evolution colour vision mammals

7/27/2019 Evolution Colour Vision Mammals

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Evolution of Colour Vision in MammalsAuthor(s): Gerald H. JacobsSource: Philosophical Transactions: Biological Sciences, Vol. 364, No. 1531, The Evolution ofPhototransduction and Eyes (Oct. 12, 2009), pp. 2957-2967Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/40486064 .

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PHILOSOPHICALTRANSACTIONS- of *nTHE ROYALW'SOCIETY JLF Phil.Trans. . Soc.B (2009) 364,2957-2967doi:10.1098/rstb.2009.0039Review

Evolution of colour vision inmammalsGerald H. Jacobs*Neuroscience esearchnstitutendDepartmentfPsychology,niversityfCalifornia,Santa Barbara,CA 93106, USAColourvision llows nimals oreliablyistinguishifferencesnthedistributionsf pectralner-giesreachinghe ye.Althoughotuniversal,capacityor olour ision ssufficientlyidespreadacross he nimal ingdomoprovide rimaacie vidence f ts mportances a toolfor nalysingand interpretinghe visual nvironment.he basicbiologicalmechanismsn which ertebratecolour ision ltimatelyests,he oneopsingenes nd thephotopigmentshey pecify,rehighlyconserved. ithin hat onstraint,owever,heutilizationf hese asic lementsariesnstrikingways nthat hey ppear, isappearndemergen altered orm uringhe course f evolution.Thesechanges, longwith ther lterationsnthevisual ystem,ave ed toprofoundariationsinthenature nd salience f colour ision mong hevertebrates.his article oncernshe vol-ution f olour isionmonghemammals,iewinghat rocessnthe ontextf elevantiologicalmechanisms,fvariationsnmammalianolour ision,ndoftheutilityfcolour ision.Keywords: olour ision; psingenes; hotopigments;ichromacy;richromacy;ammals1. THE BEGINNINGSThe earliest ruemammals volved rom herapsidancestorsduringthe Early Jurassic, omewherearound 200 Ma. Fromthe analysis f fossils t isusually nferredhatthesewere small animals hatwere almostcertainly octurnalKemp 2005). Acapacityforcolour visionrequires, t minimum,multipleensors aving ifferingpectral bsorptionpropertieshatneed to be mated o a nervousystemcapable of contrastingignalsthat reflect hotonabsorptionates n the differentlasses of sensors.Nothingn the fossil ecord peaksdirectlyo thesetraits,ut omehints an begleaned rom he xpand-ingunderstandingf he ensors nderlyingertebratecolour ision,he onephotopigments,nd theopsingenes hat pecifyhotopigmentroteins.Some twodecades go,thegenesforhuman oneopsinswere solated nd sequenced Nathans t al.1986).Subsequent nalysisfconeopsingenes roma largenumber fcontemporarynimals osteredhedevelopmentfopsingenephylogenies.he consen-sus is thatall vertebrateisualphotopigmentsrespecified y opsin genes belonging o fivegenefamilies,ne linked o rodphotopigmentshile heother our nderlieonepigmentsYokoyama000;Hisatomi& Tokunaga 002). All fourof the coneopsin gene families merged t a point early nvertebratevolution, erhapsas long as 540 Ma(Collin & Trezise2004). Gene-sequence ariationwithin ach of these families ieldsphotopigmentsthat can be tuned to absorbpreferentiallycrossrestrictedanges fpeaksensitivitiesfigure , top).*[email protected] contributionf 13 to a Theme Issue 'The evolution fphototransductionndeyes'.

Ofthemajor ontemporaryertebrateroups, epre-sentativesf all four one opsin genefamilies avebeen foundn various irds, ishesndreptiles, hileonly hree f thesehave o far eendetectedn con-temporarymphibiansBowmaker008). Mammalsdepart rom hese tandards.(a) Monotremes nd marsupialsThelineageseadingopresent aymonotremes,ar-supials nd eutheriansivergedarlyn mammalianevolution. lthoughstimatesf thetimingf theseevents ary,ccounts f mammalianistoryypically(figure ) showmonotremesivergingrom thermammals pproximately66Ma, whilemarsupialand eutheriansubsequentlyiverged pproximately148 Ma.Recent nvestigationsf conepigmentsnd opsingenes nmonotremesndmarsupialshed ome ighton theearly volutionf mammalianolourvision.Examinationf coneopsingenes nthemonotremesOrnithorhynchusplatypus) nd Tachyglossusechidna)reveal he presence f functionalWS and SWSgenes Davieset l. 2007;Wakefieldt l. 2008)withinvitroxpressionf hese wo enes ieldingigmentshaving bsorption eaks Amax)t 550 and 451nm,respectivelyDavies et al. 2007). In addition, on-functionalemnantsf n SWS1gene anbe detected.The implication,hen,s that t least hree onepig-mentswere ikely resentn theearliestmammals(drawn rom he SWSh SWS2,LWSgenefamilies).During ubsequentmonotremevolution,heSWS1gene degenerated, enderingt non-functionalnmodern epresentativesfthis ineage.Examinationsfcontemporaryarsupialsxpandon thisview. Behavioural nd electrophysiologicalstudies f the Tammarwallaby Macropus)solated

2957 This ournals 2009 TheRoyal ociety

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2958 G. H. Jacobs Review. volution f olour isionn mammals+ *a+ ]rod

SWS1 Rhl< -, < / cone/ SWS2 LWS/-"* ~vJ10 . *8 0.5 - ' / '0 ~

350 400 450 500 550 600 650 700wavelengthnm)Figure . Vertebratehotopigmentpsins reproducts ffive psingenefamiliestop). In each of thesefamilies,genesequence ariationsieldphotopigmentshoseAmaxvalues redrawn romhe pectralangesndicatedytheextentfthehorizontalines.The rangeshown re thoseappropriateor igmentsonstructedsing n 11-cw-retinalchromophore.llof theconephotopigmentsf eutherianmammals omefrom woof thesegenefamilies,WS1andLWS. t canbe inferredrom ene equence ompari-sonsthat hetwotypes fconephotopigmentsoundnancestralmembersfthisgrouphad spectralensitivitiesgiven y he urvest thebottom.two lasses fconeswithAmaxf420 and539nm, narrangementhownapable f upportingichromaticcolourvision Hemmi1999; Hemmiet al. 2002).MicrospectrophotometricMSP) studiesf he hoto-receptorsffour ther ustralian arsupialsetectedthree onetypes;n eachcase theretinasontainedshort-nd ong-wavelengthensitiveigmentsndanintermediatehirdpigmentwitha peak close to500nm Arreset l. 2002,2005). Basedonits pec-tralpositioning,his atter igment as believed oderivefroman opsin gene of the Rh2 family(figure). Behaviouralxperimentsonductednoneof these pecies, hefat-tailedunnartSminthopsiscrassicaudata),howed hat hethree one pigmentssupported trichromaticolour vision capacity(Arresetal 2006). However, subsequentxamin-ation f oneopsin enesnthis ame pecies etectedtwo one psin enes,nSWS1gene nd nLWSgene,butfound oevidenceor hepresencef nRh2gene(Strachant l 2004).Recently,owing tal (2008)haveextendedheseresults y showing,hroughnvitroxpression,hathesewo enes ode, espectively,for UV pigmentAmax363nm)andan LWSpig-mentwithnabsorptioneak f533nm.Thepigmentgene/conehotopigmenticture orthemarsupialsthusremainsomewhatlouded. t appears hat tleast omemarsupialseaturehree ifferentypes fconepigment,utconfirmationhat he hirdf heseis a productftheRh2genefamilys lacking.f thethirdonepigments notfromheRh2genefamily,tmayinsteadbe thatthispigmentAmaxt 505-510nm) s (i) theproductfa secondLWSgene, ofarundetected,r (ii) an Rhl rodpigmentxpressed

ina classof cone.The latter ossibilityains upportfromhe observationhat he fat-tailedunnart astwo opies f heRhlopsin ene Cowingt l 2008).In sum, heres evidence hat t least hree f thefour oneopsin enefamiliesharacteristicf hever-tebrates ere epresentednearlymammals. fthese,an SWS2 genepersistsn themonotremes,utthisgene familywas subsequentlyost at some pointprior othedivergencefmarsupialsnd eutherians.Whetherthe pigmentproductsof Rh2 genes,commonnmany ther ertebrates,erepresentnearlymammalsemainsncertain.(b) EutheriansRepresentativesrom wocone opsin genefamiliesappear in contemporaryutherianmammals nd,with heexceptionfsomeprimates,one oftheseanimals erivemore han single hotopigmentypefrom ach of their wo genefamiliesSWS1 andLWS;figure ). Given hat ommonality,hat onepigments ayhavebeenpresentntheretinasftheearlyeutherians?equence comparisons f coneopsin enes ave uggestedhat he ncestral amma-lian pigments rawnfrom hesetwogenefamiliespeaked n theUV, at about 360nm (Hunt et al2001), and in the long wavelengthst 560nm(Yokoyamat l 2008). Assuminghevisual igmentchromophoref earlymammalswas 11 as-retinal,the same as thatof contemporary ammals, hecone pigmentsf early utherianmammalswouldhave had absorption ropertiesimilarto thosesketchedtthebottomffigureIf thesedeductionsrecorrect,heretinasf theearlyutheriansere imilaro those f themajorityofcontemporaryammalsn containingwotypesofconepigment.uchanarrangementould upportdichromaticolourvision.Whethert did wouldadditionallyependon therehaving een at leastsomedegreef electivexpressionf he wo igmenttypes n separatereceptor lasses,on theseearlymammals aving nervousystemrganizedoallowa contrastfsignals romhetwo ypes fcone, ndon themat leastoccasionallyncounteringhoticenvironmentsufficientlyntense o activate euralcomparisonircuits. he factthatthisbasic twocone pigmentarrangements largelyconservedamong ontemporaryammalstronglyttestso itsadaptiveutilityn our eutherianncestors nd toits probable ole in supportingichromaticolourvisionn these arlymammals.2. CONE PIGMENTS AND COLOUR VISIONIN CONTEMPORARY MAMMALSContemporary ammals uccessfullyolonize animpressiveangeof naturalhabitats. or the vastmajority f the approximately000 species,thevisual ystemrovidesccessto an importantourceof environmentalnformation.he concern ere swiththe nature f cone pigment omplementsfthese nimals howthese rrangementsary mongmammalsndwhat hese ariations ay mplys tothe daptive tilityf colour ision.Having ummar-ized bovemost fwhatsknownbout onepigments

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



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Review. volutionfcolour isionn mammals G. H. Jacobs 2959

Figure . A vertebratehylogenyllustratinghedistributionfthefour oneopsingenefamilies. ll four amiliesSWS1,SWS2, Rh2,LWS) originatedarlynvertebratevolution. f contemporaryammals,monotremesaveopsinsdrawnfrom he WS2 and LWSfamilies;hese nimals lsohave non-functionalWS1opsingene asterisk).ll eutherianonepigmentsre drawn rom wo familiesSWS1 and LWS. ContemporaryarsupialsavegenerepresentativesromheSWS1 and LWS familiesnd,possibly,romheRh2genefamily.ee the ext or urtheriscussion.and colour visionin contemporarymonotremes ndmarsupials, the further focus is on eutherianmammals.(a) Conepigmentcomplementsin eutherianmammalsAvarietyftechniquesavebeen used to measure rinfer hotopigmentomplementsor a number fmammalianpecies.The results rommanysuchstudieswere summarizedn earlier eviewsJacobs1993; Ahnelt& Kolb 2000; Kelber et al 2003).In recent ears ew nsightsaveoften een derivedfrom hedevelopingnderstandingf thepathwaysbetweenpsin ene tructurendphotopigmentpec-tralsensitivity,n approach hathas proven o beparticularlyseful in characterizingpecies that,because f heirarityr ize,would ave eendifficulttostudywith raditional ethods.The cone pigment omplementsf a varietyfcontemporaryammals regivenn table1 The listis notcomprehensive,ut does include t leastonespecies rom ach of 14 eutherianrders. ll ofthesepigmentsre linked o two families f cone opsingenes,SWS1 and LWS. Each pigment as in turnbeenplaced nto ne offour roups ccordingotheinferredr measuredpectralocation fpeaksensi-tivity:ltravioletUV), shortwavelengthS), middlePh. Trans.R. Soc. B (2009)

wavelengthM), longwavelengthL). Someprimatesarepolymorphicor heM andL pigments,r theyhave bothtypes; rimatesre consideredeparatelybelow. Some species also featurenon-functionalSWS1 coneopsingenes 'absent' n SWS1 pigmentin table1). That ssue s consideredext.(b) Loss of unction n SWS1 genesThe mammalianWS1 opsingenesmapto chromo-some7 andspecifyigments ithAmaxangingrom360 nm to approximately45 nm (figure ). Theretinas f catteredpecies rom t east ourmamma-lian orders table 1) lack viablecones containingpigmentsormallyinked o thesegenes. t has longbeenknown hat umans iagnosedshavingritano-pia, one of the congenital olourvisiondefects,similarlyack a population f functional cones.Withtheadvent f molecular enetic echniquestwas learntthatmanytritanopes ave mutationalchangesn their -coneopsingenes hat enderhemnon-functionalWeitzt l. 1992), nda similarxpla-nationwasshortlyhereafteround o account or heabsence fviable cones ntwo pecies fnon-humanprimates,heowlmonkeyAotus) ndthebushbaby(Galago) (Jacobset al. 1996). n recentyears,numberof othermammalian pecies have beenfound o be similarlyfflictedfor listingftheseanimals,ee Peichl 005).



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2960 G. H. Jacobs Review. volution f olour isionnmammalsTable 1 Cone pigment omplementsn some eutherianmammals.order exemplars SWS1 pigmenta LWS pigment3 referenceRodentia Mus (mouse) UV M Jacobs t al. (1991)Rattusrat) UV M Jacobs tal (1991)Geomysgopher) UV M Williams tal (2005)Cavia (guinea pig) S M Parry& Bowmaker2002)Spermophilussquirrel) S M Jacobs tal (1985)CricetomysAfrican at) absent M/Lb Peichl & Moutairou 1998)Lagomorpha Oryctolagusrabbit) S M Nuboer et al (1983)primate Macaca (macaque monkey) S M+L Schnapf t al (1988)Saimir squirrelmonkey) S poly 3) Mollon et al (1984)Aotus owlmonkey) absent L Jacobs t al (199 3b)Alouattahowlermonkey) S M+L Jacobs t al (1996a)Galago bushbaby) absent L Deegan II & Jacobs 1996)Lemurring-tailed) S L Jacobs& Deegan II (1993)Propithecussifaka) S poly 2) Tan & Li (1999)Scandentia Tupaia tree hrew) S L Jacobs& Neitz (1986)Cetcea Eschrichtius whale) absent L Levenson & Dizon (2003)Tursiopsdolphin) absent L Fasick et al (1998)Artiodactyla Bos (cow) S L Jacobs t al (1994)Odocoileusdeer) S M Jacobs tal (1994)Sus (pig) S L Neitz& Jacobs 1989)Perissodactyla Equus horse) S L Carroll t al (2001)Carnivora Felis cat) S L Loop et al (1987)Canis (dog) S L Jacobs t al (1993a)Mustela ferret) S L Calderone& Jacobs 2003)Ursusbear) S L Levenson etal (2006)Crocutahyena) UV/S M/L Calderoneet al (2003)Phoca seal) absent L Levensonet al (2006)Enhydraotter) S L Levensonet al (2006)Chiroptera Pteropusflyng ox) UV L Wanget al (2004)Sirenia Trichechusmanatee) S L Newman & Robinson 2006)Hydracoidea Procavia (hyrax) UV/S M/L L. Peichl, personalcommunicationProboscidea Loxodontaelephant) S L Yokoyama t al (2005)Afrosoricida Echinopstenrec) UV/S M/L Peichl etal (2000)Soricomorpha Sorex commonshrew) UV/S M/L Peichlet al (2000)aPigment ategories redefined s: UV peak (540 nm).bDual designationsre givenforpigments etected hrough heuse ofopsin immunochemicalabelling.At present hattechniqueneitherallowsa distinctionetweenpigments avingUV and S peaks,nor between hosethathaveM and L peaks.

Unlikeritanopia,conditionmpactingnly rela-tivehandful f humans estimatedo be no morefrequenthan1 in 10000), the absences fS conesinthese thermammalsreveryikelypecies' raits.Explanationsor thisgene-drivenoss of S conesremain,o thispoint, omewhatlusive.The non-humanprimatesn whomthiswas first iscoveredare stronglyocturnaluggestinghat incecontri-butions o seeing rom -cone ignals reprincipallylinked o colourvision, capacitymostly seful tlight evelshigher hanthosecharacteristicf thevisualenvironmentsfthese nimals, heir bsencemight ave ittlempact n visual uccess.Manyofthe other pecies ubsequentlyhown o be withoutS cones re alsonocturnal,huspromotinghe amelinkage.f,however,hats theexplanation,t s cur-ious as to why o many thernocturnalmammals(includingome istedntable1) retain complementoffunctionalcones. urther,he act hat hese enemutations ave spreadthroughouthe populationsallows hepossibilityhat he ossofS conesmay nsomeway nhance isual itness.In sum, lthought s notthenorm, numberfmammalian species have lost their S-conePhil Trans.R. Soc. B (2009)

photopigments s a resultof opsin gene mutation.The natureof the nactivatingmutation ifferscrossgroupsof such animals,and theloss has occurred tdifferenttagesof lineage evolution, ometimesnearthebase oftheradiation, ometimesn more derivedlines (Levenson et al. 2006). This loss of functionshowssome correlationwith hephoticactivityycle,being eenmostlynspeciestypicallyescribed s noc-turnal, utthatbehaviour s notalways inked o suchloss. ndeed, f twere, tseemspossible hat unctionalSWS1 geneswouldhave been lostto all contemporarymammals given the long nocturnalphase of earlymammalianevolution.Because this loss is seen inwidelydivergent pecies, animalsoften haring ittlein commonwithregard o either hylogenyrphoticenvironment, here are probablymultiple circum-stances thatpermit,or even support,a gene-drivenloss of a completecone class and along with t thepotential or dimension fcolourvision.(c) Spectral positioning ofmammaliancone pigmentsThe retinasofmost eutherianmammalsfeature woclasses of cones one containing n SWS1 pigment,



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Review. volution fcolour ision nmammals G. H. Jacobs 2961the ther n LWSpigment,pairinghat nall cases ofar tudied rovideshepigment asis for singledimensionfcolour ision. he relativepectral osi-tioning f the cone pigments arieswidely mongmammalsnd t snaturalo ask f here re omepar-ticularspects f heir ision hatmight xplainhesevariations.roceeding rom he idea thatpigmentpositionings adaptive,some investigatorsavepursued modelling pproach o thisquestion hatstartswith pectralmeasurementsfnatural bjectsand illuminantsnd then, hroughalculation,skswhatpigmentombinationshouldprovide he bestsubstrateor olourdiscriminatione.g. LythgoePartridge 989; Osrio & Vorobyev 996; Chiaoet l 2000). Althoughhe ssumptionsfthemodelsvary,heoutcomes fthese xercises enerallygreethatwithan SWS pigment avingAmax 400nm(denoted s S in table1), variationsn thespectralpositioningf theLWS conefromts ongest o itsshortestositionfigure ) havesurprisinglyodesteffectsnpredictedolour iscriminationapabilities.Inaddition,ormost iewingonditionst ppearshat(i) itwouldnotprove eneficialoshiftheS pigmenttowardshe ongerwavelengthsnd (ii) that or ur-posesofcolourdiscriminationn thesedichromaticsystemst is generallydvantageouso increase hespectraleparationfthe twopigments,rrespectiveof hedetails f hephotic nvironment.Assuminghatthesemodelsreasonably redictcolourvisionperformancendernatural onditionsandthat heLWSpigmentn the ncestralutherianmammalhad a Amax t approximately60nm(figure ), it is not obviouswhy heposition fthispigmentasvery requentlyeenshiftedowardsheshorter avelengths.onsiderationfthoseaspectsofmammalianision hat o not nvolveolour oesnot seemto help. In mammals, hosefeaturesfseeingthatare based on utilizationf luminancedifferencesre supportedy signals rom he LWSpigments). For daylightlluminantpectra,uantalcaptures maximized y having he cone pigmentshifted s far as possible towardsthe longerwavelengths.or othercommonterrestrialhoticenvironments,or nstance,ight ilteredhroughleafynvironment,uantal aptures about he amefor ll LWS pigment ositionsOsrio& Vorobyev2005). In short,tpresenthereeems obe nogen-eral daptivexplanationsor hediversityfspectralpositionsf heLWScones ndichromaticammals.Thus far, hylogeneticelationshipseemtoprovidethe trongestredictorf thepositioningftheLWSpigmentn dichromaticmammals nd this maysuggesthat etailedonsiderationfvisualdemandsandopportunitiesxperiencedy pecific ammalianlineagesmightrovideome everagenthis ssue.To date thesemodelshavenotbeen appliedtoevaluatethose rodentsthat have UV pigments(table1). UV signals re known o play mportantrolesnthe isual ehavioursf omevertebrates,ar-ticularlynbirds, ndthat inkageuggestshat hismayalso be thecase fortheserodents. herehasbeen ittlenvestigationn this ssue.One suggestionis thatunderphotopic ightingonditions,odentsmight se signals romheir V conesto detect hePhil.Trans.R. Soc. B (2009)

presenceof fresh rinarymarkings hich featureheightenedV reflectivityChavezet al. 2003). Inthe onlydirect xamination f possiblefunctionalutilityf mammalian V cones, t was found hatforaging icebehavewithndifferencenthepresenceor absence ffood-relevantV signalsHonkavaaraetal. 2008). Whether V sensitivityay fferomealternativedvantagessnot knownnd thus here scurrentlyoexplanationorwhy,lone mong uther-ianmammals, number frodents averetained Vcones.(d) RolesforrodsThe retinas f all mammals ontain othrods andcones,but there reimpressivepeciesvariationsnthe relativeepresentationf the tworeceptor ypes.It has ongbeenknown hat hese ariationsenerallycorrelate ith he normal hotic nvironmentf theanimal,nd a recentuantitativetudyf he natomyof he entralndperipheralarts f hevisual ystemin a number of nocturnal nd diurnalspeciesestablisheshat, ndeed, here re argeniche-specificvariationsn thereceptoromplementKaskan tal.2005). The response f the retina o environmentalpressuresanbe dramatic.or nstance,ven houghit has a smaller etina, henocturnal at has eighttimesmore ods handoesthehighlyiurnal roundsquirrelin rat bout1 percentofall receptorsrecones,whilethecomparable igure or thegroundsquirrels approximately6 percent. At least twodifferenceseem inked o thisdisparity.irst, herearemanymore utput ibresrom heretinaarryingcolour ignalsntheground quirrelhan n therat.Second, since the signal-to-noiseatio shouldbeimprovedy ummingignalscross onepopulations,increasesn localconedensitymight e expectedoenhance hesalience fcolour ignalsn thevisualsystem. othofthesefeaturesredict ariationsnrobustnessf the colourcapacity. ormal testsofcolour ision eem osupporthis dea.Bothrat ndgroundquirrelave wo ypes fconeandboth anbe formallyhown ohavedichromaticolour ision,butthatcapacitys much easierto demonstratenthecone-richroundquirrelhan t s in the cone-poorrat Jacobs Yolton 971;Jacobs tal. 2001).Comparativetudies sually ocus n thenumberfcone types nd on their pectralensitivity,utforpredictionsbout heutilityf olour isionn under-standingftherod/cone eightings also aptto behighlyelevant.Rods analso nfluence ammalianolour isionnmoredirectways. n all duplexvisual ystems,odsand conesoperate n common vera considerablerange fretinallluminances:or xample,n the aseofhumanvision cross omefour ogunits f ightintensity.od andcone ignals avemultipleocationsofpotentialnteractionn theretinandthey oursealong hared utput athwaysnto hecentral isualsystem.nhumans,od ignalsan be showno nflu-encecolour erceptionncomplex aysBuck2004);infact, nder herightonditionsfviewingod ndconesignals anbe contrastedoyield n additionaldimensionf colour isionSmith Pokorny977).



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2962 G. H. Jacobs Review. volution f olour isionn mammalsRod influences n colour vision remainvirtuallyunstudiednothermammals,utgiven hatmany fthese pecies renormally ost ctive nder ightingconditions hat houldsupportointrod and conefunction,od contributionso mammalian olourvisionmaywell urn utto be ofgreatmportance.(e) Primatecolourvision s a special caseAlthoughhreeormore) ypes f conepigmentsrecommon mongvertebrates,n eutherianmammalsonlyprimates avethree one pigments,nd evenamong hem hat rrangements farfrom niversal.Researchconducted n recentyearshas greatlyadvanced urunderstandingf the distributionndevolutionfprimateolourvision.Referenceso thenow numerousriginalrticles n these opics anbe foundnseveralecenteviewsRegan t l. 2001;Osrio t l. 2004;Jacobs 007,2008).The first primates appeared at 80-90 Ma(Bininda-Emondst al. 2007; Springer Murphy2007). Althoughhe dea s sometimesisputede.g.Tan etal. 2005), these arly rimatesregenerallybelieved o have been nocturnalMartin& Ross2005), and thus, like those of most eutherianmammals, heirretinasprobablyfeatured inglerepresentativeigments rom he SWS1 and LWSgenefamilies,upportingichromaticolourvision.Subsequently,any rimateineages ecamediurnal,fosteringn enhanced ependencenvision ndset-ting hestagefor lterationsn photopigmentsndcolourvision. WS opsingenes n mammals reontheX-chromosome.llcontemporaryatarrhineri-matesOldWorldmonkeys,pes,humans) ave woLWS genes that are positionedn a head-to-tailtandemrray. hesegenes pecifypectrallyiscretecone pigmentsAmax alues of approx.530 and560nm,usually ermedM and L). In conjunctionwithan SlFS-derived igment,hisprovides hreeconepigmentshat upport capacityor richromaticcolour isionfigurea) TheM andL photopigmentswere pparentlyerived rom uplicationftheorig-inal X-chromosome psin gene (Nathans et al.1986). Since this hree-pigmentrrangements notgenerallyharedwithmembers f theothermajoranthropoidgroup, the New World platyrrhinemonkeys, ut is common to all catarrhines,heX-chromosomepsingene duplications believed ohaveoccurredt thebaseofthecatarrhineadiation,some30-40 Ma.In distinctiono theseOld World rimates,latyr-rhinemonkeyseature ore aried psingene/colourvisionarrangements. ost of the speciesin thisgrouphaveX-chromosomepsin-gene olymorph-isms, ypicallyeaturinghree lternativeersions ftheLWSgene, achofwhichpecifiesconepigmentwith Amaxn therange fapproximately30 and560 nm (figure b). Such an arrangementieldstotalof sixdiscretehotopigmenthenoypes.Malemonkeysndhomozygousemalesxpress ny neofthethree WSopsingenes nd, n conjunction iththeSWS genecommon o all individuals,henhaveany fthe hree ombinationsftwophotopigments.Heterozygous emaleshave differentWS genes

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/ '0.5 / '0 -

0.5 y 'U "400 450 500 550 600 650 700wavelengthnm)

Figure . Variationsnprimateonephotopigmentrrange-ments,a) All atarrhinerimatesnd he latyrrhineowlermonkeyave hreelasses f onepigmentshatupportri-chromaticolour ision,b)Many latyrrhineonkeysavepolymorphicolour isionnwhich ll malemonkeysndhomozygousemales et anyof threeM/L-cone igments(dashed ines)whichnconjunctionith he pigmentup-ports ichromaticolour ision. emale latyrrhineonkeysthat reheterozygousave ny air f heM/Lpigmentsndtheyre richromatic,c)Theplatyrrhineotusmonkeynda number fstrepsirrhinerimatesaveonly single onephotopigmentnd thus ack a colourvision apacity,d)Somestrepsirrhineonkeysave wo ypes f conephoto-pigmentnd dichromaticolour ision.on theirX-chromosomesand, for them,the earlydevelopmental process of random X-chromosomeinactivation esultsin a retina that contains threeclasses of conepigments. ince there re three ossiblepairingsof the LWS pigments, hereare also threetypesofheterozygous emales.When they re testedbehaviourally,nimalshavingeach of thesetypesofpigment rrays refoundto have colour visionthat spredictablefrom he pigmentcomplement, .e. ani-mals with two pigments re dichromatic,hosewiththree retrichromaticJacobs2007).Two genera fplatyrrhine onkeys epart rom hisgeneralpolymorphic attern.As alreadynoted, the

Phil. Trans. . Soc. B (2009)



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Review. volution f olour ision nmammals G. H. Jacobs 2963nocturnalwlmonkeyAotus) as a non-functional-opsingeneso thisprimate as only single ype fconepigmentfigurec) andthus acks hecapacityfor onventionalolourvisionJacobs t al. 19936).The howlermonkeyAlouatta),n theother and, ssimilar o the catarrhinesn having wo differentX-chromosomepsingenes ndseparate opulationsofcones ontaining,M andL pigmentsfigurea)allowing or trichromaticolour vision ArajoJr.et l. 2008). Howlermonkeysre theonly latyrrhinemonkeysohave chievedpecies-widerichromacy.The thirdarge roup f rimates,hemore rimitivestrepsirrhines,resentsn evenmore aried icturefopsin genesand cone photopigments.xamples fthreedifferentrrangementsre listed n table 1.Some, uch s thebushbaby alago re similaro theowlmonkeynhaving non-functional-opsin eneand a singleL pigmentfigure c). Such animalspresumablyackcolour ision.Anothers exemplifiedby he ing-tailedemurLemuratta)which as a func-tionalS-conepigmentnd a singleL pigment,narrangementredicting ichromaticolour vision(figured).A third ariantas beendetectednstrep-sirrhinesuch s the ifakasPropithecus)In additionoan S-conepigment,hese nimals eature wopoly-morphicWS pigments. lthoughotyet valuatedbehaviourally,t seemsikelyhat eterozygousemalesfromhis roupwill ave wo ifferentormsf richro-matic olour isionwhile, imilar o thepolymorphicplatyrrhines,ales and homozygousemaleswill beobligateichromats.This brief ccount llustrateshat someprimatelineageshave been able to expand their colourcapacitieseyondhose haracteristicsfothermam-malsby adding third lassof conepigment,husallowinghem o achieve n additional imension fcolourvision.Whatfactorsmighthave supportedthis hange?Alterationsnopsingenes anchange he pectralabsorptionropertiesfphotopigments.tminimum,a mutationhat esultsnthe ubstitutionf a singlenucleotide an be sufficiento produce spectralshift n the photopigmentncodedby thatgene(Merbs& Nathans 993;Asenjo tal. 1994). If thismutatedenethen omesunder ositiveelection,polymorphicersion f thepigment illemergenthe opulation.ustuch scenariorobablynderliesthehigh-frequencyolymorphismf theLWSgenesseen n someplatyrrhinend strepsirrhinerimates.A potentialimitationn cases like this s that nyvisualadvantagesinked o thepresence f a newalele annot e equallyhared yallmembersfthepopulation.ull pecies epresentationf henewpig-ment anbe achievedhroughpsin eneduplication,as apparentlyappened arlyn catarrhinevolution.It remains nclearwhetherhotopigmentolymor-phisms,which upport mixturef colourvisionphenotypesnthepopulation,tand s a typicalnter-mediate tageon thewayto routinerichromacyrwhetherhe wo rrangementsepresentndependentevolutionaryrajectories.etailsofthearrangementoftheX-chromosomepsingene rrayn thehowlermonkey,heonly latyrrhineo achieve pecies-widetrichromacy,tronglymplyhat t least n thisonePhil.Trans.R. Soc. B (2009)

case M/LpigmentolymorphismaspreliminaryoroutinerichromacyDulai et l. 1999).There s no evidence or volutionf a third onepigmentnanynon-primateutherian ammal. nepossiblereasonforthis s thatsurvival f a newpigmentmaydependon thepriorpresence f anappropriateopulation f cones and on a nervoussystemhat sorganizedo as to be ableto take dvan-tage of any informationhe added pigmentmayprovide. he retinas fmanymammalsontain nlysmall onepopulations.n such ases, ignalsmergingfromnly relative andfulfreceptorsontainingnew igment ight roveneffectivenreliablyupport-ing nynewdiscriminatoryapacitynd thusmay ailto evolve.And even fthere s a sufficientopulationofcones, cquisitionf a new colourvision apacityalsorequireshat ignals rom he newconetype eneurally omparedwith those from nother oneclass. Thereare twocircuitsn mammalianetinasknown o supportuchcomparisonsMartin1998;Lee 2004). One involves class ofganglionell thatreceivesntagonisticnputs rom /UV ones ndM/L conesresultingn a spectrallypponentignal eingfedforwardnto hevisual ystem. pponentignalsofthis ype recapableofsupportingcapacityorcolourvision Solomon& Lennie2007). The othercircuitriginatesromhe ntagonisticombinationfsignals romM andL cones n theso-calledmidgetcellsystem. lthoughheevidences limited,hefirstof hese ircuitss believedo be common o the etinasof all eutherian ammals, hile he second rrange-ment s uniqueto primates.ecause themidgetellsystemas been dentifiednspecies rom ll three fthe arge rimate roupings,ncludinghose hat aveonly single ype f M/Lcone, t has beensuggestedthat hemidgetell ystemvolvedarlynprimateis-tory, erhapsosupport eightenedisual cuity,ndthat tspresencehen rovidednefficienteural ub-strate,o that heemergencefa novelM/Lpigmentimmediatelyielded newdimensionf colour ision(Wassle 004). In thisview, heabsence f a midgetcellsystemntheretinas f mammalsther han ri-matess an importantactorimitinghe xpansionftheir olourvision. vidence hat uchabsencemaynot present n absolutebarriers containedn arecent emonstrationhatmicewhose retinaswereengineeredo contain third lass of conepigmentdid gainsome novel olourvision venthoughhisspeciesacks retinalmidgetell ystemJacobst l.2007).Given hesebuilding locks,whatfeaturesfpri-mate ife upportedhe volutionf newdimensionof colourvision? t is a long-helddea that sincemany primates re frugivores,nd since ripenedfruitsanoffer istinctivehromaticignals,he vol-utionof the dimension f primate olour visionsupportedyM/Lpigmentss causallyinked o theharvestffruitse.g. Reganetal. 2001). In recentyears, number fcomputational odelsof colourvision ave een mployedo testwhetherhe rimateM/Lpigmentsrewell uitedo underliehediscrimi-nation f fruitsmbeddednfoliage. he consistentanswer s thatthey re (Osrio& Vorobyev996;Reganet al. 2001; Parraga t al. 2002). However,



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2964 G. H. Jacobs Review. volution f olour isionn mammalsmodelcomputationslso showthat here re otherclasses of criticalbehaviours, or example dis-criminationfediblefoliage r of variationsn skincoloration,hichwouldbe similarlyell served ythe M/L dimensionof primatecolour vision(Dominy& Lucas 2001; Changizi t al 2006). Sofar,tappears hatmodel tudies loneare ncapableof clearlydentifyinghoseaspectsof primateifethatmpactedhe volutionf heirolour ision.Anotherpproachntryingo understandowpri-mate olour ision volveds to examine irectlyowbehavingnimalsxploitolournformation.orthispurpose,hepolymorphiclatyrrhinesaveprovidedan invaluableesource,inceweknow hat i) opsingenepolymorphismsesponsibleor he olour isionvariationsn platyrrhineonkeys avebeen main-tained ynatural electionver ongperiods ftime(Boissinot t al 1998; Surridge t al 2003) and(ii) individual onkeysnthese pecies reforcedodeploystrikinglyifferentolourvisioncapacitiesto achieve ommonife-supportingoals.Studies fsuchspecies an ask,for nstance, hethernimalswith lternativeolour ision rrangementsrebetteror worseat particularoragingasks. n testsrununder emi-naturalonditions,richromaticonkeysprovedo be more fficienttgatheringoodspredi-cated n theuseof olour uesthanwere ichromaticconspecificsCaine & Mundy2000; Smithet al2003). Althoughuch outcomesmply hat richro-macy ouldhave evolvedn the service fefficiencyin foodharvesting,ther esearchuggestshat hestorymay be more complicated han that. Forinstance,everalets f bservationsade nmonkeysfeedingn natural ircumstancesound no causalrelationshipsetween olourvision tatus nd effi-ciencynforagingDominy tal 2003; Smith t al2003;Vogel tal 2007). Supportinghis onclusionis a recent xaminationf he fficiencyffruitather-ing npolymorphicpidermonkeysAteies)hat lsodetectedno differencesetweendichromaticndtrichromaticnimals Hiramatsut al 2008). Thisexperimentocused pecificallyn foraginghat sconducted ververy hortrange within n armslength) nd thephysical eature f thetarget ruitsthat best predictedforaging fficiency as notcolour,but rather uminance ontrast, cue thatshould eequallyvailableotrichromaticnddichro-matic iewersHiramatsut l 2008). Itmay e notedthat hort-rangeoraginguchas this lso allows orthe exploitationf various non-visual ues (e.g.Dominyt l 2001).Researchersavehad little ifficultynidentifyingpotential dvantageshatmight xplainwhy olourvisionevolved n thewaythat t has amongtheprimates,ut so farhavehad less success n demon-stratingwhich among these may hold greaterimportancer, ndeed,whetherny ingle etofcir-cumstancesmay providea general explanation.Future tudies n this opicwillno doubtcontinueto exploit he exceptional pportunitiesorstudyoffered y the polymorphic latyrrhine onkeys,whilehaving o paycloser ttentiono thephysicaldetailsof theviewing nvironmentperative or arange fnatural ehaviours.Phil Trans.R. Soe. B (2009)

3. MAMMALIANCOLOUR VISION: THECOMPARATIVECONTEXTAs a resultf ventshat ccurreduringhe arly is-toryfmammals,utherian ammalsetainnly woofthefour oneopsingenefamiliesoundnmanyother ertebrates.eryikely uringhis ametimeframe,heelaborateystemf coloured il dropletscharacteristicfphotoreceptorsn many ertebrateswere lsoabandoned,swasa portionfthe pecificretinalircuitryedicatedoprocessingolournfor-mationJacobs& Rowe2004). These changeseftmost utherian ammals ith single imensionfcolourvision.Primates ubsequentlyscapedthisrestrictionyevolvingseries fvisual ystemltera-tions that providedopportunitiesor expandedcolourvision. hese changes,hat requitevariableacrossdifferentrimateineages,nclude greatlyenhancedpopulationof cones denselyorganizedaround centralizedovea, headdition f a thirdtypeof cone photopigment,nd theappearance fretinal ircuitryhatfacilitateshe comparisonfsignals rom ifferentoneclasses.Viewedncomparisonith thernimals,many fwhich eaturemuchmore laborate eripheraldap-tationsor xtractingolournformation,t sperhapsappropriatehatmammalsreroutinelyescribedshaving mpoverishedolourvision e.g. Goldsmith2006). Despite tsapparentimplicity,owever,hemaintenancef a colourvision apacityhroughoutthe onghistoryf eutherian ammalsrgues hat tmusthaveplayed useful ole n supporting am-malian uccess.Comparativeudgementsbouttherelativeimitationsfmammalianolourvision resometimesxtendedo nclude heprimates,ut t sa lot ess clear hat his tep s ustified.onsider,orexample,hat nder tringentest onditionsumantrichromatsan be shown o makereliable olourdiscriminationsasedonwavelengthifferencesfaslittle s 0.25nm (Mollonet al 1990),and that hetotalnumber f surface olours thattrichromatichumans andiscernmay eupwardsf pproximately2.3 millionPointer Attridge998).So far,t eemsnotto havebeendemonstratedhat ny therpeciescan matchthese rather mpressiveerformances.In anycase, perhaps hemajor trengthfprimatecolourvision omesnot justfrom hekeenness ftheir iscriminationbilities, hich reconsiderable,but ratherrom hefact hat rimatesave volvedlarge, gile ndplastic rain hat llows hem ousecolour nformationn a multitudefwaysgenerallyunavailableo those pecieswithmore imited entralprocessingapability.I thankMickey owe nd threenonymousefereesorhelpful omments. reparationf this reviewwassupportedya grant rom heNational yeInstitute(EY002052).REFERENCESAhnelt, . K. & Kolb,H. 2000 The mammalianhoto-receptormosaic-adaptiveesign. rog.Retinal yeRes.19,711-770. (doi:10.1016/S1350-9462(00)00012-4)Arajo r3 . C.5 Didonet, .J.3 rajo, . S.5Saletti, .G.,Borges, . R.J.& Pessoa,V. F. 2008 Colorvisionn the



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platypus: novelrouteto mammalianolour vision.Curr.Biol. 17, R161-R163. (doi:10.1016/j.cub.2007.01.037)Deegan I, J.F. & Jacobs, . H. 1996Spectralensitivityandphotopigmentsf a nocturnalrosimian,hebush-baby (Otolemurrassicaudatus)Am. J. Primatol.0,55-66. (doi:10.1002/(SICI)1098-2345(1996)40:l3.0.CO;2-#)Dominy, .J.& Lucas,P. W.2001Ecologicalmportanceftrichromaticolour ision oprimates.ature10,363-365. (doi:l0.1 38/35066567)Dominy, . J.,Lucas,P.W, Osrio,D. & Yamashita, .2001 The sensorycology fprimateoodperception.Evol.Anthopol.0,177-188.Dominy,N. J.,Garber, . A., Bicca-Marques, . C. &Azevedo-Lopes, . A. 2003 Do female amarins sevisual cues to detectfruit ewardsmoresuccessfullythan do males?Anim.Behav.66, 829-837. (doi:10.1006/anbe.2003.2288)Dulai,K. S.,vonDornum,M., Mollon, .D. & Hunt, . M.1999 The evolutionf richromaticolor ision yopsingeneduplicationnNew WorldndOld World rimates.Genomees. , 629-638.Fasick, .L, Cronin, .W, Hunt,D. M. & Robinson,. R.1998 The visualpigmentsf the bottlenose olphin(Tursiopsruncatus).is.Neurosci.5,643-651.Goldsmith,.H. 2006What irds ee. Sei.Am. 95,68-75.Hemmi,J. M. 1999 Dichromatic olourvision n anAustralianmarsupial,he tammarwallaby. . Comp.Physiol. 185,509-515. (doi:10.1007/s003590050411)Hemmi,J.M., James,A. & Taylor,W. R. 2002 Coloropponent etinal anglionells n thetammar allabyretina. . Vision, 608-617. (doi:l0.1167/2.9.3)Hiramatsu,, Melin,A. D., Aureli, ., Schaffner,. M.,Vorobyev, ., Matsumoto, . & Kawamura, . 2008Importancefachromaticontrastn short-rangeruitforagingfprimates.LOS One3,e3356. doi:10.1371/journal.pone.003356)Hisatomi, . & Tokunaga, . 2002 Molecularvolutionfproteins nvolved n vertebrate hototransduction.Comp. iochem.hysiol. 133,509-522. (doi:10.1016/S1096-4959(02)00127-6)Honkavaara,.,Aberg, . & Viitala, .2008 Do housemiceuse UV cues whenforaging?. Ethol.26, 339-345.(doi: 0.1 07/s 1 4-007-0068-6)Hunt, D. M., Wilkie,S. E., Bowmaker, . K. &Poopalasundaram,. 2001 Visionn theultraviolet.ell.Mol.Life ci.58,1583-1598. doi:10.1007/PL00000798)Jacobs, . H. 1993The distributionndnature f colourvision mong hemammals. iol.Rev.68, 413-471.Cdoi:10.1111/j.l469-185X.1993.tb00738.x)

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