AmJHumGenet.2003Jun72(6):15861590.doi:10.1086/375407

PMCID:PMC1180321

SouthAsia,theAndamanese,andtheGeneticEvidenceforanEarlyHumanDispersaloutofAfricaRichardCordauxandMarkStoneking

MaxPlanckInstituteforEvolutionaryAnthropologyLeipzigAddressforcorrespondenceandreprints:RichardCordaux,MaxPlanckInstituteforEvolutionaryAnthropology,DepartmentofEvolutionaryGenetics,DeutscherPlatz6,D04103Leipzig,Germany.Email:cordaux@eva.mpg.de

Copyright2003byTheAmericanSocietyofHumanGenetics.Allrightsreserved.

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TheoutofAfricamodelofanatomicallymodernhumanevolutionpositsanAfricanorigin100,000200,000yearsago,followedbysubsequentdispersal(s)toEurasiaandothercontinentswithinthelast100,000years(StringerandAndrews1988).Althoughalternativemodelshavebeenproposed,theoutofAfricascenarioreceivesthemostsupportbothfromarcheologicalandgeneticevidence(LahrandFoley1994).However,theroute(s)followedbytheAfricanmigrantsremainpoorlyunderstood.OneproposedroutewasthroughnorthernAfricatowardtheLevant,whichfindssupportinthearcheologicalandfossilrecords(LahrandFoley1994).ThisexitofmodernhumansoutofAfricawouldhavetakenplaceduringtheUpperPaleolithicera(45,000yearsago),whichconsiderablypostdatestheearliestevidenceofmodernhumanpresenceintheSahul.Indeed,luminescencedating,paleovegetationchanges,andskeletalremainssuggestthatAustraliawasinhabitedbymodernhumansby60,000yearsago(RobertsandJones1994Johnsonetal.1999Milleretal.1999Thorneetal.1999),implyingasubstantiallyearliermigrationfromAfricatoAustralia.Totakethisevidenceintoaccount,aswellasmorphologicalandarcheologicalfeaturesofmanyAustralianfossils,asecondmigrationofmodernhumans,knownasthesouthernroutehypothesis,wassuggestedtohaveoccurredduringMiddlePaleolithictimes(60,000100,000yearsago)fromeasternAfricatoSahulviaSouthAsia(CavalliSforzaetal.1994LahrandFoley1994).

IntheJanuary2003issueoftheJournal,Endicottetal.(2003)investigatedthegeneticaffinitiesof11Andamanislanders,agroupofpeopleintheIndianOceanwithphenotypicsimilaritiestosomeAfricanpopulations(i.e.,Negritofeatures)andreputedtobepossibledescendantsofearlymigrantsoutofAfricatoSahul,followingthesouthernroute.TheauthorsclaimthattheresultsoftheirinvestigationsupportthegrowingevidenceofanearlymovementofhumansthroughsouthernAsia.Inouropinion,EndicottandcolleaguesresultsdonotsupportanyrelationshipbetweenthepresentAndamanesepopulationandthehypothesizedearlysouthernmigration.TheauthorsidentifiedthreedifferentmtDNAhaplotypesin11Andamanislanders,twobelongingtohaplogroupM2andonebelongingtoM4.ThesehaplogroupshadpreviouslybeenreportedonlyintheIndiansubcontinent(Kivisildetal.1999bBamshadetal.2001).TheAndamanM4haplotypehasbeenfoundpreviouslyinmainlandIndia(Kivisildetal.1999b),whereasthetwoAndamanM2haplotypesare(sofar)uniquetotheAndamanese.Giventhat(1)thelattertwotypesoccupyabasalpositionintheM2network,whichhasanestimatedcoalescencetimeof63,0006,000years(Kivisildetal.1999b),and(2)theyarenotfoundinmainlandIndia,Endicottetal.(2003)concludetheyrepresentanearlysettlementoftheAndamanIslands.Thesetwopointsneeddiscussion.

Regardingpoint1,theageofahaplogroupcannotbeautomaticallyequatedtotheageofsubsetsofthishaplogroup.ThefoundingtypeofhaplogroupM2,characterizedby16223Tand16319ArelativetotheCambridgereferencesequence(CRS)(Andersonetal.1981)(fig.1),isdatedto63,000yearsbutisstillpresentinmainlandIndia.Thisdoesnotmeanthatanyclusterbranchingoffofthisnodeis63,000yearsold,butratherthatitis,at

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most,63,000yearsold.Inprinciple,theAndamanM2clustercouldbedatedtoanytimebetween63,000yearsandtoday.

Figure1Medianjoiningnetwork(afterEndicottetal.2003)ofmtDNAhaplogroupM2.SubstitutionpositionsrelativetotheCRSareshown.Thenumberofassignedindividualsfromsamplingtodateisindicatedintherelevantnodes.

Regardingpoint2,wedonotquestionthefactthattheAndamanM2haplotypeshavenotbeenfoundinmainlandIndia.However,relatedsequencesarefoundinmainlandIndia,oneofwhichiscitedbyEndicottetal.(2003)asacandidateancestralhaplotypeoftheAndamanM2sequences,sinceitdiffersbyonlyonesubstitutionat16274fromoneAndamanM2haplotype.Fromfigure2ofEndicottetal.(2003),weidentifyinmainlandIndiaanothercandidateancestralhaplotypefortheAndamanM2types,namely,thefoundertypeoftheentireM2haplogroup(characterizedby16223T,16319A).ThishaplotypediffersfromoneAndamanhaplotypebyasinglesubstitution(at16357)andhasalreadybeenreportedinmainlandIndia(Kivisildetal.1999b).Therefore,althoughidenticalhaplotypesarenotfoundelsewhere,theAndamanM2haplotypeshavecloselyrelatedcounterpartsinpresentdaymainlandIndia.

TheextentofisolationexperiencedbyAndamanislanders(and,thus,anapproximateuppertimelimitforthecolonizationofthearchipelago)canbeestimatedbydatingthetimeneededtoaccumulatetheobservedvariationoftheAndamanspecificmtDNAlineages.Inthisrespect,weanalyzed42unambiguouslydeterminedmtDNAsequencesfromOnge,Jarawa,andGreatAndamaneseindividuals(Thangarajetal.2003)andsixsequencesfromAkaBeaindividuals(Endicottetal.2003)belongingtohaplogroupM2(onthebasisofthemotif16223T/16319A).Altogether,the48AndamanM2sequencesdefinedfivehaplotypesunifiedby16357C(fig.1).First,weinvestigatedthepatternofdemographichistoryforthedatasetof48AndamanM2sequences,bycalculatingFusF (Fu1997)andTajimasD(Tajima1989)(Pvaluesarebasedon1,000simulatedsamples),aswellasHarpendingsr(Harpendingetal.1993),asimplementedinARLEQUIN2.0.BothFusF andTajimasDwerenotsignificantlydifferentfromzero(F =0.66,P=.35D=0.19,P=.50),suggestingnodemographicexpansionoftheAndamanesepopulation.Inaddition,Harpendingsrvaluewas0.146,consistentwithascenarioofconstantpopulationsize.

Assumingaconstantpopulationsize,theKimuratwoparametermodelofsubstitution(asimplementedinMEGA2.1)andamutationrateof1.6510 persiteperyear(correspondingto33%divergencepermillionyears[Wardetal.1991]),divergencetimesoftheAndamanM2haplotypesrelativetotwodifferentfounderswereestimated.WhenthemostancestralAndamanspecificM2type(bearingthemotif16223T,16319A,16357C)(fig.1)wasusedasafounder,theaveragetimeneededtoaccumulatetheobservedvariationinAndamanIslandswas25,300years.WhentheIndiancandidateasancestraltypeoftheAndamanM2sequences(bearingthemotif16223T,16319A)(fig.1)wasusedasafounder,theaveragetimebacktotheIndiancommonancestorwas42,300years.TheseresultsindicatethatAndamanislandersmayhaveremainedisolatedfrommainlandIndiafor25,00042,000years.However,thistimeisalmostcertainlyoverestimated.TheaveragesubstitutionrateofthefivesubstitutionsfoundintheAndamanM2cluster(16213,16234,16311,16344,16357)(fig.1)is2.5timesthatofthecontrolregionasawhole(Meyeretal.1999)thus,therealtimetoaccumulatetheobservedvariationmaybeupto2.5foldless,or10,10016,900years.Moreover,thetimeestimatesarebasedontheassumptionthatalltheAndamanM2typesarederivedfromasinglefoundinglineagemorerecenttimeswouldresultiftherewasmorethanonefoundinglineage.Insummary,thepresenceoftheuniqueM2lineagesintheAndamanIslands(aswellastheAndamanM4lineagethatisidenticaltopresentdayIndianM4lineages)suggestsacolonizationeventfromtheIndiansubcontinentoccurringduringtheUpperPaleolithic(orperhapsevenmorerecently),atmost40,000yearsago,whichisstillatleast20,000yearsaftertheearlysouthernroutemigrationtoSahul.

Thangarajetal.(2003)alsopresentedYchromosomeevidenceforAndamanislanders.TheysuggestedthathaplogroupD,anAsianspecificYAPlineagebearingthederivedstateatM174(Underhilletal.2000),isanoriginalpaternallineageofAndamanislanders.ToestimatetheageofM174,wecalculatedthattheaveragenumberofmutationsfromM174tocontemporaryhaplotypeswas4.89,onthebasisofthedatainUnderhilletal.(2000).Underhilletal.(2000)estimatedthattheaveragetimeforanewmutationwas5,6006,900years,which

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putstheageofM174at27,00034,000years.SincetheageofM174isanupperestimateforthetimewhenthisYhaplogroupreachedtheAndamanIslands,theYchromosomeevidencesuggestsanupperfigureof30,000yearsforthecolonizationofAndamanIslands,ingoodagreementwiththemtDNAevidence.Hence,bothYchromosomeandmtDNAdatasupportanUpperPaleolithicratherthanMiddlePaleolithicsettlementofthearchipelago.

OtherstudieshaveshownthatmtDNAhaplogroupsMandUarecommonintheIndiansubcontinent,andbothhavecoalescencetimesof50,00070,000years(QuintanaMurcietal.1999Kivisildetal.1999a,1999b,2003).Thishasbeentakenasageneticsignatureforanearly(i.e.,MiddlePaleolithic)colonizationofSouthAsiabymodernhumansand,consequently,asaconfirmationofthesouthernroutehypothesis.However,inSouthAsia,theearliestevidenceofmodernhumanindustriesandremainsisdatedto30,000years(KennedyandDeraniyagala1989Misra2001).BecauseearlierrecordsfromNeanderthalliketechnologiesarefoundinSouthAsia(Misra2001),theabsenceofmodernhumantracesdoesnotseemtobeduetoagapinthearcheologicalrecord.Howtoexplainagapofatleast20,000yearslongbetweenthearcheologicalandgeneticevidence?ThecoalescencetimeofhaplogroupUinEuropeisalsodatedto50,00060,000years(Richardsetal.2000),buttheacceptedtimescaleofthepeoplingofEuropebymodernhumansis35,00040,000yearsago(BocquetAppelandDemars2000).Ifso,whyshouldSouthAsia,butnotEurope,beconsideredtohavebeencolonized50,00070,000yearsago?Theobservedtimingdiscrepanciesbetweengeneticandarcheologicalestimatesaresimplyexplainedbythefactthatthedivergenceofgenespredatesthatofpopulations(Barbujanietal.1998).Consequently,theevidenceforaMiddlePaleolithiccolonizationoftheIndiansubcontinentprovidedbymtDNAstudiesandthegeneticconfirmationofthesouthernroutehypothesisareallthemoredebatable.

Whatconclusivegeneticevidenceremainsforthesouthernroutehypothesis?IftheIndiansubcontinenthadreceivedmigrantsfromthisputativemigrationfromAfricatotheSahul,itwouldbereasonabletoexpectatleastsomeremoteaffinitiesbetweenAfrican,Indian,Australian,and/orPapuaNewGuinean(PNG)genepools.Unfortunately,todate,moststudiesaimedatdetectingtracesofanancientpeoplingofSouthAsiathroughthesouthernroutehavenotcomparedtheIndiandatainawidercontext,inparticularwithpeople(exceptAfricans)fromregionsbelievedtohavebeeninvolvedinthesouthernroutemigration.AluinsertionsdataareinterpretedassupportinganancientAfricanPNGrelationship,butIndiaisnotapartofthisrelationship(Stonekingetal.1997).YchromosomeandmtDNAdatasuggestaconnectionbetweentheIndiansubcontinentandAustralia,whichis,however,datedto

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SouthAsiabefore30,000yearsago.HypothesizingaMiddlePaleolithicmigrationtoSouthAsiawouldcreatemoreproblemsthanitwouldsolve:itwould,inparticular,hardlyexplaintheabovecrucialpointsiiiandiv.

WeconcludethatthereiscurrentlynoconvincinggeneticevidencethatsupportsthepostulatedMiddlePaleolithicmigrationofmodernhumansfromAfricatotheSahulthroughSouthAsia.Thisdoesnotnecessarilymeanthatsuchamigrationneveroccurred,sincearchaeologicalevidencedoesdocumentmodernhumansinSahulby60,000yearsago.However,itispossiblethatsubsequentUpperPaleolithicmigrationsinEurasiaerasedthegenetictracesincontemporarypopulationsofthisearlyeventinourhistory(CavalliSforzaetal.1994Cordauxetal.2003)inanyevent,thesouthernroutehypothesisstillawaitsgeneticsupport.

Acknowledgments

WethankDavidHughes,ManfredKayser,VanoNasidze,andBrigittePakendorfforcriticalreadingofthemanuscript.

ElectronicDatabaseInformation

URLsfordatapresentedhereinareasfollows:

ARLEQUIN2.0,http://lgb.unige.ch/arlequin/

MEGA2.1,http://www.megasoftware.net/

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