evolution of vertebrate colour vision - sites.oxy.edu

OPTOMETRY

I INVITED REVIEW I

Evolution of vertebrate colour vision

Gerald H Jacobs BA PhD Mickey P Rowe BSE PhD Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara, USA

Submitted: 3 March 2004 Revised: 2 June 2006 Accepted for publication: 7 June 2004

Clin Exp Optom 2004; 87: 4-5: 206216

Recent years have witnessed a growing interest in learning how colour vision has evolved. This trend has been fuelled by an enhanced understanding of the nature and extent of colour vision among contemporary species, by a deeper understanding of the paleontological record and by the application of new tools from molecular biology. This review provides an assessment of the progress in understanding the evolution of vertebrate colour vision. In so doing, we offer accounts of the evolution of three classes of mechanism important for colour vision-photopigment opsins, oil droplets and retinal organisation-and then examine details of how colour vision has evolved among mammals and, more specifically, among primates.

Key words: colour vision, evolution, opsin, photopigments, retinal cells

Colour vision is a behavioural capacity that permits animals to discriminate variations in the spectral composition of light irrespective of variations in intensity. Colour vision is widespread, though far from uni- versal, across species and among individuals. To support colour vision, visual systems must possess two basic devices: multiple sensors, each providing a means for the differential filtering of spectral energies, and comparators designed to contrast signals originating from these different sensors. Although other mechanisms can be imagined, the sensors of choice across contemporary phyla are multiple types of photopigment, each type preferentially tuned in its spectral absorption properties and usually sequestered individually in a subpopulation of photoreceptors. The comparators are typically spectrally- opponent neurons, cells so wired within nervous systems that they can provide

comparisons of the activation patterns of different types of photopigment. Overlaid on these common features of the solution to yielding colour vision is an imposing array of variations characteristic to specific animal groups. Understanding the evolution of colour vision would allow one to see how and why these commonalities and variations appear in contemporary visual systems. We are still far from such an understanding but notable progress has been made toward that goal.

The evolution of colour vision has long been a matter for speculation. Classically, such speculations were based mainly on natural history considerations and on comparative examinations of ocular anatomy.'.2 In recent years, a flood of new information about the mechanisms underlying colour vision and an intensified interest in the ecology of colour vision have provided fresh impetus for examin-

ing the evolution of colour vision. A key to recent progress is that molecular biology now provides powerful tools for expanding our understanding of photopigmen ts.

Study of the genetics of opsins, the photopigment proteins, is less than two decades old, but it has already produced an impressively large accumulation of opsin sequence information. Comparisons of these sequences can be used to adduce photopigment phylogenies that can be viewed in light of known relationships between photopigments and colour vision in contemporary species, so as to draw inferences about colour vision in ancestral species. One should recognise that such inferences are potentially subject to error. For one thing, there is no analogous way to derive information about the comparator arrangements in ancestral visual systems and thus, their presence and nature

Clinical and Experimental Optometry 87.4-5 July 2004

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Evolution of colour vision Jacobs and Rowe

often must be assumed.g Another limita- tion is that current molecular markers do

0rig.h~ of multiple pigments and CO~OUI' vision

not offer any information about photopigment expression and, as a consequence, it is impossible to learn how any particular pigment may have been represented in the photoreceptors. As a result, the prevalence of the pigment and its spatial distribution across the receptor array re- main unknown; this can be important as both features can impact significantly on the nature of colour vision. Finally, there are the general difficulties inherent in try- ing to align molecular phylogenies with information gleaned from the fossil record.

In what follows, we first make observa- tions on the evolution of three classes of mechanism important for determining colour vision and then consider issues surrounding the evolution of mammalian colour vision and, more specifically, primate colour vision.

OPSINS AND THEIR EVOLUTION

Amino acid sequences have been com- piled and absorption spectra measured for more than 100 vertebrate visual pigments." A consensus view (Figure 1) emerging from comparisons of these sequences is that vertebrate visual pigment opsins fall into five groups; one (RHl) consists of pigments expressed in vertebrate rods and the remaining four (SWSl, SWS2, RH2 and LWS) are normally cone photopigments.

Although experts tend to agree on the groupings of opsins suggested in Figure 1, the timing of the various events de- picted is less certain. Sequence comparisons among contemporary organisms indicate that opsins were an ancient invention. One suggestion is that motile micro-organisms like green algae may have been the first to develop photo- ~ igmen t s .~At a later time, perhaps 800 to 1100 MYA, the progenitor opsin gene duplicated and subsequently diverged in structure yielding two types of cone pig-

Visual pigments consist of apoproteins, opsins, which are covalently bound to chromophores. Vertebrate pigments uti- lise only two different chromophores, 1 14s-retinal or 1 l-cis-3,4dehydroretinal, but there is a large array of different opsins. In the past 20 years, it has been established that sequence variations in opsins cause predictable shifts in the absorption spectrum of the photopigment. This relationship between sequence variation and spectral tuning can be subtle; for example, change of a single nucle- otide in a human cone pigment gene yields a predictable peak shift in the long- wavelength sensitive (L) pigment of about six nanometres.46 These tuning mechanisms are also conserved across a wide range of species. For example, the spectral positioning of mammalian M/L opsins can be accounted for by variation at a total of only five of approximately 350 amino acid positions that characterise these cone o p ~ i n s . ~ A consequence is that the determination of opsin gene sequences provides a rich source of information about visual photopigments and their evolution.

ment with respective peaks in the short and middle to long wavelengths.'O

Recent work on the opsin genes of the lamprey (Geotria australis), an agnathan (jawless) fish, suggests that there were four cone opsin lineages prior to the emergence of jawed vertebrates and only rod opsins emerged after that event." Al- though we do not know that comparator mechanisms and hence true colour vision appeared coincident with multiple opsins, it seems clear that the pigmentary basis for some colour vision has been available throughout vertebrate evolution.

Evolution of O P S ~ S following the appearance of dour vision Evolution of opsin genes subsequent to the divergence into four major cone opsin families has taken a number of twists and turns in the various branches of the vertebrate tree. In many cases, genes from the different families have been lost; in some of these, opsin diversity has been at least partially reacquired through subsequent gene duplication and divergence. Loss of pigments appears to follow evolution into ecological niches where light is relatively

For example, probably as a consequence of early nocturnality, eutherian mammals retain opsins from only two of the four families, while Old World primates exemplify reacquisition of pigment diversity as their LWS opsin gene has been duplicated to yield two separate types of LWS gene.15

Within a given opsin family, photopig- rnent spectral sensitivities are tuned to various extents. It is generally assumed that tuning is adaptively significant and often implied that opsins can be tuned to any wavelengths that it might benefit an animal to see. That conclusion is probably too extreme. For example, among some invertebrates phylogenetic relatedness is a better predictor of opsin complement than is visual ecology.Ifi

There are many interesting patterns in the evolution of opsins and this may be particularly so in the spectral tuning of opsins in the SWSl family. For instance, it was a surprise to find evidence for rodent photoreceptors with primary sensitivity to UV wavelengths." We now have evidence that UVsensitivity was ancestral for all vertebrates and that this was retained in the most recent common ancestor of all mam- m a l ~ . ' ~ , ' ~ Although falling in the range of sensitivities for SWS2 genes, the S cones of humans and other primates are members of the SWSl family. In most eutherian mammals, this pigment has been shifted toward longer wavelengths.

Similarly, as a result of mutations at four key sites the SWSl photopigment in the line leading to birds appears to have shifted its of 360 nrn to 390 nm.19 In four avian lineages, a different set of mutations has shifted the SWS %,= back to about 360 nm.20 Another interesting aspect of SWS opsins in birds speaks to the lability of photopigments; there is no significant correlation between the A,,, values of SWSl and SWS2 opsins when the SWSl opsin is primarily a UV photoreceptor. However, there is a significant positive correlation between the A,= values of the two opsins when the SWSl opsin is an S cone rather than a UV cone, as if a large shift in %,=of SWSl induces a concomi- tant shift in SWS2 to maintain spectral separation between the two pigments.*'


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Figure 1. Opsin family tree for representative vertebrates as calculated from amino acid sequences using the neighbour joining method. The scale bar represents the substitution rate of each amino acid. Adapted from Hisatomi and Tokunaga.=

Evolution of colour vision entails more than the evolution of opsins It is important to stress that opsin evolution is not equivalent to colour vision evolution and it is not even equivalent to the evolution of photoreceptor types. Absorp- tion of light by opsin initiates a biochemical cascade, which eventuates in a change in the rate of release of neurotransmitter from the photoreceptor to post-synaptic cells. Recent evidence confirms what has generally been assumed; exchanging opsins in a photoreceptor is sufficient to change its spectral sen~itivity.~*~~As all cells contain an organism's entire genome, the spectral sensitivity of any given photorecep tor is set by what amounts to a molecular switch determining which photopigment

gene is expressed in that cell. Some of the functional distinctions be-

tween rods and cones, such as their relative noise levels, sensitivities and time courses of activation, are established in part by differences in the proteins, aside from opsin, that participate in the phototransduction cascade.*' It seems that rods and cones can be transmuted into each other largely through the effects of another single switch, this one determining which set of genes is expressed for the rest of the biochemical transduction cascade.22

In general, only one opsin gene is expressed in any given photoreceptor, however, there are notable exceptions to this rule, particularly among rodents, where many cones coexpress two visual pig-

r n e ~ ~ t s . * ~ . ~ ~ While it is theoretically possible that dual expression could support colour vision (for example, if activation of one pigment initiated a biochemical cascade that was shut down by activation of the other), it does not appear that any vertebrates use such a system. Dual expression of pigments does serve to expand the wavelength range, over which a given photoreceptor responds to light and that in itself can be adaptively

Vertebrates can employ variation in opsin expression as a mechanism for modi- fying the fundamental bases of colour vision. Extreme cases are the cichlid fishes, which selectively express a particular set of opsins as a means to tune their overall spectral sensitivity.28 Generally, animals regulate the pattern of opsin expression across their retinas. Much of this process is under direct genetic control, as indicated by the regularity across individuals of density maps of particular photoreceptor types. The retinas of humans and similar primates illustrate an exception to this level of controlm in that M/L opsin expres sion appears to be governed by a stochastic process.s0 As noted above, colour vision requires

not only receptors with differing spectral sensitivities but also comparison of their outputs. For an animal to perceive colour without scanning eye movements, these comparisons should arise from receptors with different photopigments placed at roughly the same retinal locations. Opsin expression patterns generally serve this goal but that is not always the case. For example, the distributions of the two classes of cone in the retina of the tarsier show very little spatial overlaps1 and thus seem unlikely to support traditional colour vision. Cases like this reinforce the view that knowledge of the opsin gene complement is not sufficient to infer the status of colour vision. Comparative studies suggest that distributional variations in opsin expression are related to visual ecology as well as phylogeny (fish:* birds"). An extreme case is the European starling, a bird in which opsin expression patterns differ for the two eyes in a way that makes one eye potentially better for colour proces~ing.~~


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In addition to differences in opsin expression, photoreceptor types often have characteristic morphologies that can be used to distinguish them. Common features of many vertebrate retinas are double or, less commonly, triple cones, photoreceptors so closely associated with each other that they function at least partially as single units. Many hypotheses have been proposed on the benefits of these associa- tions and although colour processing has rarely been posed as a primary reason for double cones, these receptors bear men- tion here because of what they suggest about the evolution of cone types. In some animals, both halves of each double cone express the same pigment;s4 in others the two halves express different pigments.s5 In the simplest evolutionary scenarios, one of these double cone types evolved into the other. The implication is that ‘new’ photoreceptor types may evolve not just through the addition of photopigments via gene duplication, but also through a change in gene expression causing a cell to switch between two pigments that already exist in the genome. Indeed, when developmental mechanisms are disrupted, cones of one morphological type may express the opsin normally associated with cones of a different morphological type.”

OIL DROPLETS AND THEIR EVOLUTION

A variety of spectrally-selective filters exists in animal eyes. Potentially, the most important of these for colour vision are the oil droplets located in the inner segments of cone photoreceptors. Many of these oil droplets are pigmented, acting as long-pass spectral filters.36 The location of the passband varies across different types of oil droplets, giving them their conspicuously coloured appearance in fresh tissue. Func- tionally, oil droplets act to selectively filter incident light and yield three effects: 1. effectively narrowing the absorption

spectrum of the pigment lying behind it 2. shifting the peak absorption of the

photopigment toward the longer wavelengths

3. decreasing the overall absorption efficiency of the pigment.

Figure 2. Distribution of oil droplets in a number of contemporary animals and a probable phylogeny. Note that oil droplets have either evolved several times or have been modified and/or lost several times. The figure is modified from those provided by Robinson” and Rowe.% The branching topology and timing are approximated from several sources, principally Meyer and z a n l ~ y a . ~ ~

In theory, an animal might derive colour vision by comparing signals from receptors having identical photopigments but with differing types of oil droplets. No animals seem to have taken advantage of this possibility but oil droplets are known to significantly impact the character of colour vision that an animal derive^.^'

Oil droplets are found in the retinas of a wide variety of animals, suggesting that oil droplets were also an early invention, possibly predating the emergence of ter- restrial vertebrates (ca 400 MYA) .% Figure 2 provides an account of the distribution of oil droplets among the vertebrates. A notable feature is that oil droplets are r e p resented only sporadically across contemporary vertebrates and a typical interpre- tation of this fact is that some lineages have lost oil droplets over the course of time.

One important example of such loss is in eutherian mammals, where oil droplets are completely absent. Gordon Walls’ suggested that oil droplet loss could be occa- sioned by a shift from diurnal to nocturnal patterns and that, once lost, oil droplets are hard to reacquire. The first of these ideas is eminently reasonable on grounds of visual efficiency and it receives some support because although the retinas of some nocturnal species retain oil droplets, their droplets are unpigmented. As for whether oil droplets may be dXi- cult to reacquire, there seems to be no evidence one way or the other.

On the other hand, there is clearly lability in the pigmenting of oil droplets and their distribution across the retina, as these properties can vary much as does the pattern of opsin e x p r e s s i ~ n . ~ ~ * ~ ~


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NEURAL MECHANISMS AND THEIR EVOLUTION

As there are neither molecular nor paleontological markers to provide inferences about the comparator mechanisms that are a requirement for colour vision, any understanding of the evolution of this portion of the colour vision apparatus is rudimentary. Spectrally-opponent neurons are widespread, perhaps even univer- sally present, in contemporary vertebrates and invertebrates known to have colour vision. Their ubiquity alone implies they have a long evolutionary history.

Invertebrates frequently display what is called wavelength-selective b e h a v i ~ u r . ~ ~ This is defined by a compulsive linkage between some spectral input and a pattern of behaviour; for example, escape behaviour in the butterfly, Pieris, is selectively elicited by ultraviolet lights4] Wavelength- selective behaviour need not be learned nor can it be altered by learning, as is the case for colour vision. Measurements of the spectral sensitivities of wavelength- selective behaviour show that they require multiple pigments and that signals from these pigments interact in the nervous system. Many arthropods show evidence for some wavelength-selective behaviour, which can be present side by side with true colour vision. This fact has been taken to suggest that neural mechanisms needed for wavelength-selective behaviour may have predated the appearance of colour vision.I6 There are no claims for wave- lengthdependent behaviour in vertebrates, but that may reflect more of a lack of attention to the possibility than a reality.

Comparative retinal form and function As with the five families of vertebrate opsin genes, the basic neural circuitry of the vertebrate retina appears to have been e s tablished early in evolutionary history. The neural retina of all vertebrates is divided into three layers containing cell bodies and two layers composed primarily of intercel- lular connections. Retinal research of the past 30 years has allowed classification of retinal cells and their connections accord- ing to both anatomy and function. Most

of the circuitry in the retina appears to have been conserved, at least among ter- restrial vertebrates. This is true even in mammals despite their loss of photoreceptor types and other specialisations. Al- though much could be said about each of the several classes of retinal cell, we focus here mainly on horizontal cells to point out the sort of questions that should be answered for all retinal cells in order to understand the evolution of colour vision.

Horizontal cells receive direct input from photoreceptors, and by contacting several cones of more than one type, they can contribute to the spatial and spectral processing of visual information. Svaetichin and MacNicho14* first demonstrated a likely role for these cells in spectral processing when they showed that re- sponses of some teleost horizontal cells receive opponent input from cones of different spectral type-a hallmark of colour vision. Cells exhibiting opponent behaviour were called Gtype (chromaticity) and distinguished from L-type (luminosity), the latter showing no indication of spectral opponency. As it seems clear that some horizontal cells in some animals play a role in processing colour information, it makes sense to try to compare different horizontal cell types across different animals, to learn how colour vision has evolved. Above, we identified five families of opsin that are conserved across vertebrates. Are there classes of horizontal cell that could be used to indicate how the processing of cone signals has evolved? The answer is probably yes, but we have not progressed as far in the quest to answer that question as we have in understanding the evolution of opsin genes.

Excluding mammals, vertebrates generally have four horizontal cell types (Hl- H4). The structure and function of teleost horizontal cells dif€er in ways that make assignment to categories derived for ter- restrial vertebrates problematic, so we will not consider them further. We are reason- ably confident that the mammalian H1 type is homologous to the H1 type of turtles. In both turtle43 and mammal,44 these cells have two electrically isolated arborisations: a dendritic arbor close to the cell body and a telodendritic arbor

separated from the cell body by a long thin axon. The dendritic arbor in turtle H1 cells contacts cones presumably expressing LWS, RH2, and SWS2. In primate H1 cells, the dendritic arbor contacts M and L cones, that is, cones containing different forms of LWS pigments. Thus, the con- nectivity of the dendritic arbors is the same in turtle and primate, given that mammals have no receptors expressing SWS2 or RH2 pigments. The two cell types are not identical, as the telodendritic arbor of primate H1 cells contacts only rods whereas the telodendritic arbor of turtle H1 cells connects with rods and LWS containing cones. In mammal and turtle, H1 cells are classified as L-type cells; they hyperpolarise in response to light irrespective of wavelength.

Turtle H2 horizontal cells receive inputs primarily, if not exclusively, from cones that likely express RH2 and SWS2 pig- m e n t ~ . ~ ~ As the turtle retina retains the ancestral state of five photopigments, it is reasonable to conclude that the turtle H2 horizontal cell is similarly retained from one of our earliest ancestors. Thus, mammals lost this cell type, when they lost RH2 and SWS2 pigments.

Turtle H3 cells receive direct input from both SWSl and SWS2 cones and hyperpolarise in response to their stimulation. This is similar to the behaviour of primate H2 horizontal cells, which hyperpolarise in response to stimulation of S cones. How- ever, primate H2 cells have direct connections with M and L cones and hyperpolarise when they are stimulated as well.45 This contrasts with turtle H3 cells that depolar- ise as a response to stimulation by long wavelength light. The turtle H3 cell’s long wavelength response is mediated by indirect contacts as LWS cones do not synapse onto H3 cells.43

Are primate H2 cells homologues of turtle H3 cells? If so, did primates add the direct M/L path while deleting the indirect, opponent path from LWS cones, did turtle H3 cells delete direct contacts with LWS cones while adding indirect contacts, or did the ancestral horizontal cell have neither direct nor indirect input from LWS cones? The indirect input for turtle H3 cells probably comes ultimately from


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double cones, so the major rewiring of the mammalian H 2 horizontal cell may have occurred as double cones were lost. The turtle H4 cell is little understood but also appears to get its major input from double cones45 and hence, may have been lost from the mammalian retina at the same time that the mammalian H 2 cell was being rewired. Clearly, we have more questions than answers but we believe these are the sorts of questions that should be raised in an effort to understand the evolution of colour vision. More detail on the relationships of horizontal cells to colour processing in vertebrate retinas is provided elsewhere. 45.46,

There is some information on the relative numbers of cell types in reptilian and mammalian retinas. Ammermdler and K ~ l b ~ ~ found evidence for 13 bipolar cell types, 36 amacrine cell types and 24 ganglion cell types in the turtle retina. In a similar survey, Masland4’ catalogued nine to 11 bipolar cell types, 29 amacrine cell types and 10 to 15 ganglion cell types in a typical mammalian retina. These numbers are likely to represent lower limits, and turtle cell diversity is underestimated probably even more than mammalian cell diversity. The gross similarity between the numbers suggests either that the number of cone types is not a good indicator of the amount of processing that an animal performs on colour signals or that mammals, rather than shedding neuronal types, co-opted them to process non-spectral as- pects of visual information.

Colour processing beyond the retina is relatively unexplored in most animals. Primates represent a notable exception. Research on that topic has been reviewed recently4s and is covered elsewhere in this issue.

EVOLUTION OF MAMMALIAN COLOUR VISION

Mammals diverged from other vertebrates approximately 300 MYA, so roughly half of their history as multi-cellular life forms comprises independent evolution. Over these subsequent millennia, Mammalia has evolved into its current 18 orders and more than 4,600 species. Evidence from

palaeontology indicates that early mammals were small and nocturnal. This basic nocturnality has impacted indelibly on the nature of mammalian vision. Unlike other groups of vertebrate, the retinas of the vast majority of contemporary mammals are dominated by rod photoreceptors. In addition to a dramatic alteration in the mix of rods and cones, there have been con- spicuous losses of potential colour vision mechanisms. As noted above, the coloured oil droplets that characterise the colour vision machinery of many birds and r e p tiles are missing from mammalian retinas and two of the vertebrate cone opsin gene families are not represented in eutherian mammals (SWSP and RH2, Figure 1) having apparently been lost in the evolution of this group. This reduction in the number of potential cone photopigment types and the loss of an important source of selective spectral filtering has yielded greatly simplified colour vision in mammals.

With the exception of primates (and, possibly, some marsupials-see below) the loss of cone opsin genes means mammals have only two cone types, pigments produced by SWSl and LWS gene representatives. Thus, from a pigment perspective, this limits most mammals to dichromatic colour vision. That dichromacy is the mammalian mode is now well established from behavioural studies and from cata- loguing mammalian phot0pigments.4’~~ The LWS photopigments employed by different mammals are spread across a large spectral range (ca. 500 to 560 nm); similarly, the SWSl representatives appear in different mammals over the spectral range from about 360 to 440 nm. The relative r e p resentation of cones containing LWS and SWSl pigmen& varies across species but generally the former greatly outnumber the latter (by ratios of 10 to more than 1OO:l).

Dichromatic colour vision may be the norm for mammals, but it is misleading to assume that there are no differences in colour vision among these dichromats. Partly, this reflects the variations in the spectral positioning of the two cone classes. Beyond that, there are significant differences in cone density and cone distributions among mammalian retinas, and

both of these factors will influence the acuteness of colour vision. For example, domestic cats and human deuteranopes have two types of cone pigment with spectral properties that are not greatly different for the two species. With much higher cone densities and more robust spectral opponency, human dichromats have much more acute colour vision than cats. There are many other such examples to reinforce the idea that although counting opsin genes or photopigment types can provide predictions about colour vision, they are far from the whole story.

Figure 3 shows the tree topology of the LWS pigments for a number of representative mammals. In that figure the Amaxvalues for pigments of contemporary mammals were obtained from in situ measurements while estimates of the peaks of the ancestral pigments were derived from the five- sites rule for spectral tuning. By this account, the ancestral LWS pigment of all mammals is estimated to have had a peak of about 530 nm.53

We noted that phylogenetic relatedness has an impact on the spectral positioning of the cone pigments. Additional evidence of that influence can be seen in mammals. For example, Figure 3 identifies the Am= of the LWS cone pigment of the domestic cat as being about 553 nm. This spectral location is very close to the LWS cone position of many different carnivores; including not only other felines but also various canids and procyonids along with, interestingly, many marine carnivores (pinnipeds). These carnivores inhabit a wide range of different photic habitats but share in common the spectral positioning of their only LWS cone pigment.

There are two recent twists to the mammalian colour vision story relevant to the issue of evolution. The first of these in- volves the loss of function of the SWSl gene in a number of mammalian lineages. Although there were earlier indications from physiological and anatomical work for an absence of an S cone in some species, it was from direct examination of SWSl opsin genes in two nocturnal primate species that it first became clear that this loss reflects mutational changes in the genes that have made them nonfunc-


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having much of any colour capacity.64 Clearly, there is still much to be learned about the evolution of opsin genes and colour vision among marsupials.

Figure 3. A tree topology of mammalian LWS cone pigments (modified from Yokoyama and Radlwhmer’). The numbers in parentheses indicate the k- values for the pigment; the numbers beside the branches were predicted from the five-sites rule, while those adjacent to common names represent values obtained from in vitmrneasurements of cone pigments.

ti0na1.~~ Unlike the very rare mutations that render human SWS genes inoperative and lead to the colour vision defect called

A second complication is the recent discovery that some marsupials appear to have three cone classes rather than the two

tritanopia, the gene mutations detected in these non-human primates were common across individuals. The inescapable conclusion is that loss of SWSl related photopigment must have been adaptive. Soon after this discovery, a variety of other mammals, including some rodents and carnivores, were demonstrated to show a similar loss.55-56 Perhaps most striking is the widespread loss of function of the SWSl gene in marine mammals. It appears that all cetaceans and pinnipeds lack functional SWSl Thus, these animals have only a single type of cone pigment and perforce must lack colour vision.

Although the presence of SWSl pseudogenes is now clearly established in a number of mammalian lineages, how this may have come about is unclear. Various explanations of the reasons for such loss being adaptive have been offered but none of these seems very compelling. At present, the loss of SWSl cone function in some mammals remains an intriguing mystery.

typical of most mammals. Specifically, two Australian marsupials, the honey possum (Tussipes rostrutus) and the fat-tailed dunnart (Sminthopsis crassicaudata) , have been found to have three types of cone pigment. One of these peaks in the UV. The other two are around 505 nm and, depending on the species, at either 535 or 557 nm.61 The middle of these three pigments is suggested to be an RH2 pigment, although this has not been established. Thus, from a pigment perspective, these marsupials have the basis for trichromatic colour vision. Whether they achieve that capacity remains to be seen. Although our knowledge of marsupial colour vision is scanty, the arrangement found in these two species does not seem to be common to all marsupials. The tammar wallaby (Mucropus eugenit], for instance, has only two cone classes and dichromatic colour visi0n.6**~~ Nocturnal New World marsupials, such as the opossum, Didelphis sp, have so few cones that it is hard to conceive of them being trichromatic or, indeed, of

EVOLUTION OF PRIMATE COLOUR VISION

Primates hold a special place in the evolution of mammalian colour vision, primarily because many members of this order have effected an escape from the confines of dichromatic colour vision characteristic of other mammals. Over the past two decades, much has been learned about the nature and evolution of primate colour vision. Here, we provide a brief summary of the current understanding; more exhaus- tive listings of original papers can be found in several recent reviews of this topic.6569

The realisation that humans have trichromatic colour vision began to emerge more than 300 years ago, and unequivo- cal evidence that this capacity reflects the presence of three separate types of cone pigment is now 40 years old. That not all primates share the human colour vision arrangement first became evident in an early examination of monkey colour vi- ion.^' In this pioneering study,” behavioural tests of three species of Old World (catarrhine) monkey showed them to be trichromats but similar tests of a New World (platyrrhine) monkey indicated it is a dichromat. Subsequent examinations of a range of catarrhine species show that all species from this group have very similar, if not identical, trichromatic colour v i s i~n .~ ’ .~~

Colour vision in platyrrhine monkeys differs dramatically from the catarrhine standard and this difference has proven useful as an aid to understanding the evolution of primate colour vision. The CIU-

cia1 fact is that colour vision in platyrrhine monkeys is highly polymorphic. Within most such species, there are both dichromatic and trichromatic individuals, and each of these classes includes variant forms. Early studies documented these colour vision variations and showed they could be directly traced to variations in LWS photopigments of these In addition to an SWSl pigment common to all individuals, dichromatic monkeys


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have only a single representative pigment drawn from the LWS class, while trichromatic animals have two. Strikingly, although male platyrrhine monkeys are exclusively dichromatic, females may be either dichromatic or trichromatic.

Based on pedigrees of human colour vision defects it had long been appreciated that the human LWS opsin genes must be X-chromosome linked and that there must be at least two such genes. Accordingly, it was natural to suggest that, unlike catarrhines, platyrrhine monkeys have only a single X-chromosome opsin gene with allelic versions of the gene.74.75 Such an arrangement would limit males to dichromacy but would permit females that are heterozygous at the LWS opsin gene site to produce two spectrally discrete cone pigments. Random X-chromosome inac- tivation could be used to sort the two pigments into separate cone classes and so these females become trichromatic. Both pedigree studies and direct examination of opsin genes support this ~uggestion.’~*’’

Expansion of these studies to additional platyrrhine species revealed that, with the exception of only two genera, all New World monkeys have similar opsin gene and colour vision polymorphisms. How- ever, among these polymorphic species, there are other important variations. One is that the set of allelic genes, and thus the spectral positioning of the cone photopigments, varies in different lineages and this will greatly influence the character of colour vision beyond its dimensionality. An- other variant is that although most platyrrhines appear to have three allelic versions of the gene, members of at least two genera seem to have only Among other things, the number of alleles can influence the incidence of female trichromacy. Finally, monkeys from two platyrrhine genera are not polymorphic. One of these is Aotus, one of the nocturnal primates known to lack a functional SWSl pigment. These animals also have no LWS gene polymorphisms and so lack colour vision.79 The other exceptions are the howler monkeys (Alouatta) that, sur- prisingly, have an opsin gene/photopigment arrangement very similar to that of the catarrhine primates, for example, they

Figure 4. The distribution of colour vision among primates. The nature of colour vision measured or inferred for a number of extant genera has been divided into three categories: routinely trichromatic; polymorphic; routinely dichromatic or monochromatic. See the text for further details. The numbers identify the three taxonomic groupings referred to in the text (lstrepsirrbines, 2-platyrrbines, 3- catarrbines). Tarsius (4) is currently considered as belonging in the same sub-order (Hafilorhini) as the platyrrhme and catarrhine monkeys. Figure adapted from Surridge, Osorio and M ~ n d y . ~

have two separate X-chromosome opsin genes and so all individuals are trichromatic.8O

We know rather less about colour vision in the third major group of primates, the more primitive strepsirrhines. Until recently, it was believed that strepsirrhines are either routinely dichromatic, like many mammals, or that they lack colour vision entirely as a result of non-functional SWSl genes. It is now known that in addition to these two forms some of the diurnal strepsirrhine species have X-chromosome opsin gene polymorphisms similar to those

seen in platyrrhines, allowing heterozygous females to have three cone photopigments and potential trichromacy.81-82

There are some variations in the densities of cones and their retinal distributions among catarrhines and platyrrhines. With the exception of the nocturnal Aotus monkey, which has low cone densities and lacks a fovea, these variations are modest relative to the large differences in the organi- sations of the photoreceptor mosaics between these two groups and the strepsirrhines. The strepsirrhines have lower (often much lower) cone densities and


21 3


they have no distinct foveal specialisations. Irrespective of the dimensionality of colour vision, these differences predict much less acute colour vision among the strepsirrhines than in the other two groups.

The primate phylogeny shown in Figure 4 summarises what we know about the distribution of colour vision among primates. The events leading to these variations in colour vision are still matters of some uncertainty. The consensus is that the earliest primates had a single LWS pigment (with a peak at perhaps around 550 nm, as suggested in Figure 3) and an SWSl pigment, the standard arrangement for routine dichromacy. Some time after the divergence of catarrhine and platyrrhine lineages, perhaps about 30 MYA,Ss the X-chromosome opsin gene in catarrhines duplicated to yield genes that coded for two spectrally discrete LWS pigments (usually called L and M, respec- tively).

Whether polymorphism was a prelimi- nary to catarrhine gene duplication or whether divergence occurred following the duplication is not yet established.68 Because this duplication event occurred early in catarrhine evolution, all subsequent catarrhines share their M and L cone pigments. Most platyrrhines achieve some partial trichromacy through polymorphism at a single gene site. Sequence comparisons suggest the platyrrhine polymorphisms had a single origin and that the gene duplication that led to routine trichromacy in howler monkeys is a relatively recent event that occurred independently of the catarrhine gene duplica- t i ~ n . ~ ” ~ There is evidence that the platyrrhine colour vision polymorphisms have been adaptively maintained over consider- able periods of time.ffi Opsin gene polymorphism has emerged only sporadically in the strepsirrhines (Figure 4) and there is de- bate on whether these polymorphisms emerged independently of those occumng in the anthropoid lines.’4**’

The evolution of primate colour vision provides nice examples of how colour vision undergoes change over time but it also raises some questions. For example, opsin gene polymorphism has been

revealed as a means to provide new colour vision capacities. As primates accom- plish this starting from opsin gene arrangements similar to those of most other mammals, it is intriguing to know why no other mammals have followed the primate lead and reacquired some of the colour vision lost by their ancestors.

There are several possible explanations for this disparity but the most popular is that the primate retina is uniquely organ- ised to take immediate advantage of the addition of new cone types.87 Crucial to this argument is the presence of midget- cell pathways in the primate retina that serve to conduct signals from cones through the retina to P-type ganglion cells. In the central portion of the retina, the receptive field centres of small P cells receive input from a single M or L cone, while their surrounding regions are preferentially dominated by either M or L cone input. This imparts to the ganglion cell strong spectral opponency and provides the basis from which a dimension of colour vision can subsequently emerge.

It appears that the midget cell pathway is common to all catarrhine and platyrrhine primates, irrespective of the number of cone pigments they possess; indeed, there is evidence that an analogous organisation also exists in retinas of strepsir- rhines8* This suggests that the midget cell pathway must have arisen early in primate evolution, possibly as an adaptation to s u p port higher spatial acuity. The argument is that the presence of a new LWS pigment can be exploited without any additional changes to the primate retina and imme- diately yield novel spectral opponency. Support for this hypothesis comes from the fact that, other than the number of photopigment types, there are no known differences in the organisation of retinas of conspecific dichromatic and trichromatic monkeys?’

The description of the steps involved in the evolution of primate colour vision inevitably raises questions about the functional utility of the various forms of colour vision. For example, why has trichromacy evolved in primates? Are there advantages in maintaining highly polymorphic colour vision? The ecology of primate colour

vision has become a topic of great interest in recent years. Following classical sugges- tions, most of this focus is on the potential uses of colour vision as an aid to the harvesting of food. The literature on this topic is fascinating and currently under rapid expansion but its review is beyond the scope of this paper. For insight into the ecology of primate colour vision a number of recent sources may be con- sulted.w93

Evolution in studying the evolution of colour vision Recent years have seen great progress in our understanding of the evolution of colour vision. This review has touched on areas well known and areas relatively unexplored in efforts to understand what has happened to this capacity throughout vertebrate history. In doing so, we attempted to illustrate the wealth of facts available to contemporary researchers, to point out new tools useful in this endeavour and to highlight significant lacunae still needing attention. Much of the research discussed here was necessarily focused on particular molecules, types of cell or neural net- works. Although all of these levels of analysis are important, none taken in isolation is sufficient to explain the evolution of a complex ability like colour vision. In the end, the evolution of colour vision needs always to be viewed in the context of our understanding of colour vision as a sensory capacity.

DEDICATION Dedicated to the memory of Russell L De Valois (1926-2003), who made major contributions to the understanding of colour vision.

GRANTS AND FINANCIAL SUPPORT Preparation of this review was supported by a grant from the National Eye Institute (EY002052).

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Author's address: Gerald H Jacobs Neuroscience Research Institute University of California Santa Barbara, CA 93106 USA

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