In a recent comment, a reader of this blog had highlighted some concerns regarding an evolutionary trajectory of color vision evolution that I had proposed in conjunction with the evolution of color terms in human languages and as a possible explanation for the linguistic trend. At that time, I had proposed a possible evolutionary scenario, without doing due diligence investigation of existing evolutionary theories of color vision, as my post had more of a linguistic and developmental focus and the evolutionary conjecture was just that- a conjecture, which, if found true, would lend more credence to my linguistic trend. Thanks to Andreas, I reviewed the literature on color vision evolution and was surprised to find some support for my theorization.
Before I discuss the color vision evolution, I'll strongly recommended reading two posts on the evolution of color vision and the evolution of retinal structures (more Avian focus here) , for getting some basic familiarities with the retinal structures involved in color vision and how they might have evolved.
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.
The above succinctly defines what we usually mean by color vision. You can either have a dichromatic color vision, when you have two differently tuned receptors to detect different light wavelengths and the different signal combinations from these receptors yield different hues; or you can have trichroimatic / tetrachromatic vision where three/four independent color signals are combined to yield an entire Hue range. One familiar with the RGB color system used in computers, would note that it is based on the assumption of 3 pure colors, which can be mixed in different amounts to yield most of the color hues we see on the monitor.Pigeons, and birds in general, have a tetrachromatic color vision.
Now for some basic visual circuitry:
The retinal structures involved in vision, in mammals, are, pohotorecptors (classified as cones and rods), horizontal, bipolar, amaracine and ganglion cells.
However, for all vertebrates (mammals as well as reptiles and birds) and invertebrates as well, the receptor mechanism is conserved and is basically the same and we will discuss that first:
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.
The above clarifies, that in mammals, we associate color vision with cones or specialized photoreceptors that contain a single pigment and are responsive to a single wavelength range. In reptiles, we also have double cones, wherein, two photopigment/ receptors are part of the same cell and then there are other mechanism like oil droplets that are also involved in color vision (but thankfully not in mammals). Rods are also a type of receptors, tuned to a frequency, but we normally do not associate rods with color vision, because they are usually used for night vision and their signals are not combined to create the color hue; yet a limited form of monochromatic color vision is possible by having a combination of one rod and one cone receptor types.
Next we need to differentiate between the rhabodermic eyes of invertebrates (based on r-opsin and the ciliary eyes of vertebrates based on c-opsins. Pharyngula does an excellent job here.
Eyes can be further categorized as rhabdomeric or ciliary by the nature of the cellular elements that make up the photoreceptors, by the kind of opsin molecule used to transduce the light signal, and by the signaling pathway used to convert a conformation change of the opsin molecule into a change in the electrical potential across the cell membrane.
As many accounts of color vision evolution focus on the phylogentic tress of opsin genes evolution to make their case, it is important to distinguish between the levels of analysis. All the known Opsin genes can be classifies in seven sub-families: two of these the r-opsin families and the c-opsin families are pertinent to, and expressed in, the photorecptors found in invertebrates and vertebrates respectively.
Thus, if one wants to focus on mammal color vision evolution, one needs to focus on c-opsins mostly. Many studies have been conducted over these and the phylogentic data indicates that the vertebrate opsins too form a neat tree with five sub-families relevant for (color) vision and 3 other sub-families having non-visual functions.
Thus, in mammals we have a five types of opsins : one rhodopsin-type and expressed in rods, and four other chromatic types (detecting Red, Blue, Green and U/V colors) and expressed in cones.
One should pause here and note that the human S(short) or blue receptor actually belongs to the U/V (S) family; while the human L (red) and M (green) receptors both belong to the Red (L) family.
These 5 opsin families (Red, Gree, Blue, U/V and Rhodipsin)have been variously characterized as (L, ML, MS, S and Rh) or as(RH1, RH2, LWS, SWS1 and SWS2).
With this background, information, we can now go straight to the heart of the problem: the evolutionary trajectory of these different receptors / opsins and how the color vision evolved in humans. I'll limit the discussion here to mammals first and then to primates , as my original thesis that color terms evolution follows the color vision evolution requires the analysis to happen only in that time frame in which linguistic abilities make sense. Assuming some proto-language in Apes and primates, it is reasonable to expect that whatever sequence of color terms we see in languages, would reflect the successive levels of color vision as experienced by Primates, and would be independent of how color was perceived in invertebrates. (I'm sure no one contends that the color terms of human languages should capture the early chromatic experiences of invertebrates).
Although I do not buy the bottleneck theory of Mammal evolution -stock, barrel and lock - I believe we can take that as a reasonable starting point. It posits that mammals were reduced to being a nocturnal burrowing species during the age pf the dinosaurs and thus were reduced to having just the rods, and lost the earlier, cones, double cones and oil pigments that reptiles still have. In any case, in mammals, rods seem to be older and more conserved than cones. (Pat on the back: one claim originally made defended to satisfaction!!)
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.
Which of the two primary classes, rods or cones, is the ancestral photoreceptor? Given the tremendous variation seen photoreceptors across vertebrate and invertebrate species, this in not an easy question to answer based on simple phylogenetic assumptions. In addition, it is often difficult to clearly distinguish certain rod and cone types from each other, or classify them into one or the other category. Rods appear to be relatively more conserved in vertebrates in terms of pigments and structure than cones, and therefore could be considered the more ancestral form. However, rods in some respects are more morphologically complex than cones, having developed extreme sensitivity (capable of detecting as little as one photon of light).
Now,coming to the evolution(or re-evolution) of the cones or the chromatic system in mammals, it is instructive to pause here and note that having three cones does not necessarily mean that the two species will have the same qualia of color hues.
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.
Also, it is instructive to note here how a higher level chromatic vision (dichromatic for instance) may arise form a lower level chromatic vision (monochromatic in this example). Although, along with the photoreceptors, we will need additional supporting neural wiring, in both the retina and the brain, for the opponent-processing mediated color perception to take place, we will restrict the discussion to the emergence of a new photoreceptor.
A new photoreceptor, may come into existence by a duplication and polymorphisms of an existing receptor (opsin) gene. The new receptor would have a slightly different frequency sensitivity than the original receptor and, by selectively expressing these two genes in different receptors, we can have two types of receptors. By processing and combining the two types of signals, one can now get dichromatic vision, from the original monochromatic vision.
Much confusion, in primate color vision evolution, depends on the fact that one takes as base the other mammals like dogs, and their blue-yellow world as a baseline from where to start. It should be emphasized that even though dogs may currently have two receptors, tuned to detect blue and yellow, we cannot conclude form that anything about humans or ancient ancestral mammals. In the human ancestry lineage, the dichromatic phase may have involved Red-Green perception. This is evident form the bee-human trichromatic example given above.
A very good paper summarizing the latest research on primate color evolution concludes that their are five types of primate color vision systems- beginning with a Monochromatic (L opsin only)_ system in nocturnal primates to a S + M+L (multiple copies) trichromatic system in humans.
It is interesting to note here that the human Green evolved, by replication and polymerization of the Red opsin present on the X chromosome. From the hierarchy of primate color systems, it is reasonable to conclude, that initially when we were nocturnal primates, we had a dysfunctional S-opsin gene and a functional L gene- conferring us the ability to perceive the red qualia to some extent.
In diurnal prosimians, the S become functional and they have two qualia- that of red and blue.
In the new world monkeys, the L gene is polymorphic (it is on X chromosome and as explained in the paper, if we have two alleles for that L gene, that encode for slightly different frequencies, then as females have two X chromosomes, they can have both the alleles; the males meanwhile have only one X chromosome; so at at a time they can have only one of the alleles present. By X chromosome inactivation process, all cells of a female new world monkey, will have only one of the alleles; but different cells may have different alleles expressed and thus, the females may have 3 types of receptors (one S type and two L types), thus endowing them with trichromatic vision. The Males meanwhile will have dichromatic vision, but as the gene is polymorphic, we will differences in their dichromatic perceptions. This is exactly what is observed.
The old world monkeys, have the full apparatus for trichromatic vision- with one S and two L genes. The second L (or rather M as it detects green) gene was formed by replication and polymorphisms of the L gene that detected red. thus, they had the qualia of Red, Blue and Green.
Lastly, the humans, are more or less the same as old world Monkeys; but their L gene shows polymorphisms. This has the effect of making some females tetrachromatic (as this polymorphisms will only affect females- only they have two copies of X chromosome) and it seems , that by fortuitous replication, we might get a fourth cone type in all humans. Till then, this polymorphisms will explain some of the color perception differences that we may exhibit.
Suffice it to say, that the evolution of color terms should follow the same trajectory- with Black and White (rod based) color terms preceding Red, Blue, Green and Yellow color terms.
A final note of caution: only receptor types do not guarantee that the qualia experienced would change. In an experiment with mice, in which the mice were endowed with human pigments, they could not still learn to distinguish Red, as presumably the latter opponent-processing wiring, required for that qualia generation was not present/ couldn't develop.
Thats all for now. Hope you found this post Eye opening!! Do let me know via comments of any incompatible/recent evidences and arguments.