Origin of Clothing Lice Indicates Early Clothing Use by Anatomically Modern Humans in Africa
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Title: Origin of Clothing Lice Indicates Early Clothing Use by Anatomically Modern Humans in Africa
Series Title: Molecular Biology and Evolution 28(1):29-32.
Physical Description: Journal Article
Creator: Reed, David
Toups, Melissa A.
Kitchen, Andrew
Light, Jessica E.
Publisher: Oxford Journals
Publication Date: 2011
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Abstract: Clothing use is an important modern behavior that contributed to the successful expansion of humans into higher latitudes and cold climates. Previous research suggests that clothing use originated anywhere between 40,000 and 3 Ma, though there is little direct archaeological, fossil, or genetic evidence to support more specific estimates. Since clothing lice evolved from head louse ancestors once humans adopted clothing, dating the emergence of clothing lice may provide more specific estimates of the origin of clothing use. Here, we use a Bayesian coalescent modeling approach to estimate that clothing lice diverged from head louse ancestors at least by 83,000 and possibly as early as 170,000 years ago. Our analysis suggests that the use of clothing likely originated with anatomically modern humans in Africa and reinforces a broad trend of modern human developments in Africa during the Middle to Late Pleistocene.
Acquisition: Collected for University of Florida's Institutional Repository by the UFIR Self-Submittal tool. Submitted by David Reed.
Publication Status: Published
Citation/Reference: Toups, M. A., A. Kitchen, J. E. Light, and D. L. Reed. 2011. Origin of clothing lice indicates early clothing use by anatomically modern humans in Africa. Molecular Biology and Evolution 28(1):29-32.
Funding: This work was supported by grants to D.L.R. from the University of Florida Research Opportunity SEED Fund and the National Science Foundation (DEB 0555024, DEB 0717165, and DEB 0845392). Publication of this article was funded in part by the University of Florida Open-Access Publishing Fund.
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OriginofClothingLiceIndicatesEarlyClothingUseby AnatomicallyModernHumansinAfricaMelissaA.Toups, ,1,2AndrewKitchen, ,3,4JessicaE.Light,5,6andDavidL.Reed*,61DepartmentofBiology,IndianaUniversity2DepartmentofBiology,UniversityofFlorida3DepartmentofBiology,ThePennsylvaniaStateUniversity4DepartmentofAnthropology,UniversityofFlorida5DepartmentofWildlifeandFisheriesSciences,A&MUniversity6FloridaMuseumofNaturalHistory,UniversityofFlorida Theseauthorscontributedequallytothismanuscript. Correspondingauthor :E-mail:dlreed@u.edu. Associateeditor :BarbaraHollandAbstractClothinguseisanimportantmodernbehaviorthatcontributedtothesuccessfulexpansionofhumansintohigher latitudesandcoldclimates.Previousresearchsuggeststhatclothinguseoriginatedanywherebetween40,000and3Ma, thoughthereislittledirectarchaeological,fossil,orgeneticevidencetosupportmorespecicestimates.Sinceclothinglice evolvedfromheadlouseancestorsoncehumansadoptedclothing,datingtheemergenceofclothinglicemayprovide morespecicestimatesoftheoriginofclothinguse.Here,weuseaBayesiancoalescentmodelingapproachtoestimate thatclothinglicedivergedfromheadlouseancestorsatleastby83,000andpossiblyasearlyas170,000yearsago.Our analysissuggeststhattheuseofclothinglikelyoriginatedwithanatomicallymodernhumansinAfricaandreinforces abroadtrendofmodernhumandevelopmentsinAfricaduringtheMiddletoLatePleistocene. Keywords: lice,humanevolution,isolationwithmigration. HomininsmigratedoutofAfricanumeroustimesoverthe lasttwoMy(reviewedin Stringer2002).Throughthe courseofthesemigrations,archaichomininpopulations occupiedpartsofEurope(e.g.,Atapuerca,Spain; Carbonell etal.2008)andCentralAsia(e.g.,theAltaiMountains,Siberia; Krauseetal.2010)thatwerecoolerandincreased theirvulnerabilitytocoldstress.Althoughevidencesuggeststhatarchaichomininsestablishedlong-lastingpopulationsintheseregions,anatomicallymodernhumans (AMHs)likelyoutcompetedarchaichomininsandwere abletothrivedespitethemoreseasonallyvariableclimates ( Gilligan2010).Asuiteofcomplexbehaviorsandtechnologiesassociatedwiththetransitionofarchaictomodern Homosapiens ,includingimprovedclothing,arecredited withfacilitatingthesuccessfulexpansionofAMHoutof Africaintohigherlatitudes.Critically,althoughclothing waslikelyanecessarytechnologyforAMH,itisunknown whetherclothinguseoriginatedearlyenoughtoplayan importantroleintheexpansionofarchaicpopulations outofAfrica. Determiningwhenclothingusebeganischallengingbecauseearlyclothing(i.e.,animalhides)woulddegraderapidly,erasinganydirectevidenceofclothingusefromthe LatePleistocenearcheologicalrecord.Therstevidence oftoolsusedtoscrapehidesappears ; 780Ka( Carbonell etal.1999),buttheseveryolddatesdonotnecessarilysignifyclothinguse.Animalhideshadotherusesbesides clothing(e.g.,providingshelter),althoughclothingis thoughttobeoneoftheearliestusesforskins.Eyedneedles rstappearinthearchaeologicalrecord ; 40Ka( Delson etal.2000),butthesesignaltheproductionofmorecomplexclothing(e.g.,tailoredmultilayeredgarmentassemblages),whichisundoubtedlyarelativelyrecentinnovation ( Gilligan2010).Importantly,thedevelopmentofclothing likelyoccurredafterhumanslosttheircoveringofbody hair.Geneticdatasuggestthatbodyhairwaslost ; 1.2 Ma( Rogersetal.2004),andanevenolderdate(3Ma) washypothesizedforthelossofbodyhairbasedonthe originofpubicliceinhumans( Reedetal.2007; Gilligan 2010).Thesestudiessuggestthatclothingusemayhave evolvedanywherefrom40Kato3Ma,andgiventhevastnessofthistime-span,alternativeapproachesforestimatingtheoriginofclothinguseareessential. Parasitesofferanidealsourceofalternativedatafordeterminingwhenclothinguserstbeganinhominins.Parasitescanprovidenovelinsightsintotheevolutionary historyoftheirhosts,especiallywhenthehostsexhibit lowlevelsofgeneticvariation( WhitemanandParker 2005).Theparasiticsuckingliceofprimates(Phthiraptera: Anoplura)havecospeciatedwiththeirhostsandtrack bothancient(e.g.,humanchimpsplit5Ma)andrecent (e.g.,expansionofAMHs ; 100Ka)eventsinhumanevolution( Reedetal.2004, 2007).Thehumanlouse( Pediculus humanus)isasinglespeciesthatoccursastwoecological TheAuthor(s)2010.PublishedbyOxfordUniversityPressonbehalfoftheSocietyforMolecularBiologyandEvolution. ThisisanOpenAccessarticledistributedunderthetermsoftheCreativeCommonsAttributionNon-CommercialLicense (http://creativecommons.org/licenses/by-nc/2.5),whichpermitsunrestrictednon-commercialuse,distribution,and reproductioninanymedium,providedtheoriginalworkisproperlycited.OpenAccess Mol.Biol.Evol. 28(1):292.2011doi:10.1093/molbev/msq234AdvanceAccesspublicationSeptember7,201029 Letter

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types(headandclothinglice)exhibitingmorphological,behavioral,andecologicaldifferences( Reedetal.2004; Light etal.2008).Thelossofhumanbodyhairrestricted P humanus tothehead,andthesubsequentdivergenceofthe twolousetypesisunlikelytohavebegunpriortotheavailabilityofthenewclothingniche( Burgess1995; Kittleretal. 2003).Thus,determiningwhenheadandclothinglicebegantodivergeprovidesadatebywhichclothingmusthave beeninregularusebyhumans. Inthisstudy,weanalyzedamultilocusdatasetofclothingandheadlouseDNAsequencesfromthreenucleargenes (18SribosomalRNA[rRNA],nuclearelongationfactor1a [EF-1 a ],andRNApolymeraseII[RPII])andthemitochondrialgenecytochrome c oxidasesubunitI(COI).Afterestimatingsubstitutionratesforeachlocusbasedonthe codivergenceofhumanandchimpanzeelicewiththeirprimatehosts( LightandReed2009 ),weemployedamultilocus Bayesianisolation-with-migration(IM)coalescentmethod ( NielsenandWakeley2001 ; HeyandNielsen2004 ; Hey 2005 )tojointlyestimatethedivergencetime( t ),effective sizes( NeHEAD, NeCLOTH, NeANCESTRAL),andeffectivemigration rates( mHEADtoCLOTH, mCLOTHtoHEAD)ofheadandclothing lousepopulationsfromourcombinedmultilocusdata set.Thismodelisidealforestimatingthedivergenceofhead andclothinglicebecauseitassumesanancestralpopulation (i.e.,headlice)divergedatsometime t intotwodaughter populations,whichthenexperienceindependentratesof exponentialgrowthwithmigrationbetweenpopulations. Ourresultsindicateasmalleffectivepopulationsizefor ancestral P humanus ( NeANCESTRAL,median 5 0.934 106; 95%highestprobabilitydensity[HPD] 5 0.011.161 106; table1 ),whichisconsistentwitheitherabottleneck createdbythelossofbodyhairorabottleneckimposed intheancestralhumanhostpopulation.Theestimatesof effectivepopulationsizeforbothheadandclothinglice werelarger( NeHEAD5 7.008 106;95%HPD 5 1.991 16.998 106and NeCLOTH5 4.038 106;95%HPD 5 0.461.676 106)andconsistentwithpostbottleneck expansions.Estimatesof s ( ; 0.24)indicatethatalargefractionoftheancestralheadlousepopulationinitiallybecame clothinglice,perhapsrapidlyexploitingnewnichespace. Parameterestimatesshowedelevatedratesofcontinuousmigrationinthedirectionofclothingtoheadlice ( mCLOTHtoHEAD5 1.615,95%HPD 5 0.495.785)but notablylessmigrationintheoppositedirection ( mHEADtoCLOTH5 0.235,95%HPD 5 0.005.755).These estimatescontradictpreviousstudiesthatfoundnomigrationbetweenheadandclothinglicebasedonmicrosatellite data( Leoetal.2005).Inaddition,thedirectionofgeneow isunexpectedgiventhatheadlicecanreadilycolonizethe clothingniche( AlpatovandNastjukova1955; Leveneand Dobzhansky1959; Lietal.2010). Theposteriorprobabilitydistributionfortheheadand clothinglousedivergencetimeischaracterizedbyamode (i.e.,thesingleestimatewiththehighestposteriorprobability)of83Kaandamedianvalueof170Ka(95%HPD 5 29Ka; g.1 ).Thesedatesarelargelyconsistentwith thoseestimatedby Kittleretal.(2003 2004),whoanalyzed asinglemitochondrialgeneusingadistance-based method.However,theBayesianmultilocusIMmethodaccountsforuncertaintyinthemodelparametersaswellas stochasticvariationbetweenloci,whichprovidesamore robustandaccurateparameterestimate( Edwardsand Beerli2000). DuringthelatterpartoftheMiddlePleistocene(e.g.,83 170Ka),archaichomininslivedincoldclimatesinEurasia, whereas H sapiens wasstillinAfrica.Whetherthesearchaic homininshadclothingisunknownbecausetheyleftno clothinglousedescendentsthatwecansampleamonglivinghumans.Allmodernclothingliceareconnedtoasinglemitochondrialcladethatshowsacontemporaneous populationexpansionwithmodernhumans ; 100Ka ( Reedetal.2004, 2007).Therefore,wearelefttoconclude thatregularclothingusemusthaveoccurredin H sapiens atleastby83Kaandpossiblyasearlyas170Ka.Whether archaichomininsusedclothingcannotbeassessedfrom theseliceandmayrequirethecollectionoflicefromarchaichumanremains,whichisunlikely. EventhougharchaichomininsdispersedintocoldclimateshundredsofthousandsofyearsbeforeAMH,modernhumansareoftencreditedwithoutcompeting contemporaryarchaicspeciesduetoincreasedtness stemmingfromasuiteofmodernbehaviorsandtechnologiesthatincludetheuseofclothing( Gilligan2010).Interestingly,weestimatedthatclothingmayhavebeeninuse asearlyas170Ka,whichcorrespondstotherapidonsetof Table1. Mean,Median,Mode,and95%HPDforParametersEstimatedinIM.95%HPD Mean Median Mode NeHEAD a1.991.998 3 1068.033 3 1067.008 3 1064.893 3 106NeCLOTH b0.461.676 3 1064.742 3 1064.038 3 1063.274 3 106NeANCESTRAL c0.011.161 3 1061.317 3 1060.934 3 1060.011 3 106tDivergence d29Ka 229Ka 170Ka 83Ka mHEADtoCLOTH e0.005.755 0.492 0.235 0.005 mCLOTHtoHEAD f0.495.785 1.836 1.615 1.335 sg0.001.879 0.325 0.242 0.001aEffectivepopulationsizeofmodernheadlice( NeHEAD).bEffectivepopulationsizeofmodernclothinglice( NeCLOTH).cEffectivepopulationsizeofancestralheadlicepopulation( NeANCESTRAL).dTimeofclothingandheadlicedivergence( tDivergence).eMigrationfromheadtoclothinglicepopulations( mHEADtoCLOTH).fMigrationfromclothingtoheadlicepopulations( mCLOTHtoHEAD).gProportionoftheancestralheadlicepopulationthatcontributestothemodernheadlicepopulation( s ). Toupsetal. doi:10.1093/molbev/msq234MBE30

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aniceage,MarineIsotopeStage6( ; 190Ka; EPICA CommunityMembers2004),thatwouldhavecausedcold stressforpopulationslivingoutsidethetropicsandcould haveledtotheinitialuseofclothingbymodernhumans. Ourestimatefortheoriginofclothingusesuggeststhat oneofthetechnologiesnecessaryforsuccessfuldispersal intocolderclimateswasalreadyavailabletoAMHprior totheiremergenceoutofAfrica.MethodsAllavailableDNAsequencesforCOI(108headand58 clothinglice),18SrRNA(10headand12clothinglice), EF-1 a (25headand9clothinglice),andRPII(25head and10clothinglice)for P humanus andtheoutgroup P schaef (chimpanzeelouse)weredownloadedfromGenBank(availableas supplementarytableS1 Supplementary Material online).Allsequenceswerealignedbyhandusing Se-Alv2.01a11( http://tree.bio.ed.ac.uk/software/seal/ ), withthe18SrDNAalignedtosecondarystructure ( Gillespie2004; Gillespieetal.2005). Substitutionrates( table2 )forthefourgeneswereestimatedinBEASTv.1.5.3( DrummondandRambaut2007). Rateswerecalibratedbyplacinganexponentialpriordistribution(lowerbound 5 5Ma,mean 5 5.5Ma)onthe divergenceof P humanus (human)and P schaef (chimpanzee)licethatreectsconservativelyrecentestimates forthedivergenceoftheirhosts( KumarandHedges 1998).Eachgenewasanalyzedusingarangeofsubstitution andclockmodels,aswellastreepriors,withposteriorestimatesmadefromthemodelthatbesttthedataasdeterminedbymarginallikelihoodsestimatedintheprogram 200 KYA 400 KYA 600 KYA 1000 KYA 800 KYA 1200 KYA 0.002 0.004 0.0060PresentYears before presentPosterior Probability Estimated time for loss of body hair ~1.2 MYA First evidence for hide scrapers ~780 KYA Median head-clothing louse divergence ~170 KYA First evidence for tailored clothing ~40 KYA FIG.1. Divergencetimeofhumanheadandclothinglice.Theposteriordistributionforthedivergenceofheadandclothinglice(graycurve) placesthemedianestimatefortheoriginofclothingliceat170Ka(blackarrow).Thisestimateissubstantiallyolderthanapreviousestimate of30Kafrommoleculardata( Kittleretal.2003 )andisconsistentwiththerelativeantiquityoftherstarchaeologicalevidenceforhide scrapers ; 780Ka(Carbonelletal.1999 ),thelossofhumanbodyhairby ; 1.2Ma( Rogersetal.2004 ),andtherstevidencefortailored clothing ; 40Ka(Delsonetal.2000 ),whichareindicatedbybluearrows.Furthermore,themedianestimatelieswithintheiceagecoincident withMarineIsotopeStage6 ; 130Ka( EPICACommunityMembers2004 ),indicatedbythered-shadedregion. Table2. ModelsofSubstitution,LikelihoodScores,andMeanSubstitutionRatesPerGeneCalculatedinBEAST.Gene Substitution Model Clock Model Tree Prior Marginal Likelihood Mean SubstitutionRate(95%HPD) COIGTR 1 CPaUCEDbBSPc2 1318.7286.28 3 102 8(3.36.64 3 102 8) 18srDNAHKY 1 Gd1 IeUCEDBSP 2 3087.5197.19 3 102 9(3.64.01 3 102 9) EF-1a GTR 1 CP 1 GUCEDBSP 2 853.4017.89 3 102 9(3.90.622 3 102 9) RPIIGTR 1 CP 1 GUCEDConstantf2 1144.3251.26 3 102 8(0.46.34 3 102 8)aBetweensiteratevariationpartitionedbycodonposition(CP).bUncorrelatedexponentiallydistributedrelaxedclock(UCED, Drummondetal.2006 ).cBayesianskylineplottreeprior(BSP, Drummondetal.2005 ).dGammadistributionofbetweensiteratevariation(G).eInvariateproportionofsites(I).fConstantpopulationsizetreeprior. OriginofClothingUseinHumans doi:10.1093/molbev/msq234MBE31

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Tracerv1.5( http://tree.bio.ed.ac.uk/software/tracer ).Markovchainswererunforatleast100milliongenerations, sampledevery10,000generations,andtherst10%ofsampleswerediscardedasburn-in.Allrunswereduplicatedto ensureconvergence. MultilocusBayesianIMcoalescentanalysiswasperformedonthe P humanus sequencesusingtheprogram IM( Hey2005).AllanalysesusedtheHKYsubstitution model,whereaspriorsonmodelparameterswerebroad uniformdistributionsconservativelyestimatedfrompreliminaryruns.Markovchainswererunfor 200million generationsandreplicated8timestoensureconvergence. Alousegenerationtimeof21days(18generationsper year)andthesubstitutionratesin table2 wereusedtoconvertparameterestimatesfrommutationaltodemographic units.SupplementaryMaterialSupplementarytableS1 isavailableat MolecularBiology andEvolution online( http://www.mbe.oxfordjournals. org/ ).AcknowledgmentsWethanktwoanonymousreviewersforvaluablecomments.WeacknowledgetheUniversityofFlorida High-PerformanceComputingCenterforprovidingcomputationalsupport.Thisworkwassupportedbygrants toD.L.R.fromtheUniversityofFloridaResearchOpportunitySEEDFundandtheNationalScienceFoundation(DEB 0555024,DEB0717165,andDEB0845392).ReferencesAlpatovWW,NastjukovaOK.1955.Transformationofthehead formofPediculushumanusL.intothebodyformunderthe inuenceofchangedlivingconditions. BullSocNatMoscow. 60:79. BurgessIF.1995.Humanliceandtheirmanagement. Advancesin Parasitology 36:271. CarbonellE,deCastroJMB,ParesJM,etal.(30co-authors).2008. ThersthomininofEurope. Nature 452:U465U467. 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