Evolution of Colour Vision in Mammals Author(s): Gerald H. Jacobs Source: Philosophical Transactions: Biological Sciences, Vol. 364, No.

1531, The Evolution of Phototransduction and Eyes (Oct. 12, 2009), pp. 2957-2967 Published by: The Royal Society Stable URL: http://www.jstor.org/stable/40486064 . Accessed: 16/09/2013 17:26
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PHILOSOPHICAL TRANSACTIONS of *n

THE ROYALW' SOCIETY JLF

R. Soc. B (2009) 364,2957-2967 Phil.Trans. doi:10.1098/rstb.2009.0039

Review

Evolution of colour vision in mammals

Gerald H. Jacobs*
Neuroscience Research Institute and Department University ofCalifornia, ofPsychology, Santa Barbara, CA 93106, USA

enerin thedistributions ofspectral Colourvision allows animals to reliably differences distinguish vision is a for colour the not sufficiently widespread giesreaching eye.Although universal,capacity as a toolfor across theanimal to provide evidence ofitsimportance analysing facie kingdom prima on whichvertebrate and interpreting mechanisms the visualenvironment. The basic biological arehighly colourvision theconeopsingenesand thephotopigments rests, they specify, ultimately in striking varies ofthese basicelements conserved. Within that theutilization constraint, however, thecourseof evolution. in altered form and emerge during waysin thatthey appear,disappear variations in thevisualsystem, haveled to profound These changes, alterations alongwithother theevolin thenature This article concerns and salience ofcolourvision the vertebrates. among of relevant in the context ution ofcolour vision the that biological among mammals, viewing process ofcolourvision. in mammalian ofvariations colourvision, and oftheutility mechanisms, mammals trichromacy; Keywords:colourvision; dichromacy; opsingenes;photopigments; vertebrate 1. THE BEGINNINGS Of themajorcontemporary repregroups, have The earliest true mammalsevolvedfromtherapsid sentatives of all fourcone opsin gene families while and in various fishes ancestorsduring the Early Jurassic,somewhere beenfound birds, reptiles, in conaround 200 Ma. From the analysisof fossilsit is onlythree ofthesehaveso farbeen detected Mammals inferred that these were small animals that 2008). (Bowmaker usually temporary amphibians were almost certainly from thesestandards. nocturnal(Kemp 2005). A depart capacityfor colour vision requires,at minimum, sensors multiple having differing spectral absorption thatneed to be matedto a nervous properties system (a) Monotremesand marsupials martopresent daymonotremes, leading capable of contrasting signalsthat reflect photon The lineages in mammalian and eutherians in rates the different classes of sensors. early diverged supials absorption of these of the timing estimates in the fossil record to these evolution. Although Nothing speaksdirectly of mammalian events accounts but some hints can be from the history typically vary, traits, gleaned expandfromother ofthesensors vertebrate (figure 2) show monotremes diverging ingunderstanding underlying 166Ma, while marsupial colourvision, theconephotopigments, and theopsin mammalsapproximately and eutherians diverged approximately subsequently genesthatspecify photopigment proteins. Some twodecadesago, thegenesforhumancone 148Ma. and opsin of cone pigments Recentinvestigations opsinswereisolatedand sequenced(Nathanset al. shed some in and monotremes of cone from light marsupials genes 1986). Subsequent analysis opsingenes colourvision. of mammalian a largenumber ofcontemporary animals fostered the on the earlyevolution of cone opsingenesin themonotremes of opsingenephylogenies. The consen- Examination development sus is that all vertebrate (echidna) visual photopigments are Ornithorhynchus (platypus)and Tachyglossus 2 LWS and S WS specifiedby opsin genes belongingto five gene revealthe presenceof functional with et al. et al. Wakefield one linked to rod photopigments whilethe genes(Davies 2007; 2008) families, twogenes ofthese other fourunderlie cone pigments yielding pigments expression 2000; invitro (Yokoyama at 550 and 451 nm, Hisatomi& Tokunaga2002). All fourof the cone having absorption peaks (Amax) non(Davies et al. 2007). In addition, opsin gene familiesemergedat a point early in respectively can be detected. of an SWS1 functional remnants vertebrate as as 540 Ma gene evolution, perhaps long cone pigis thatat leastthree then, variation The implication, (Collin & Trezise 2004). Gene-sequence mammals in the earliest within each of these families present yieldsphotopigments mentswere likely from the SWSh SWS2, LWS genefamilies). that can be tuned to absorb preferentially across (drawn theSWS1 monotreme evolution, restricted 1, top). Duringsubsequent rangesof peak sensitivities (figure in it non-functional rendering gene degenerated, of this modern representatives lineage. of contemporary Examinations *jacobs@psych.ucsb.edu expand marsupials and view. Behavioural on this electrophysiological One contribution of 13 to a Theme Issue 'The evolution of isolated and eyes'. studiesof the Tammarwallaby(Macropus) phototransduction
2957 Thisjournal is 2009 The Royal Society

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2958

visionin mammals Evolution G. H. Jacobs Review. ofcolour

+ *a+
< Rhl SWS1 < -, / / LWS SWS2

]rod
cone

10 . 8 0.5 -

-"* J / *~v
* ' / '

in a classofcone.The latter gainssupport possibility has thatthe fat-tailed dunnart the observation from etal 2008). twocopiesoftheRhl opsingene(Cowing ofthe is evidence thatat leastthree In sum,there ofthevercharacteristic coneopsingenefamilies four in early mammals. Ofthese, were tebrates represented in the monotremes, but this an SWS2 genepersists some lost at was point subsequently gene family ofmarsupials and eutherians. to thedivergence prior Whether the pigmentproducts of Rh2 genes, in werepresent in manyothervertebrates, common uncertain. remains mammals early

(b) Eutherians fromtwo cone opsin gene families Representatives mammalsand, eutherian in contemporary appear 350 400 450 500 550 600 650 700 none of these of some primates, withthe exception (nm) wavelength derive morethana single animals type photopigment of fromeach of theirtwo gene families (SWS1 and opsinsare products photopigment Figure1. Vertebrate fiveopsingene families whatcone (top). In each of thesefamilies, LWS; figure 1). Giventhatcommonality, whoseAmax pigments yieldphotopigments ofthe in retinas the have been genesequencevariations present may indicated thespectral from valuesare drawn by the early eutherians? ranges of Sequence comparisons cone are those shown lines.The ranges of thehorizontal extent mammatheancestral that have suggested an 11-cw-retinal opsingenes constructed for using pigments appropriate families two these from drawn lian gene pigments of eutherian All of thecone photopigments chromophore. et al nm 360 about at in the (Hunt UV, peaked SWS1 two of thesegene families, come from mammals nm at 560 in the and wavelengths long 2001), from and LWS. It can be inferred genesequencecomparithe visual et al pigment 2008). Assuming in found (Yokoyama cone of two the that sons photopigments types of earlymammalswas 11-as-retinal, sensitivities chromophore of thisgrouphad spectral members ancestral the of contemporary as that the same mammals, at thebottom. bythecurves given would mammals of earlyeutherian cone pigments similarto those have had absorptionproperties of420 and 539 nm,an sketched twoclassesofconeswith Amax 1. offigure at thebottom dichromatic shown of the capableofsupporting the retinas arrangement are correct, If thesedeductions colourvision(Hemmi 1999; Hemmi et al. 2002). to thoseofthemajority weresimilar eutherians early ofthephoto- of contemporary (MSP) studies two types in containing Microspectrophotometric mammals detected ofconepigment. Australian other four of marsupials couldsupport Such an arrangement receptors contained dichromatic in each case the retinas cone types; three colour vision. Whetherit did would and an additionally sensitive and long-wavelength shortpigments depend on therehavingbeen at least with a peak close to somedegree thirdpigment intermediate ofthetwopigment ofselective expression etal. 2002, 2005). Based on itsspec- typesin separatereceptor 500 nm (Arrese classes, on these early was believedto mammals thislatter tralpositioning, to allow pigment a nervous organized system having Rh2 family a contrast the of an derive from ofcone,and opsin gene thetwotypes from of signals on one on them at least occasionally conducted experiments 1). Behavioural (figure encountering photic dunnart (Sminthopsis environments of thesespecies,the fat-tailed neural intenseto activate sufficiently cone three the that showed pigments two basic this that fact crassicaudata), The circuits. comparison vision colour trichromatic a capacity conserved is supported cone pigmentarrangement largely examin- amongcontemporary a subsequent et al 2006). However, to its attests mammals (Arrese strongly detected samespecies in this ofconeopsingenes ation to and ancestors eutherian our in adaptiveutility an SWS1 geneandan LWSgene, its probablerole in supporting twoconeopsin colour dichromatic genes, ofan Rh2gene vision thepresence for no evidence butfound mammals. in theseearly etal (2008) al et Cowing 2004). Recently, (Strachan in theseresults through have extended by showing, two these 2. CONE PIGMENTS AND COLOUR VISION that code, respectively, vitro genes expression, = 363 nm) and an LWS pig- IN CONTEMPORARY MAMMALS fora UV pigment (Amax colonize an mammalssuccessfully an absorption with ment peakof533 nm.The pigment Contemporary the vast For for the marsupials impressive range of naturalhabitats. picture photopigment gene/cone at 5000 that of the approximately clouded.It appears somewhat species, the thusremains majority source of an to access different three feature visualsystem important types leastsomemarsupials provides is here concern these The of third the information. that environmental of confirmation but conepigment, of If the is cone of nature the Rh2 with the of complements is a product pigment genefamily lacking. - how thesearrangements it theseanimals theRh2genefamily, is notfrom varyamong conepigment third as to 505variations at these what and this mammals that be imply may instead pigment(Amax may summarofcolourvision. of a secondLWS gene,so theadaptive Having 510 nm) is (i) theproduct utility aboutconepigments is known ofwhat or (ii) an Rhl rod pigment expressed izedabovemost farundetected,
0 ~

R. Soc. B (2009) Phil. Trans.

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visionin mammals G. H. Jacobs 2959 Review.Evolution ofcolour

All four families cone opsingenefamilies. ofthefour thedistribution 2. A vertebrate (SWS1, Figure phylogeny illustrating haveopsinsdrawn monotremes in vertebrate evolution. Of contemporary mammals, SWS2, Rh2,LWS) originated early cone Alleutherian SWS1 opsingene(asterisk). theseanimals also havea non-functional from theSWS2 and LWS families; the from have SWS1 and LWS. are drawn from two families representatives gene marsupials Contemporary pigments discussion. for further See thetext theRh2genefamily. SWS1 and LWS families from and,possibly, monotremesand and colour vision in contemporary marsupials, the further focus is on eutherian mammals.

(a) Cone pigmentcomplements in eutherianmammals or A variety havebeenused to measure oftechniques for a numberof infer complements photopigment mammalian species. The resultsfrommany such in earlierreviews studiesweresummarized (Jacobs 1993; Ahnelt& Kolb 2000; Kelber et al 2003). In recent been derived newinsights haveoften years of the from the developing understanding pathways and photopigment between specopsingenestructure tral sensitivity, an approachthathas provento be useful in characterizing species that, particularly havebeendifficult becauseoftheir orsize,would rarity to study methods. with traditional of of a variety The cone pigment complements 1 in table . The list mammals are given contemporary is not comprehensive, but does includeat leastone All ofthese each of 14 eutherian orders. speciesfrom of cone opsin are linkedto two families pigments has in turn genes,SWS1 and LWS. Each pigment to the beenplacedintoone offour groups according of peak sensiinferred or measured location spectral ultraviolet (UV), short (S), middle wavelength tivity:
Ph. Trans. R. Soc. B (2009)

(L). Someprimates (M), longwavelength wavelength or they fortheM and L pigments, are polymorphic are considered have both types;primates separately below. Some species also featurenon-functional SWS1 cone opsingenes('absent'in SWS1 pigment next. in table1). That issueis considered (b) Loss offunctionin SWS1 genes SWS1 opsingenesmap to chromoThe mammalian from withAmax some 7 and specify ranging pigments 445 nm (figure1). The 360 nm to approximately mammafrom at leastfour retinas ofscattered species lian orders(table 1) lack viable cones containing to thesegenes.It has long linked normally pigments tritanoas having humans that beenknown diagnosed colour vision defects, pia, one of the congenital S cones. of functional lack a population similarly it Withthe adventof molecular techniques genetic mutational have was learntthat many tritanopes them render in their S-coneopsingenesthat changes a similar and et al. non-functional expla1992), (Weitz for the to account found thereafter was shortly nation ofnon-human ofviableS conesintwospecies absence and thebushbaby the owl monkey (Aotus) primates, (Galago) (Jacobset al. 1996). In recentyears,a number of other mammalianspecies have been of these afflicted foundto be similarly (fora listing see Peichl animals, 2005).

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2960

Evolution G. H. Jacobs Review. ofcolourvisionin mammals

in some eutherian Table 1. Cone pigment mammals. complements order Rodentia exemplars Mus (mouse) Rattus(rat) (gopher) Geomys Cavia (guinea pig) (squirrel) Spermophilus rat) (African Cricetomys (rabbit) Oryctolagus Macaca (macaque monkey) Saimir(squirrel monkey) Aotus(owl monkey) Alouatta(howlermonkey) Galago (bushbaby) Lemur(ring-tailed) (sifaka) Propithecus Tupaia (treeshrew)
Eschrichtius(whale)

SWS1 pigmenta UV UV UV S S absent S S S absent S absent S S S

absent

LWS pigment3 M M M M M M/Lb M M+L poly (3) L M+L L L poly (2) L

L

reference Jacobsetal. (1991) Jacobset al (1991) Williamset al (2005) Parry& Bowmaker(2002) Jacobset al (1985) Peichl & Moutairou (1998) Nuboer etal (1983) Schnapfetal (1988) Mollon et al (1984) Jacobsetal (199 3b) Jacobsetal (1996a) Deegan II & Jacobs(1996) Jacobs& Deegan II (1993) Tan & Li (1999) Jacobs& Neitz (1986) Fasick et al (1998) Jacobset al (1994) Jacobset al (1994) Neitz & Jacobs(1989) Carrolletal (2001) Loop et al (1987) Jacobsetal (1993a) Calderone & Jacobs(2003) Levenson et al (2006) Calderone etal (2003) Levensonet al (2006) Levenson etal (2006) Wanget al (2004) Newman & Robinson (2006)
L. Peichl, personal Levenson & Dizon (2003)

Lagomorpha primate

Scandentia
Cetcea

Artiodactyla Perissodactyla Carnivora

Chiroptera Sirenia
Hydracoidea

(dolphin) Tursiops Bos (cow) Odocoileus (deer) Sus (pig) Equus (horse) Felis(cat) Canis (dog) Mustela(ferret) Ursus(bear) Crocuta(hyena) Phoca (seal) (otter) Enhydra fox) (flyng Pteropus Trichechus (manatee)
Procavia (hyrax)

absent S S S S S S S S UV/S absent S UV S

UV/S

L L M L L L L L L M/L L L L L
M/L

Proboscidea Afrosoricida Soricomorpha

Loxodonta (elephant) (tenrec) Echinops Sorex(common shrew)

S UV/S UV/S

L M/L M/L

communication Yokoyamaet al (2005) Peichl etal (2000) Peichl et al (2000)

are definedas: UV peak (<400 nm); S peak (400-450 nm); M peak (510-540 nm); L peak (>540 nm). categories aPigment the use of opsin immunochemical are givenforpigmentsdetectedthrough labelling.At presentthattechniqueneither bDual designations betweenpigments allows a distinction havingUV and S peaks, nor betweenthose thathave M and L peaks.

a relaa condition Unlike only impacting tritanopia, to be no more of humans(estimated tivehandful than1 in 10000), the absencesof S cones frequent arevery mammals in theseother species'traits. likely loss of S cones for this gene-driven Explanations elusive.The nonto thispoint,somewhat remain, discovered first was this in whom humanprimates contrisince that nocturnal are strongly suggesting are principally S-conesignals from to seeing butions usefulat linkedto colourvision,a capacity mostly of the characteristic those than levels higher light theirabsence of theseanimals, visualenvironments have little impacton visualsuccess.Many of might shownto be without the otherspeciessubsequently thesame thus S conesare also nocturnal, promoting it is curis the that explanation, If,however, linkage. mammals ious as to whyso manyothernocturnal a complement intable1) retain somelisted (including these that thefact S cones.Further, offunctional gene the populations have spreadthroughout mutations thattheloss of S conesmayin allowsthepossibility visualfitness. somewayenhance of a number it is notthenorm, In sum,although mammalian species have lost their S-cone
R. Soc. B (2009) Phil Trans.

as a result of opsin gene mutation. photopigments across mutationdiffers The natureof the inactivating groups of such animals, and the loss has occurredat different stages of lineage evolution,sometimesnear the base of the radiation,sometimesin more derived lines (Levenson et al. 2006). This loss of function withthe photic activity shows some correlation cycle, describedas nocin speciestypically beingseen mostly turnal,but thatbehaviouris not alwayslinkedto such loss. Indeed, ifitwere,itseemspossiblethatfunctional SWS1 geneswould have been lost to all contemporary mammals given the long nocturnal phase of early mammalian evolution. Because this loss is seen in species, animals oftensharinglittle widely divergent or photic in common withregardto eitherphylogeny there are probably multiple circumenvironment, stances that permit,or even support,a gene-driven loss of a complete cone class and along with it the potentialfora dimensionof colour vision. (c) Spectral positioning of mammalian cone pigments The retinasof most eutherianmammals featuretwo classes of cones- one containingan SWS1 pigment,

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Review.Evolution visionin mammals G. H. Jacobs 2961 ofcolour

a pairing that inallcasesso theother an LWS pigment, which feature presenceof freshurinary markings the pigment basis fora single heightened farstudiedprovides UV reflectivity (Chavez et al. 2003). In ofcolour vision. The relative dimension of possiblefunctional spectral posi- the only directexamination varieswidelyamong utility of the cone pigments of mammalian UV cones, it was foundthat tioning to askifthere aresomepar- foraging micebehave mammals anditis natural with inthepresence indifference that or of food-relevant of their vision these absence ticular UV signals(Honkavaara might explain aspects fromthe idea that pigment et al. 2008). Whether variations. UV sensitivity some Proceeding mayoffer have is some alternative not known is and thus there is investigators advantages positioning adaptive, to this that no for a alone eutherquestion currently explanation approach why, pursued modelling among of natural a number ofrodents withspectral measurements haveretained starts UV objects ian mammals, asks cones. and then,through and illuminants calculation, shouldprovide the best combinations whatpigment & forcolourdiscrimination substrate (e.g. Lythgoe 1996; Chiao (d) Roles for rods 1989; Osrio & Vorobyev Partridge ofthemodels The retinas of all mammals containboth rods and theassumptions etal 2000). Although but there are in these exercises of the outcomes agree cones, impressive speciesvariations generally vary, > nm the relative of the two 400 thatwithan SWS pigment representation havingAmax receptor types. that these in the spectral It has longbeenknown variations generally (denotedas S in table 1), variations withthenormal of the its longest to its correlate of the LWS cone from photicenvironment positioning oftheanatomy and a recent modest animal, shortest study quantitative 1) havesurprisingly (figure position andperipheral ofthevisual discrimination colour on predicted effects parts system capabilities. ofthecentral that in a number of nocturnaland diurnal species itappears conditions most for In addition, viewing there are largeniche-specific to shift theS pigment establishes beneficial that, indeed, (i) itwouldnotprove in the variations for and that thelonger towards (Kaskanetal. complement receptor purwavelengths (ii) The of the retina to environmental in dichromatic these discrimination colour of 2005). response poses For instance, eventhough the pressures can be dramatic. to increase it is generally advantageous systems nocturnal rat has eight the a smaller it has the two of retina, irrespective pigments, separation spectral diurnal times morerodsthandoes thehighly environment. ofthephotic ofthedetails ground - in ratabout 1 per centof all receptors are that these models reasonably predict squirrel Assuming forthe ground conditions cones,whilethe comparable undernatural colourvisionperformance figure 86 per cent.At least two is approximately eutherian squirrel in theancestral and thattheLWS pigment there to thisdisparity. linked seem 560 nm differences at approximately First, mammal had a Amax from the retina fibres more are this of carrying output many 1), it is not obviouswhytheposition (figure thanin therat. in theground the coloursignals towards been shifted has very squirrel frequently pigment ratio should be of thoseaspects Second, since the signal-to-noise Consideration shorter wavelengths. conepopulations, across colourdoes improved thatdo notinvolve vision signals ofmammalian bysumming to be expected in local cone density of increases those features might not seem to help. In mammals, visual in the colour of salience the enhance luminance of on utilization based are that signals seeing in variations Both of thesefeatures the LWS system. are supported predict differences by signalsfrom Formaltestsof of the colour capacity. illuminant quantal robustness spectra, (s). For daylight pigment thisidea. Bothratand seemto support by havingthe cone pigment colourvision captureis maximized ofcone and bothcan have two the types shiftedas far as possible towards squirrel longer ground colourvision, dichromatic have to shown be terrestrial common For other formally photic wavelengths. in demonstrate to much easier is that but a filtered for capacity through light environments, instance, in the coneit is than cone-rich the same the is about squirrel ground environment, quantalcapture leafy etal. 2001). & Yolton1971; Jacobs forall LWS pigment (Osrio & Vorobyev poorrat (Jacobs positions of number the on focus studies no be to seems there at usually In Comparative genshort, present 2005). but for ofspectral cone typesand on theirspectral forthediversity sensitivity, eraladaptive explanations an undervision ofcolour abouttheutility mammals. predictions oftheLWS conesin dichromatic positions is also rod/cone the of seemto provide standing apt to be weighting Thus far, relationships phylogenetic relevant. LWS the of ofthepositioning thestrongest highly predictor in vision colour mammalian Rodscanalsoinfluence mammalsand this may pigmentin dichromatic rods visual In all direct more demands of visual systems, consideration detailed duplex that ways. suggest mammalian and cones operatein commonovera considerable and opportunities byspecific experienced in thecase for illuminances: ofretinal on thisissue. someleverage example, range provide might lineages To date thesemodelshave not been appliedto of humanvisionacrosssome fourlog unitsof light locations havemultiple Rod andconesignals evaluate those rodents that have UV pigments intensity. course and retina in the interaction they (table 1). UV signalsare knownto play important of potential visual central into the shared ofsomevertebrates, behaviours output pathways inthevisual roles par- along influto shown can be rod In this that in birds,and thatlinkage system. humans, signals suggests ticularly in colour ence has There ways(Buck2004); perception complex mayalso be the case fortheserodents. rodand ofviewing conditions undertheright on thisissue.One suggestion in fact, beenlittle investigation additional an to contrasted be can cone rodents yield signals conditions, is thatunderphotopiclighting & Pokorny ofcolourvision(Smith 1977). the dimension UV conesto detect their from use signals might
R. Soc. B (2009) Phil. Trans.

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2962

visionin mammals Evolution G. H. Jacobs Review. ofcolour

Rod influences on colour vision remainvirtually of butgiven thatmany in other unstudied mammals, underlighting mostactive thesespeciesare normally conditions thatshouldsupport jointrod and cone colour to mammalian rod contributions function, outto be ofgreat vision importance. maywellturn (e) Primate colour vision is a special case are ofcone pigments three (or more)types Although mammals in eutherian commonamongvertebrates, and even have threecone pigments, onlyprimates universal. is farfrom amongthemthatarrangement Research conductedin recent years has greatly and of the distribution advancedour understanding the to vision. References colour ofprimate evolution "~ | o can these on articles . now numerous /* _ topics original reviews in several recent be found 10 (Reganetal. 2001; (c) | /^' Osrioetal. 2004; Jacobs 2007, 2008). The first primates appeared at 80-90 Ma / ' & Murphy et al. 2007; Springer (Bininda-Emonds / ' 0.5 theidea is sometimes (e.g. disputed 2007). Although are generally Tan et al. 2005), theseearlyprimates believedto have been nocturnal (Martin& Ross 2005), and thus, like those of most eutherian 0 featured retinas their single mammals, probably fromthe SWS1 and LWS pigments representative colourvision. dichromatic supporting gene families, becamediurnal, many lineages primate Subsequently, and seton vision an enhanced 0.5' dependence fostering y and in photopigments tingthe stageforalterations are on colourvision.LWS opsingenesin mammals All contemporary catarrhine theX-chromosome. priU " havetwo mates(Old World monkeys, apes,humans) LWS genes that are positionedin a head-to-tail 700 650 600 450 550 400 500 These genesspecify discrete tandem array. spectrally (nm) wavelength cone pigments(Amax values of approx. 530 and inprimate conephotopigment 3. Variations arrange560 nm, usuallytermed M and L). In conjunction Figure howler andtheplatyrrhine ments, All catarrhine (a) primates withan SlFS-derived this provides three pigment, triof that classes cone have three support pigments monkey conepigments that for a capacity trichromatic support have vision, chromatic colour monkeys (b) Many platyrrhine colour vision 3a) . The M andL photopigments (figure and all malemonkeys colourvisionin which wereapparently derived from oftheorig- polymorphic duplication of three M/L-cone females pigments homozygous get any inal X-chromosome opsin gene (Nathans et al. inconjunction with theS pigment (dashed lines)which supSince this is not ports 1986). arrangement three-pigment dichromatic colour vision. Female monkeys platyrrhine sharedwithmembers of the othermajor that generally and areheterozygous haveany pairoftheM/Lpigments Aotus and aretrichromatic, anthropoidgroup, the New World platyrrhine they (c) The platyrrhine monkey but is commonto all catarrhines, of strepsirrhine haveonlya single cone the a number monkeys, primates and thuslack a colourvisioncapacity, X-chromosome is believed to photopigment (d) opsingeneduplication Some havetwotypes ofconephotomonkeys strepsirrhine haveoccurred at thebase ofthecatarrhine radiation, and dichromatic colour vision. pigment some30-40 Ma. In distinction to theseOld World primates, platyrrhine feature morevaried monkeys opsingene/colour on their X-chromosomes and, for them, the early vision arrangements. Most of the species in this developmental process of random X-chromosome grouphave X-chromosome opsin-gene polymorph- inactivationresults in a retina that contains three threealternative versions of classes ofcone pigments. Since thereare three isms,typically featuring possible theLWSgene,eachofwhich a conepigment pairingsof the LWS pigments,there are also three specifies witha Amax in the rangeof approximately 530 and typesof heterozygous females.When theyare tested 560 nm (figure animals having each of these types of 3b). Such an arrangement yieldsa behaviourally, totalof six discrete Male pigmentarrays are foundto have colour visionthatis photopigment pheno types. and homozygous females monkeys express anyone of predictablefromthe pigmentcomplement,i.e. anithethree LWS opsingenesand, in conjunction with mals with two pigmentsare dichromatic, those with theSWS genecommon to all individuals, thenhave threeare trichromatic (Jacobs 2007). combinations oftwophotopigments. Two generaofplatyrrhine this anyofthethree monkeys departfrom femaleshave different LWS genes general polymorphicpattern.As already noted, the Heterozygous
0 "

c-Xf W'

Phil. Trans. R. Soc. B (2009)

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Review.Evolution ofcolourvisionin mammals G. H. Jacobs 2963

has a non-functional nocturnal owlmonkey Scase M/L pigment was preliminary to (Aotus) polymorphism has onlya singletypeof routine opsingeneso thisprimate (Dulai etal. 1999). trichromacy cone pigment Thereis no evidence forevolution of a third cone 3c) and thuslacksthecapacity (figure forconventional colourvision(Jacobset al. 19936). pigment in anynon-primate eutherian mammal. One on theother The howler of a new hand,is possiblereason for this is that survival (Alouatta), monkey in havingtwo different pigment similarto the catarrhines may depend on the priorpresenceof an X-chromosome and of cones and on a nervous opsingenes separate populations appropriate population M L ofconescontaining and that is so S, 3a), pigments (figure system organized as to be ableto takeadvancolour vision for trichromatic of the added pigment Jr. (Arajo allowing tage any information may etal. 2008). Howler aretheonly The retinas of manymammals contain monkeys platyrrhine provide. only to haveachieved conepopulations. In suchcases,signals monkeys species-wide trichromacy. small emerging The third ofprimates, themore handful ofreceptors a large group primitive from onlya relative containing an evenmorevaried of newpigment inreliably ineffective strepsirrhines, presents picture might prove supportand thusmayfail opsin genes and cone photopigments. Examplesof inganynewdiscriminatory capacity threedifferent are listedin table 1. to evolve. And evenifthere is a sufficient arrangements population to the of cones,acquisition of a new colourvisioncapacity Some,suchas thebushbaby Galagoaresimilar in having a non-functional owl monkey thatsignals from thenew cone typebe S-opsingene also requires Such and a singleL pigment animals with those fromanothercone 3c). (figure neurally compared Another is exemplified class. There are two circuits lackcolourvision. in mammalian retinas presumably which hasa func- known to support lemur such comparisons catta) (Lemur (Martin1998; bythering-tailed and a singleL pigment, an Lee 2004). One involves tionalS-cone pigment a class of ganglion cell that colour vision receives from S/UVconesand M/ dichromatic antagonistic inputs predicting arrangement in strep- L conesresulting in a spectrally hasbeendetected variant 3d). A third opponent signal being (figure . In addition to fedforward intothevisualsystem. suchas theSifakas sirrhines (Propithecus) Opponent signals feature two poly- of thistypeare capableof supporting a capacity for theseanimals an S-conepigment, colour vision not evaluated & Lennie The other LWS (Solomon 2007). Although yet pigments. morphic from females circuit theantagonistic combination of that itseems heterozygous originates behaviourally, likely from M L in the and cones so-called different forms of trichrotwo will have from this signals midget group theevidence is limited, thefirst similar to thepolymorphic cellsystem. maticcolourvision while, Although ofthese circuits is believed tobe common totheretinas females willbe males and homozygous platyrrhines, whilethesecondarrangeof all eutherian dichromats. mammals, obligate Becausethemidget cell that some primate mentis uniqueto primates. This briefaccountillustrates in species from all three of has beenidentified lineages have been able to expand their colour system those that have the of other mamcharacteristics those including large primate groupings, beyond capacities ofM/Lcone,it has beensuggested thus onlya single class of cone pigment, mals by addinga third type inprimate hisevolved themidget cellsystem dimension of that an additional themto achieve early allowing visualacuity, and to support colour vision.What factors heightened perhaps mighthave supported tory, neural subthen an efficient that itspresence thischange? provided theemergence ofa novelM/Lpigment so that thespectral strate, in opsingenescan change Alterations ofcolour vision a newdimension Atminimum, immediately ofphotopigments. yielded absorption properties the absenceof a midget of a single (Wassle2004). In thisview, in thesubstitution thatresults a mutation other thanpriin theretinas ofmammals to producea spectral cellsystem can be sufficient nucleotide of the factor is an mates that encoded shiftin the photopigment limiting expansion important gene by absence such Evidence that colour vision. their If this al. et Nathans & may 1994). 1993; Asenjo (Merbs in a is contained not presentan absolutebarrier a mutated selection, genethencomesunderpositive were thatmice whose retinas in recentdemonstration will emerge of the pigment version polymorphic class of cone pigment to contain a third underlies engineered sucha scenario thepopulation. probably Just this of the LWS genes did gain some novelcolourvisioneventhough thehigh-frequency polymorphism etal. cellsystem lacksa retinal and strepsirrhine seen in some platyrrhine (Jacobs midget primates. species in cases like thisis thatany 2007). limitation A potential of priwhatfeatures Giventhesebuilding linkedto the presenceof a new blocks, visual advantages of a new dimension the evolution mate life of the members all shared be alelecannot equally supported by idea thatsince ofthenewpig- of colour vision?It is a long-held Fullspecies representation population. and since ripened are can be achieved ment frugivores, many primates opsingeneduplication, through theevolchromatic offer distinctive fruits can evolution. in catarrhine as apparently signals, early happened unclearwhether It remains polymor- ution of the dimensionof primatecolour vision photopigment linked to the is causally of colour vision supported whichsupporta mixture by M/L pigments phisms, of fruits inter- harvest standas a typical in thepopulation, (e.g. Regan et al. 2001). In recent phenotypes modelsof colour of computational a number or years, mediate trichromacy stageon thewayto routine theprimate whether to test have been vision thetwoarrangements whether employed independent represent the discrimito underlie suited are well M/L Details of the arrangement pigments trajectories. evolutionary consistent The in embedded of fruits nation howler in the foliage. oftheX-chromosome opsingenearray 1996; to achieve theonlyplatyrrhine species-wide answeris thattheyare (Osrio & Vorobyev monkey, al. et et al. one However, in this least 2002). at that 2001; Parraga Regan imply strongly trichromacy,
R. Soc. B (2009) Phil. Trans.

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2964

visionin mammals Evolution G. H. Jacobs Review. ofcolour

also showthatthereare other 3. MAMMALIANCOLOUR VISION: THE model computations classes of criticalbehaviours,for example dis- COMPARATIVE CONTEXT histheearly occurred that ofevents in skin As a result of ediblefoliage or of variations crimination during two retain mammals eutherian of well servedby tory mammals, whichwouldbe similarly only coloration, in found families cone four the vision of many the M/L dimension of primate colour opsingene thissame time othervertebrates. during likely Very (Dominy& Lucas 2001; Changiziet al 2006). So oil droplets of coloured the elaborate alone are incapable frame, thatmodelstudies it appears system far, vertebrates in of characteristic life of those of clearly many photoreceptors aspects primate identifying of the a was as were also vision. colour their of specific evolution the that abandoned, portion impacted colourinforto processing dedicated howpri- retinal in trying to understand Another circuitry approach how mation(Jacobs& Rowe 2004). These changesleft is to examine evolved vision matecolour directly of dimension witha single mammals For this mosteutherian colourinformation. animals exploit behaving this Primates vision. colour haveprovided escaped thepolymorphic subsequently platyrrhines purpose, alteraofvisualsystem a series sincewe knowthat(i) opsin restriction an invaluable byevolving resource, for that tions vision the colour for expanded provided opportunities responsible genepolymorphisms thatare quitevariable These changes, have been main- colourvision. in platyrrhine variations monkeys includea greatly overlongperiodsof time across different selection tainedby natural lineages, primate cones of enhanced and al et organized al densely et population 2003) 1998; Surridge (Boissinot of a third to arounda centralized in thesespeciesare forced fovea,the addition monkeys (ii) individual of and the appearance colour vision capacities typeof cone photopigment, different deploystrikingly of the facilitates that comparison common to achieve goals. Studiesof retinalcircuitry life-supporting classes. cone different from animals signals whether such speciescan ask, forinstance, of other with in comparison Viewed animals, arebetter many colourvision alternative with arrangements elaborate more much which feature run In tests adaptasks. peripheral or worse at particular foraging itis perhaps colour for trichromatic information, undersemi-natural extracting conditions, monkeys tations as described are mammals that foods efficient at more to be routinely appropriate predigathering proved colour vision(e.g. Goldsmith dichromatic havingimpoverished were cuesthan catedon theuse ofcolour the however, simplicity, 2006). Despiteits apparent (Caine & Mundy 2000; Smithet al conspecifics of a colourvisioncapacity thattrichro- maintenance such outcomes throughout imply 2003). Although thatit mammals of eutherian of efficiency thelonghistory in the service argues macycould haveevolved mamin role a useful have must thatthe otherresearch in foodharvesting, supporting played suggests the about success. malian For than that. more judgements Comparative complicated storymay be are vision colour mammalian of limitations relative made on of several sets observations instance, monkeys it is but the include to extended sometimes causal found no in circumstances natural primates, feeding for is this less clear that a lot status and effivision between colour Consider, justified. step relationships human testconditions thatunderstringent in foraging example, ciency (Dominyet al 2003; Smithet al can be shownto make reliablecolour thisconclusion trichromats 2003; Vogelet al 2007). Supporting ofas differences based on wavelength offruit is a recent examination oftheefficiency gather- discriminations as 0.25 nm (Mollon et al 1990), and thatthe thatalso little {Ateies) ingin polymorphic spider monkeys and total numberof surfacecolours that trichromatic detectedno differences betweendichromatic ofapproximately be upwards can discern trichromatic animals(Hiramatsu et al 2008). This humans may itseems & is 2.3 million that focused on 1998). So far, (Pointer Attridge experiment specifically foraging thatanyother an arms notto havebeen demonstrated conductedover veryshortrange (within species and the physical feature of the target fruits can match these ratherimpressive performances. length) of primate the majorstrength that best predictedforaging was not In any case, perhaps efficiency of the keenness luminance a cue that colourvisioncomes not just from colour,but rather contrast, whichare considerable, should be equally to trichromatic anddichro- their discrimination available abilities, a haveevolved from thefactthatprimates matic viewers etal 2008). It may be noted butrather (Hiramatsu use to allows them brain that and thatshort-range such as thisalso allowsfor large, agile plastic foraging of waysgenerally in a multitude the exploitation of various non-visualcues (e.g. colourinformation limited central more with to those et al unavailable 2001). species Dominy Researchers havehad little in capability. difficultyidentifying processing thatmight potential advantages explainwhycolour I thank for referees Roweand three anonymous Mickey vision evolvedin the way that it has among the of this reviewwas Preparation helpfulcomments. but so farhavehad less successin demon- supported primates, from the National Eye Institute by a grant which among these may hold greater (EY002052). strating whether set of ciror,indeed, importance anysingle cumstancesmay provide a general explanation. Futurestudies on thistopicwillno doubtcontinue REFERENCES to exploitthe exceptional for study Ahnelt, opportunities P. 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Phil. Trans. R. Soc. B (2009)

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R. Soc. B (2009) Phil Trans.

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