Evolution of Vertebrate Colour Vision

OPTOMETRY

I INVITED REVIEW I Evolution of vertebrate colour vision

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

Gerald H Jacobs BA PhD Recent years have witnessed a growing interest in learning how colour vision has evolved. Mickey P Rowe BSE PhD This trend has been fuelled by an enhanced understanding of the nature and extent of Neuroscience Research Institute and colour vision among contemporary species, by a deeper understanding of the Department of Psychology, University of paleontological record and by the application of new tools from molecular biology. California, Santa Barbara, USA 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 Submitted: 3 March 2004 of mechanism important for colour vision-photopigment opsins, oil droplets and retinal Revised: 2 June 2006 organisation-and then examine details of how colour vision has evolved among Accepted for publication: 7 June 2004 mammals and, more specifically, among primates.

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

Colour vision is a behavioural capacity that comparisons of the activation patterns of ing the evolution of colour vision. A key permits animals to discriminate variations different types of photopigment. Overlaid to recent progress is that molecular in the spectral composition of light irre- on these common features of the solution biology now provides powerful tools for spective of variations in intensity. Colour to yielding colour vision is an imposing expanding our understanding of vision is widespread, though far from uni- array of variations characteristic to specific photopigmen ts. versal, across species and among individu- animal groups. Understanding the evolu- Study of the genetics of opsins, the als. To support colour vision, visual systems tion of colour vision would allow one to photopigment proteins, is less than two must possess two basic devices: multiple see how and why these commonalities and decades old, but it has already produced sensors, each providing a means for the variations appear in contemporary visual an impressively large accumulation of differential filtering of spectral energies, systems. We are still far from such an opsin sequence information. Comparisons and comparators designed to contrast understanding but notable progress has of these sequences can be used to adduce signals originating from these different been made toward that goal. photopigment phylogenies that can be sensors. Although other mechanisms can The evolution of colour vision has long viewed in light of known relationships be- be imagined, the sensors of choice across been a matter for speculation. Classically, tween photopigments and colour vision in contemporary phyla are multiple types of such speculations were based mainly on contemporary species, so as to draw infer- photopigment, each type preferentially natural history considerations and on ences about colour vision in ancestral tuned in its spectral absorption properties comparative examinations of ocular species. One should recognise that such and usually sequestered individually in a anatomy.'.2In recent years, a flood of new inferences are potentially subject to error. subpopulation of photoreceptors. The information about the mechanisms un- For one thing, there is no analogous way comparators are typically spectrally- derlying colour vision and an intensified to derive information about the compara- opponent neurons, cells so wired within interest in the ecology of colour vision tor arrangements in ancestral visual sys- nervous systems that they can provide have provided fresh impetus for examin- tems and thus, their presence and nature

Clinical and Experimental Optometry 87.4-5 July 2004 206 Evolution of colour vision Jacobs and Rowe

often must be assumed.g Another limita- 0rig.h~of multiple pigments and For example, probably as a con- tion is that current molecular markers do CO~OUI' vision sequence of early nocturnality, eutherian not offer any information about photopig- Amino acid sequences have been com- mammals retain opsins from only two of ment expression and, as a consequence, piled and absorption spectra measured for the four families, while Old World pri- it is impossible to learn how any particu- more than 100 vertebrate visual pigments." mates exemplify reacquisition of pigment lar pigment may have been represented A consensus view (Figure 1) emerging diversity as their LWS opsin gene has been in the photoreceptors. As a result, the from comparisons of these sequences is duplicated to yield two separate types of prevalence of the pigment and its spatial that vertebrate visual pigment opsins fall LWS gene.15 distribution across the receptor array re- into five groups; one (RHl) consists of Within a given opsin family, photopig- main unknown; this can be important as pigments expressed in vertebrate rods and rnent spectral sensitivities are tuned to both features can impact significantly on the remaining four (SWSl, SWS2, RH2 various extents. It is generally assumed that the nature of colour vision. Finally, there and LWS) are normally cone photopig- tuning is adaptively significant and often are the general difficulties inherent in try- ments. implied that opsins can be tuned to any ing to align molecular phylogenies with Although experts tend to agree on the wavelengths that it might benefit an ani- information gleaned from the fossil groupings of opsins suggested in Figure mal to see. That conclusion is probably too record. 1, the timing of the various events de- extreme. For example, among some inver- In what follows, we first make observa- picted is less certain. Sequence compari- tebrates phylogenetic relatedness is a bet- tions on the evolution of three classes of sons among contemporary organisms ter predictor of opsin complement than mechanism important for determining indicate that opsins were an ancient is visual ecology.Ifi colour vision and then consider issues sur- invention. One suggestion is that motile There are many interesting patterns in rounding the evolution of mammalian micro-organisms like green algae may the evolution of opsins and this may be colour vision and, more specifically, have been the first to develop photo- particularly so in the spectral tuning of primate colour vision. ~igments.~Ata later time, perhaps 800 to opsins in the SWSl family. For instance, it 1100 MYA, the progenitor opsin gene was a surprise to find evidence for rodent duplicated and subsequently diverged in OPSINS AND THEIR EVOLUTION photoreceptors with primary sensitivity to structure yielding two types of cone pig- UV wavelengths." We now have evidence Visual pigments consist of apoproteins, ment with respective peaks in the short that UVsensitivity was ancestral for all ver- opsins, which are covalently bound to and middle to long wavelengths.'O tebrates and that this was retained in the chromophores. Vertebrate pigments uti- Recent work on the opsin genes of the most recent common ancestor of all mam- lise only two different chromophores, lamprey (Geotria australis), an agnathan mal~.'~,'~Although falling in the range of 114s-retinal or 1l-cis-3,4dehydroretinal, (jawless) fish, suggests that there were four sensitivities for SWS2 genes, the S cones but there is a large array of different cone opsin lineages prior to the emer- of humans and other primates are mem- opsins. In the past 20 years, it has been gence of jawed vertebrates and only rod bers of the SWSl family. In most eutherian established that sequence variations in opsins emerged after that event." Al- mammals, this pigment has been shifted opsins cause predictable shifts in the ab- though we do not know that comparator toward longer wavelengths. sorption spectrum of the photopigment. mechanisms and hence true colour vision Similarly, as a result of mutations at four This relationship between sequence vari- appeared coincident with multiple opsins, key sites the SWSl photopigment in the ation and spectral tuning can be subtle; it seems clear that the pigmentary basis for line leading to birds appears to have for example, change of a single nucle- some colour vision has been available shifted its of 360 nrn to 390 nm.19 In otide in a human cone pigment gene throughout vertebrate evolution. four avian lineages, a different set of mu- yields a predictable peak shift in the long- tations has shifted the SWS %,= back to wavelength sensitive (L) pigment of about Evolution of OPS~S following the about 360 nm.20Another interesting aspect six nanometres.46 These tuning mecha- appearance of dour vision of SWS opsins in birds speaks to the lability nisms are also conserved across a wide Evolution of opsin genes subsequent to the of photopigments; there is no significant range of species. For example, the spec- divergence into four major cone opsin correlation between the A,,, values of tral positioning of mammalian M/L families has taken a number of twists and SWSl and SWS2 opsins when the SWSl opsins can be accounted for by variation turns in the various branches of the verte- opsin is primarily a UV photoreceptor. at a total of only five of approximately 350 brate tree. In many cases, genes from the However, there is a significant positive amino acid positions that characterise different families have been lost; in some correlation between the A,= values of the these cone op~ins.~A consequence is that of these, opsin diversity has been at least two opsins when the SWSl opsin is an S the determination of opsin gene se- partially reacquired through subsequent cone rather than a UV cone, as if a large quences provides a rich source of infor- gene duplication and divergence. Loss of shift in %,=of SWSl induces a concomi- mation about visual photopigments and pigments appears to follow evolution into tant shift in SWS2 to maintain spectral their evolution. ecological niches where light is relatively separation between the two pigments.*'

Clinical and Experimental Optometry 87.4-5 July 2004 207 Evolution of colour vision Jacobs and Rowe

rne~~ts.*~.~~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.28Generally, 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 controlmin that M/L opsin expres sion appears to be governed by a stochastic process.s0 As noted above, colour vision requires Figure 1. Opsin family tree for representative vertebrates as not only receptors with differing spectral calculated from amino acid sequences using the neighbour joining sensitivities but also comparison of their method. The scale bar represents the substitution rate of each amino outputs. For an animal to perceive colour acid. Adapted from Hisatomi and Tokunaga.= without scanning eye movements, these comparisons should arise from receptors with different photopigments placed at roughly the same retinal locations. Opsin Evolution of colour vision entails gene is expressed in that cell. expression patterns generally serve this more than the evolution of opsins Some of the functional distinctions be- goal but that is not always the case. For It is important to stress that opsin evolu- tween rods and cones, such as their rela- example, the distributions of the two tion is not equivalent to colour vision evo- tive noise levels, sensitivities and time classes of cone in the retina of the tarsier lution and it is not even equivalent to the courses of activation, are established in show very little spatial overlaps1and thus evolution of photoreceptor types. Absorp- part by differences in the proteins, aside seem unlikely to support traditional col- tion of light by opsin initiates a biochemi- from opsin, that participate in the photo- our vision. Cases like this reinforce the cal cascade, which eventuates in a change transduction cascade.*' It seems that rods view that knowledge of the opsin gene in the rate of release of neurotransmitter and cones can be transmuted into each complement is not sufficient to infer the from the photoreceptor to post-synaptic other largely through the effects of an- status of colour vision. Comparative stud- cells. Recent evidence confirms what has other single switch, this one determining ies suggest that distributional variations in generally been assumed; exchanging which set of genes is expressed for the rest opsin expression are related to visual ecol- opsins in a photoreceptor is sufficient to of the biochemical transduction cascade.22 ogy as well as phylogeny (fish:* birds"). change its spectral sen~itivity.~*~~Asall cells In general, only one opsin gene is ex- An extreme case is the European starling, contain an organism's entire genome, the pressed in any given photoreceptor, how- a bird in which opsin expression patterns spectral sensitivity of any given photorecep ever, there are notable exceptions to this differ for the two eyes in a way that makes tor is set by what amounts to a molecular rule, particularly among rodents, where one eye potentially better for colour switch determining which photopigment many cones coexpress two visual pig- proces~ing.~~

Clinical and Experimental Optometry 87.4-5 July 2004 208 Evolution of colour vision Jacobs and Rowe

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;s4in others the two halves express different pigments.s5In 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 al- Figure 2. Distribution of oil droplets in a number of contemporary ready exist in the genome. Indeed, when animals and a probable phylogeny. Note that oil droplets have either developmental mechanisms are disrupted, evolved several times or have been modified and/or lost several cones of one morphological type may ex- times. The figure is modified from those provided by Robinson” press the opsin normally associated with and Rowe.%The branching topology and timing are approximated cones of a different morphological type.” from several sources, principally Meyer and zanl~ya.~~

OIL DROPLETS AND THEIR EVOLUTION In theory, an animal might derive col- One important example of such loss is in A variety of spectrally-selective filters exists our vision by comparing signals from eutherian mammals, where oil droplets are in animal eyes. Potentially, the most impor- receptors having identical photopigments completely absent. Gordon Walls’ sug- tant of these for colour vision are the oil but with differing types of oil droplets. No gested that oil droplet loss could be occa- droplets located in the inner segments of animals seem to have taken advantage of sioned by a shift from diurnal to noctur- cone photoreceptors. Many of these oil this possibility but oil droplets are known nal patterns and that, once lost, oil droplets are pigmented, acting as long-pass to significantly impact the character of droplets are hard to reacquire. The first spectral filters.36 The location of the colour vision that an animal derive^.^' of these ideas is eminently reasonable on passband varies across different types of oil Oil droplets are found in the retinas of grounds of visual efficiency and it receives droplets, giving them their conspicuously a wide variety of animals, suggesting that some support because although the reti- coloured appearance in fresh tissue. Func- oil droplets were also an early invention, nas of some nocturnal species retain oil tionally, oil droplets act to selectively filter possibly predating the emergence of ter- droplets, their droplets are unpigmented. incident light and yield three effects: restrial vertebrates (ca 400 MYA) .% Figure 2 As for whether oil droplets may be dXi- 1. effectively narrowing the absorption provides an account of the distribution of cult to reacquire, there seems to be no spectrum of the pigment lying behind it oil droplets among the vertebrates. A evidence one way or the other. 2. shifting the peak absorption of the notable feature is that oil droplets are rep On the other hand, there is clearly photopigment toward the longer wave- resented only sporadically across contem- lability in the pigmenting of oil droplets lengths porary vertebrates and a typical interpre- and their distribution across the retina, as 3. decreasing the overall absorption effi- tation of this fact is that some lineages have these properties can vary much as does the ciency of the pigment. lost oil droplets over the course of time. pattern of opsin expressi~n.~~*~~

Clinical and Experimental Optometry 87.4-5 July 2004 209 Evolution of colour vision Jacobs and Rowe

of the circuitry in the retina appears to separated from the cell body by a long thin NEURAL MECHANISMS AND THEIR have been conserved, at least among ter- axon. The dendritic arbor in turtle H1 EVOLUTION restrial vertebrates. This is true even in cells contacts cones presumably express- As there are neither molecular nor mammals despite their loss of photorecep- ing LWS, RH2, and SWS2. In primate H1 paleontological markers to provide infer- tor types and other specialisations. Al- cells, the dendritic arbor contacts M and ences about the comparator mechanisms though much could be said about each of L cones, that is, cones containing differ- that are a requirement for colour vision, the several classes of retinal cell, we focus ent forms of LWS pigments. Thus, the con- any understanding of the evolution of this here mainly on horizontal cells to point nectivity of the dendritic arbors is the same portion of the colour vision apparatus is out the sort of questions that should be in turtle and primate, given that mammals rudimentary. Spectrally-opponent neu- answered for all retinal cells in order to have no receptors expressing SWS2 or rons are widespread, perhaps even univer- understand the evolution of colour vision. RH2 pigments. The two cell types are not sally present, in contemporary vertebrates Horizontal cells receive direct input identical, as the telodendritic arbor of pri- and invertebrates known to have colour from photoreceptors, and by contacting mate H1 cells contacts only rods whereas vision. Their ubiquity alone implies they several cones of more than one type, they the telodendritic arbor of turtle H1 cells have a long evolutionary history. can contribute to the spatial and spectral connects with rods and LWS containing Invertebrates frequently display what is processing of visual information. cones. In mammal and turtle, H1 cells are called wavelength-selective behavi~ur.~~Svaetichin and MacNicho14*first demon- classified as L-type cells; they hyperpolar- This is defined by a compulsive linkage strated a likely role for these cells in spec- ise in response to light irrespective of wave- between some spectral input and a pattern tral processing when they showed that re- length. of behaviour; for example, escape behav- sponses of some teleost horizontal cells Turtle H2 horizontal cells receive inputs iour in the butterfly, Pieris, is selectively receive opponent input from cones of dif- primarily, if not exclusively, from cones elicited by ultraviolet lights4]Wavelength- ferent spectral type-a hallmark of colour that likely express RH2 and SWS2 pig- selective behaviour need not be learned vision. Cells exhibiting opponent behav- ment~.~~As the turtle retina retains the nor can it be altered by learning, as is the iour were called Gtype (chromaticity) and ancestral state of five photopigments, it is case for colour vision. Measurements of distinguished from L-type (luminosity), reasonable to conclude that the turtle H2 the spectral sensitivities of wavelength- the latter showing no indication of spec- horizontal cell is similarly retained from selective behaviour show that they require tral opponency. As it seems clear that some one of our earliest ancestors. Thus, mam- multiple pigments and that signals from horizontal cells in some animals play a role mals lost this cell type, when they lost RH2 these pigments interact in the nervous sys- in processing colour information, it makes and SWS2 pigments. tem. Many arthropods show evidence for sense to try to compare different horizon- Turtle H3 cells receive direct input from some wavelength-selective behaviour, tal cell types across different animals, to both SWSl and SWS2 cones and hyperpo- which can be present side by side with true learn how colour vision has evolved. larise in response to their stimulation. This colour vision. This fact has been taken to Above, we identified five families of opsin is similar to the behaviour of primate H2 suggest that neural mechanisms needed that are conserved across vertebrates. Are horizontal cells, which hyperpolarise in for wavelength-selective behaviour may there classes of horizontal cell that could response to stimulation of S cones. How- have predated the appearance of colour be used to indicate how the processing of ever, primate H2 cells have direct connec- vision.I6 There are no claims for wave- cone signals has evolved? The answer is tions with M and L cones and hyperpolar- lengthdependent behaviour in vertebrates, probably yes, but we have not progressed ise when they are stimulated as well.45This but that may reflect more of a lack of atten- as far in the quest to answer that question contrasts with turtle H3 cells that depolar- tion to the possibility than a reality. as we have in understanding the evolution ise as a response to stimulation by long of opsin genes. wavelength light. The turtle H3 cell’s long Comparative retinal form and Excluding mammals, vertebrates gener- wavelength response is mediated by indi- function ally have four horizontal cell types (Hl- rect contacts as LWS cones do not synapse As with the five families of vertebrate opsin H4). The structure and function of teleost onto H3 cells.43 genes, the basic neural circuitry of the horizontal cells dif€er in ways that make Are primate H2 cells homologues of vertebrate retina appears to have been es assignment to categories derived for ter- turtle H3 cells? If so, did primates add the tablished early in evolutionary history. The restrial vertebrates problematic, so we will direct M/L path while deleting the indi- neural retina of all vertebrates is divided not consider them further. We are reason- rect, opponent path from LWS cones, did into three layers containing cell bodies and ably confident that the mammalian H1 turtle H3 cells delete direct contacts with two layers composed primarily of intercel- type is homologous to the H1 type of tur- LWS cones while adding indirect contacts, lular connections. Retinal research of the tles. In both turtle43and mammal,44these or did the ancestral horizontal cell have past 30 years has allowed classification of cells have two electrically isolated neither direct nor indirect input from LWS retinal cells and their connections accord- arborisations: a dendritic arbor close to the cones? The indirect input for turtle H3 ing to both anatomy and function. Most cell body and a telodendritic arbor cells probably comes ultimately from

Clinical and Experimental Optometry 87.4-5 July 2004 210 Evolution of colour vision Jacobs and Rowe

double cones, so the major rewiring of the palaeontology indicates that early mam- both of these factors will influence the mammalian H2 horizontal cell may have mals were small and nocturnal. This basic acuteness of colour vision. For example, occurred as double cones were lost. The nocturnality has impacted indelibly on the domestic cats and human deuteranopes turtle H4 cell is little understood but also nature of mammalian vision. Unlike other have two types of cone pigment with spec- appears to get its major input from dou- groups of vertebrate, the retinas of the vast tral properties that are not greatly differ- ble cones45and hence, may have been lost majority of contemporary mammals are ent for the two species. With much higher from the mammalian retina at the same dominated by rod photoreceptors. In ad- cone densities and more robust spectral time that the mammalian H2 cell was dition to a dramatic alteration in the mix opponency, human dichromats have being rewired. Clearly, we have more ques- of rods and cones, there have been con- much more acute colour vision than cats. tions than answers but we believe these are spicuous losses of potential colour vision There are many other such examples to the sorts of questions that should be raised mechanisms. As noted above, the coloured reinforce the idea that although counting in an effort to understand the evolution oil droplets that characterise the colour opsin genes or photopigment types can of colour vision. More detail on the rela- vision machinery of many birds and rep provide predictions about colour vision, tionships of horizontal cells to colour tiles are missing from mammalian retinas they are far from the whole story. processing in vertebrate retinas is provided and two of the vertebrate cone opsin gene Figure 3 shows the tree topology of the elsewhere.45.46, families are not represented in eutherian LWS pigments for a number of representa- There is some information on the rela- mammals (SWSP and RH2,Figure 1) hav- tive mammals. In that figure the Amaxvalues tive numbers of cell types in reptilian and ing apparently been lost in the evolution for pigments of contemporary mammals mammalian retinas. Ammermdler and of this group. This reduction in the were obtained from in situ measurements K~lb~~found evidence for 13 bipolar cell number of potential cone photopigment while estimates of the peaks of the ances- types, 36 amacrine cell types and 24 gan- types and the loss of an important source tral pigments were derived from the five- glion cell types in the turtle retina. In a of selective spectral filtering has yielded sites rule for spectral tuning. By this ac- similar survey, Masland4’catalogued nine greatly simplified colour vision in mam- count, the ancestral LWS pigment of all to 11 bipolar cell types, 29 amacrine cell mals. mammals is estimated to have had a peak types and 10 to 15 ganglion cell types in a With the exception of primates (and, of about 530 nm.53 typical mammalian retina. These numbers possibly, some marsupials-see below) the We noted that phylogenetic relatedness are likely to represent lower limits, and loss of cone opsin genes means mammals has an impact on the spectral positioning turtle cell diversity is underestimated prob- have only two cone types, pigments of the cone pigments. Additional evidence ably even more than mammalian cell produced by SWSl and LWS gene repre- of that influence can be seen in mammals. diversity. The gross similarity between the sentatives. Thus, from a pigment perspec- For example, Figure 3 identifies the Am= numbers suggests either that the number tive, this limits most mammals to dichro- of the LWS cone pigment of the domestic of cone types is not a good indicator of matic colour vision. That dichromacy is the cat as being about 553 nm. This spectral the amount of processing that an animal mammalian mode is now well established location is very close to the LWS cone performs on colour signals or that mam- from behavioural studies and from cata- position of many different carnivores; mals, rather than shedding neuronal types, loguing mammalian phot0pigments.4’~~The including not only other felines but also co-opted them to process non-spectral as- LWS photopigments employed by differ- various canids and procyonids along with, pects of visual information. ent mammals are spread across a large interestingly, many marine carnivores Colour processing beyond the retina is spectral range (ca. 500 to 560 nm); simi- (pinnipeds). These carnivores inhabit a relatively unexplored in most animals. larly, the SWSl representatives appear in wide range of different photic habitats but Primates represent a notable exception. different mammals over the spectral range share in common the spectral positioning Research on that topic has been reviewed from about 360 to 440 nm. The relative rep of their only LWS cone pigment. recently4sand is covered elsewhere in this resentation of cones containing LWS and There are two recent twists to the mam- issue. SWSl pigmen&varies across species but gen- malian colour vision story relevant to the erally the former greatly outnumber the lat- issue of evolution. The first of these in- ter (by ratios of 10 to more than 1OO:l). volves the loss of function of the SWSl EVOLUTION OF MAMMALIAN Dichromatic colour vision may be the gene in a number of mammalian lineages. COLOUR VISION norm for mammals, but it is misleading to Although there were earlier indications Mammals diverged from other vertebrates assume that there are no differences in from physiological and anatomical work approximately 300 MYA, so roughly half colour vision among these dichromats. for an absence of an S cone in some spe- of their history as multi-cellular life forms Partly, this reflects the variations in the cies, it was from direct examination of comprises independent evolution. Over spectral positioning of the two cone SWSl opsin genes in two nocturnal pri- these subsequent millennia, Mammalia has classes. Beyond that, there are significant mate species that it first became clear that evolved into its current 18 orders and differences in cone density and cone dis- this loss reflects mutational changes in the more than 4,600 species. Evidence from tributions among mammalian retinas, and genes that have made them nonfunc-

Clinical and Experimental Optometry 87.4-5 July 2004 21 1 Evolution of colour vision Jacobs and Rowe

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.

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 Figure 3. A tree topology of mammalian LWS cone pigments (modified of the current understanding; more exhaus- from Yokoyama and Radlwhmer’). The numbers in parentheses indicate tive listings of original papers can be found the k- values for the pigment; the numbers beside the branches were in several recent reviews of this topic.6569 predicted from the five-sites rule, while those adjacent to common names The realisation that humans have tri- represent values obtained from in vitmrneasurements of cone pigments. chromatic 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 ti0na1.~~Unlike the very rare mutations A second complication is the recent dis- primates share the human colour vision that render human SWS genes inoperative covery that some marsupials appear to arrangement first became evident in an and lead to the colour vision defect called have three cone classes rather than the two early examination of monkey colour vi- tritanopia, the gene mutations detected in typical of most mammals. Specifically, two ion.^' In this pioneering study,” behav- these non-human primates were common Australian marsupials, the honey possum ioural tests of three species of Old World across individuals. The inescapable con- (Tussipes rostrutus) and the fat-tailed (catarrhine) monkey showed them to be clusion is that loss of SWSl related photo- dunnart (Sminthopsis crassicaudata) , have trichromats but similar tests of a New World pigment must have been adaptive. Soon been found to have three types of cone (platyrrhine) monkey indicated it is a after this discovery, a variety of other mam- pigment. One of these peaks in the UV. dichromat. Subsequent examinations of a mals, including some rodents and carni- The other two are around 505 nm and, range of catarrhine species show that all vores, were demonstrated to show a simi- depending on the species, at either 535 species from this group have very similar, if lar loss.55-56Perhaps most striking is the or 557 nm.61 The middle of these three not identical, trichromatic colour visi~n.~’.~~ widespread loss of function of the SWSl pigments is suggested to be an RH2 pig- Colour vision in platyrrhine monkeys gene in marine mammals. It appears that ment, although this has not been estab- differs dramatically from the catarrhine all cetaceans and pinnipeds lack func- lished. Thus, from a pigment perspective, standard and this difference has proven tional SWSl Thus, these ani- these marsupials have the basis for trichro- useful as an aid to understanding the evo- mals have only a single type of cone pig- matic colour vision. Whether they achieve lution of primate colour vision. The CIU- ment and perforce must lack colour that capacity remains to be seen. Although cia1 fact is that colour vision in platyrrhine vision. our knowledge of marsupial colour vision monkeys is highly polymorphic. Within Although the presence of SWSl is scanty, the arrangement found in these most such species, there are both dichro- pseudogenes is now clearly established in two species does not seem to be common matic and trichromatic individuals, and a number of mammalian lineages, how this to all marsupials. The tammar wallaby each of these classes includes variant may have come about is unclear. Various (Mucropus eugenit], for instance, has only forms. Early studies documented these explanations of the reasons for such loss two cone classes and dichromatic colour colour vision variations and showed they being adaptive have been offered but none visi0n.6**~~Nocturnal New World marsupi- could be directly traced to variations in of these seems very compelling. At present, als, such as the opossum, Didelphis sp, have LWS photopigments of these the loss of SWSl cone function in some so few cones that it is hard to conceive of In addition to an SWSl pigment common mammals remains an intriguing mystery. them being trichromatic or, indeed, of to all individuals, dichromatic monkeys

Clinical and Experimental Optometry 87.4-5 July 2004 21 2 Evolution of colour vision Jacobs and Rowe

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.74.75Such 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 Figure 4. The distribution of colour vision among primates. The and colour vision polymorphisms. How- nature of colour vision measured or inferred for a number of extant ever, among these polymorphic species, genera has been divided into three categories: routinely trichromatic; there are other important variations. One polymorphic; routinely dichromatic or monochromatic. See the text is that the set of allelic genes, and thus the for further details. The numbers identify the three taxonomic spectral positioning of the cone photopig- groupings referred to in the text (lstrepsirrbines,2-platyrrbines, 3- ments, varies in different lineages and this catarrbines). Tarsius (4) is currently considered as belonging in the will greatly influence the character of col- same sub-order (Hafilorhini) as the platyrrhme and catarrhine our vision beyond its dimensionality. An- monkeys. Figure adapted from Surridge, Osorio and M~ndy.~ 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 have two separate X-chromosome opsin seen in platyrrhines, allowing heterozygous Among other things, the number of alleles genes and so all individuals are trichro- females to have three cone photopigments can influence the incidence of female matic.8O and potential trichromacy.81-82 trichromacy. Finally, monkeys from two We know rather less about colour vision There are some variations in the densi- platyrrhine genera are not polymorphic. in the third major group of primates, the ties of cones and their retinal distributions One of these is Aotus, one of the noctur- more primitive strepsirrhines. Until re- among catarrhines and platyrrhines. With nal primates known to lack a functional cently, it was believed that strepsirrhines the exception of the nocturnal Aotus mon- SWSl pigment. These animals also have are either routinely dichromatic, like many key, which has low cone densities and lacks no LWS gene polymorphisms and so lack mammals, or that they lack colour vision a fovea, these variations are modest rela- colour vision.79The other exceptions are entirely as a result of non-functional SWSl tive to the large differences in the organi- the howler monkeys (Alouatta) that, sur- genes. It is now known that in addition to sations of the photoreceptor mosaics prisingly, have an opsin gene/photopig- these two forms some of the diurnal between these two groups and the strepsir- ment arrangement very similar to that of strepsirrhine species have X-chromosome rhines. The strepsirrhines have lower the catarrhine primates, for example, they opsin gene polymorphisms similar to those (often much lower) cone densities and

Clinical and Experimental Optometry 87.4-5 July 2004 213 Evolution of colour vision Jacobs and Rowe

they have no distinct foveal specialisations. revealed as a means to provide new col- vision has become a topic of great interest Irrespective of the dimensionality of colour vision capacities. As primates accom- in recent years. Following classical sugges- our vision, these differences predict much plish this starting from opsin gene arrange- tions, most of this focus is on the poten- less acute colour vision among the ments similar to those of most other tial uses of colour vision as an aid to the strepsirrhines than in the other two mammals, it is intriguing to know why no harvesting of food. The literature on this groups. other mammals have followed the primate topic is fascinating and currently under The primate phylogeny shown in lead and reacquired some of the colour rapid expansion but its review is beyond Figure 4 summarises what we know about vision lost by their ancestors. the scope of this paper. For insight into the distribution of colour vision among There are several possible explanations the ecology of primate colour vision a primates. The events leading to these vari- for this disparity but the most popular is number of recent sources may be con- ations in colour vision are still matters of that the primate retina is uniquely organ- sulted.w93 some uncertainty. The consensus is that ised to take immediate advantage of the the earliest primates had a single LWS pig- addition of new cone types.87 Crucial to Evolution in studying the ment (with a peak at perhaps around this argument is the presence of midget- evolution of colour vision 550 nm, as suggested in Figure 3) and an cell pathways in the primate retina that Recent years have seen great progress in SWSl pigment, the standard arrangement serve to conduct signals from cones our understanding of the evolution of col- for routine dichromacy. Some time after through the retina to P-type ganglion cells. our vision. This review has touched on the divergence of catarrhine and platyr- In the central portion of the retina, the areas well known and areas relatively un- rhine lineages, perhaps about 30 MYA,Ss receptive field centres of small P cells explored in efforts to understand what has the X-chromosome opsin gene in receive input from a single M or L cone, happened to this capacity throughout ver- catarrhines duplicated to yield genes that while their surrounding regions are pref- tebrate history. In doing so, we attempted coded for two spectrally discrete LWS pig- erentially dominated by either M or L cone to illustrate the wealth of facts available to ments (usually called L and M, respec- input. This imparts to the ganglion cell contemporary researchers, to point out tively). strong spectral opponency and provides new tools useful in this endeavour and to Whether polymorphism was a prelimi- the basis from which a dimension of col- highlight significant lacunae still needing nary to catarrhine gene duplication or our vision can subsequently emerge. attention. Much of the research discussed whether divergence occurred following It appears that the midget cell pathway here was necessarily focused on particu- the duplication is not yet established.68 is common to all catarrhine and platyr- lar molecules, types of cell or neural net- Because this duplication event occurred rhine primates, irrespective of the number works. Although all of these levels of analy- early in catarrhine evolution, all subse- of cone pigments they possess; indeed, sis are important, none taken in isolation quent catarrhines share their M and L there is evidence that an analogous organi- is sufficient to explain the evolution of a cone pigments. Most platyrrhines achieve sation also exists in retinas of strepsir- complex ability like colour vision. In the some partial trichromacy through poly- rhines8*This suggests that the midget cell end, the evolution of colour vision needs morphism at a single gene site. Sequence pathway must have arisen early in primate always to be viewed in the context of our comparisons suggest the platyrrhine evolution, possibly as an adaptation to sup understanding of colour vision as a sen- polymorphisms had a single origin and port higher spatial acuity. The argument sory capacity. that the gene duplication that led to rou- is that the presence of a new LWS pigment tine trichromacy in howler monkeys is a can be exploited without any additional DEDICATION relatively recent event that occurred inde- changes to the primate retina and imme- Dedicated to the memory of Russell L De pendently of the catarrhine gene duplica- diately yield novel spectral opponency. Valois (1926-2003), who made major ti~n.~”~There is evidence that the platyr- Support for this hypothesis comes from contributions to the understanding of rhine colour vision polymorphisms have the fact that, other than the number of colour vision. been adaptively maintained over consider- photopigment types, there are no known able periods of time.ffiOpsin gene polymor- differences in the organisation of retinas GRANTS AND FINANCIAL SUPPORT phism has emerged only sporadicallyin the of conspecific dichromatic and trichro- Preparation of this review was supported strepsirrhines (Figure 4) and there is de- matic monkeys?’ by a grant from the National Eye Institute bate on whether these polymorphisms The description of the steps involved in (EY002052). emerged independently of those occumng the evolution of primate colour vision in the anthropoid lines.’4**’ inevitably raises questions about the func- REFERENCES The evolution of primate colour vision tional utility of the various forms of colour 1. 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