have one X chromosome. In the population, there are two types of male (depending on which allele they have on their X chromosome), and three types of female (depending on whether they are heterozygous, or homozygous for one or the other allele). The monkeys' developing nervous systems seem to take advantage of whatever photoreceptor classes happen to be out there in that animal's retina.
I'm sure I've left a lot of things unclear, but if anyone wants to find out more, I can recommend a few references. A good general source for information about neurobiology, with several chapters on vision is:
Principles of Neural Science 3rd Edition, edited by Eric R. Kandel, James H. Schwartz, Thomas M. Jessell, Elsevier, New York, 1991.
An excellent book that treats the principles necessary for appreciating comparative studies of visual systems is:
Lythgoe, J. N. (1979). The Ecology of Vision, Oxford University Press, Oxford (and also Clarendon Press, New York).
After reading that, you'll probably be prepared for:
Jacobs, G.H. (1981). Comparative Color Vision, Academic Press, New York.
and a few papers:
Goldsmith, T.H. (1990). "Optimization, Constraint, and History in the Evolution of Eyes", Quarterly Review of Biology, 65(3):281-322.
McFarland, W.N. and Munz, F.W. (1975). "The Evolution of Photopic Visual Pigments in Fishes", Vision Research, 15:1071-1080.
Hemila, S., Reuter, T. and Virtanen, K. (1976). "The Evolution of Colour-Opponent Neurons and Colour Vision", Vision Research, 16:1359-1362.
Lythgoe, J.N., and Partridge, J.C. (1989). "Visual Pigments and the Acquisition of Visual Information", Journal of Experimental Biology, 146:1-20.
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