CurrentBiology,Vol.13,979 - PDF document

CurrentBiology,Vol.13,979–984,May27,2003,2003ElsevierScienceLtd.Allrightsreserved.DOI10.1016/S0960-9822(03)00373-7AYChromosomeCensusoftheBritishIsles[6].Morerecently,Wealeetal.[7]arguedforsubstan-CristianCapelli,NicolaRedhead,JuliaK.Abernethy,FionaGratrix,tialAnglo-SaxonmalemigrationintocentralEnglandbasedontheanalysisofeightBritishsamplesetscol-JamesF.Wilson,TorolfMoen, CurrentBiologyFigure1.BritishIslesSamplingLocationsMapThelocationofthesampledsmall,urbanar-easandthe35gridofcollectionpointsareshown.Foreachgridpoint,weselectedtheclosesttownwithina20-mileradius.Onlytownswith5–20,000inhabitantswerecho-sen.Individualswere,withtheexceptionofonelocation,thenselectediftheirpaternalgrandfather’sbirthplacewaswithina20-mileradiusoftheselectedcenter.Midhurstsam-pleswerecollectedupto40milesfromtherespectivegridpoint.Whenthegridpointwasatsea,thenearestpointonthecoastwasused(MorpethandStonehaven).Wealsoaddedadditionalpointstocoverimportantgeographicregionsnotcoveredbythegrid(Shetland,York,Norfolk,Haverfordwest,Llangefni,Chippenham,Cornwall,ChannelIslands)andincludedtwoIrishsamples,Cas-tlereaandRush(NorthofDublin).ThetotalnumberofpointssampledintheBritishIsleswas25. 0.05).SamplingintheBritishIsleswasmainlyundertakenbepolymorphicinEurope[13,14].ThemostfrequenthaplogroupsobservedwerethosedefinedbyM173,toconformtoasystematic35grid(Figure1).WegenotypedsixY-linkedmicrosatellites(identifyingM170,andM17mutations(Table1)(HgsR1xR1a1,IxI1b2,andR1a1,referredtoashgs1,2,and3in[4]).haplotypes)[12]and11uniqueeventpolymorphisms(UEPs,identifyinghgs,asdefinedinFigure2)knowntoFormostanalyses,wesubdividedchromosomeswithinFigure2.YChromosomeGenealogyYchromosomegenealogyoftheUEPstypedisshown.NomenclatureisassuggestedbytheYchromosomeconsortium[18].Forsim-plicity,onlythelastderivedmutationisindi-catedinthetext. YChromosomesintheBritishIsles Table1.YChromosomeHaplogroupFrequenciesintheDifferentPopulations SampleE3bFxIJKJxJ2J2IxI1b22.471I1b2KxPN3N3PxR1R1xR1a1AMH1R1a13.65 Shetland0.050.050.170.490.060.1763Orkney0.070.070.010.020.230.410.070.12121Durness0.020.120.470.330.020.0451WesternIsles0.180.070.170.490.030.0688Stonehaven0.020.020.110.340.450.0544Pitlochry0.070.100.240.560.0241Oban0.020.050.020.260.600.020.0242Morpeth0.020.010.030.120.060.210.520.020.0195Penrith0.030.010.020.080.100.160.520.020.0690IsleofMan0.020.080.080.150.550.080.0562York0.040.020.150.170.200.370.020.0246Southwell0.060.060.140.040.200.440.040.0170Uttoxeter0.040.010.040.080.100.260.450.0284Llanidloes0.050.040.020.070.120.190.470.0457Llangefni0.040.010.040.010.210.680.0180Rush0.080.030.450.410.010.0376Castlerea0.070.020.370.5343Norfolk0.030.020.170.140.230.370.020.02121Haverfordwest0.030.020.020.270.640.0259Chippenham0.020.040.060.140.020.160.490.060.0251Faversham0.040.050.040.070.270.490.020.0255Midhurst0.010.010.010.040.090.060.030.200.540.0180Dorchester0.040.010.010.030.070.070.260.470.0473Cornwall0.020.040.080.250.540.060.0252ChannelIslands0.040.020.010.010.100.110.030.270.390.020.01128Basques0.020.020.020.050.290.6042Germany/Denmark0.030.020.030.190.200.020.130.260.080.04190Norwayaa0.130.150.010.040.080.220.120.22201 R1xR1a1,IxI1b2,andR1a1havebeenindicatedbysubtractingAMH1,2.471,and3.651,respectively.a,frequencyof0.005. thesegroupsbyusingone-stepneighborclustersoftion.Inadditiontotheserelativelyclearpatterns,thePCplotsalsoprovideasuggestionofmoresubtlediffer-thehaplotypesAMH,2.47,and3.65[4],indicatedas1,2.471,and3.651,respectively.ences.Forexample,thereisagroupofpopulationsthatappearsshiftedtotheleftfromthemainangleofInPrincipalComponent(PC)plotssummarizingvaria-tioninYchromosomefrequencies(Figure3),alltheGerman/Danishinfluence,andthisisconsistentwithsomedegreeofNorwegianinput.ItisnotsurprisingthatBritishpopulations(excludingOrkneyandShetland)skewedtowardtherightofaxisone;thisreflectsthetheWesternIslesandIsleofManareinthisgroup,buttheinclusionofPenrithisofparticularinterestgiventherelativelyhighfrequenciesofAMH1inthesepopula-tions.TheBasques,themostextremeonthisaxis,clus-Scandinavianinfluenceondialectinthisregion[15].Similarly,RushappearstobeshiftedslightlytowardtheteredwithsamplesfromcentralIreland(Castlerea)andWales(HaverfordwestandLlangefni).ItisinterestingNorwegianpoleonPC1,butthereisnoshifttowardtheGerman/Danishposition.Inaddition,themainlandScotstonotethatScottishmainlandsitesappeargenerallybetweenEnglishonesandthese“indigenous”popula-aresomewhatclosertotheindigenoustypethananyEnglishsets,exceptCornwall.Thesiteswiththehighesttions.TheNorwegianandtheGerman/Danishsamplesareseparatedonaxistwo.degreeofGerman/DanishinputareYorkandNorfolk,followedbySouthwellandLlanidloes.AlloftheseexceptToaidinterpretationofthisplot,wesimulatedad-mixedpopulationsbydrawingvaryingproportionsofLlanidloesarehistoricallyinregionswheretheDanesareknowntohavehadasignificantpresence.Thepeculiarindividualsatrandomfromeachofthesourcepopula-tionsandplottingthemonPCplotsthatalsoincludedpositionofLlanidloesmightreflectrecentmigrationinthepasttwocenturies[1].Theremainingsamplesarethesourcepopulationsthemselves(Figure4).Thesimu-latedpopulationsshowthatthepositionofapopulationclosertotheindigenousgroup;forthesepopulations,thisfindingsuggestsalowerdemographicimpactbyonthefirsttwoaxesprovidesasensitiveindicatorofthedegreeofcontinentalinputintoanindigenousback-NorthEuropeanpopulations.ThiscanalsobeseeninthefrequencyofAMH1,whichisalwaysabove33%ground,withNorwegianinputmovingpopulationsstrictlyalongaxis1andGerman/DanishinputmovinginBritishpopulationsbutremainsbelow26%inthecontinentalsourcepopulations;thesedataareconsis-populationsatananglethroughbothaxes.InspectionofFigure3,inlightofthesesimulations,showsthattentwiththepresenceofsomeindigenouscomponentinallBritishregions.OrkneyandShetlandhavesignificantNorwegianinputandlittletonoGerman/Danishinput,thattheEnglishAdmixtureproportionswerealsoevaluatedbyusingalikelihoodapproachimplementedbytheprogramLeaandScottishsitesallhaveGerman/Danishinfluence,andthattheWesternIslesandIsleofManhaveGerman/[16].ThisquantitativeanalysiswasconsistentwiththevisualpatternshownbyPCinvestigation,anditalsoDanishinfluence,presumablyduetoEnglishimmigra- CurrentBiology Figure3.PrincipalComponentsPlotAplotofthefirstandsecondprincipalcomponentsoftheYchromosomehaplogroupfrequenciesofthepopulationsshowninTable1.ThefirsttwocomponentsofthePrincipalComponentsanalysisofYchromosomefrequenciesexplainalmost60%ofthetotalvariation.TheloadingswiththegreatestmagnitudeforthefirstaxisareforAMH1and3.650.152and–0.241),while2.471and3.651havethegreatestimpactonthesecondaxis(providessignificantevidencethattherehasnotbeensionisthelimitedcontinentalinputinsouthernEngland,whichappearstobepredominantlyindigenousand,bycompletepopulationreplacementanywhereintheBrit-ishIsles(seeTableS1intheSupplementalDataavail-someanalyses,nomoreinfluencedbythecontinentalinvadersthanismainlandScotland(Figure3andTableablewiththisarticleonline).TheapportionmentofgeneticvariationwasinferredS1).ItisinterestingtonotethattheareasinsouthernEnglandwere,historically,mostlyoccupiedbytheAn-withAMOVA,asimplementedbytheArlequinpackage[11].Comparisonofthedifferentsmalltownssampledglo-Saxons,whiletheactivitiesoftheDanishVikingsweremainlyineasternEngland[1].Theresultsseemindicatesthatthevastmajorityofthediversitypresentwaswithinpopulations(96.35%),withonly3.65%acrosstosuggestthatinEnglandtheDaneshadagreaterdemographicimpactthantheAnglo-Saxons.Analterna-populations.ThesubdivisionofthesamplesintoCeltic(Ireland,Wales,andmainlandScotland)versustheresttiveexplanationwouldbethattheinvadersinthetwoareasweregeneticallydifferentandthatwecannotseeofthepopulationsshowedadistributionacrossthetwogroupsof3.65%ofthetotalvariation;theexclusionofthisdifferencereflectedinthecurrentinhabitantsoftheContinentalareascorrespondingtoAnglo-SaxonandLlanidloesandDurness,whichclearlyshowevidenceofcontinentalinput,increasedthisvalueto6.16%(Figure3Danishhomelands.Thiswouldseemtobeadifficultdistinctiontomake,anditshouldbeemphasizedthatandTableS1).Consideringtheindigenous/nonindige-nousclusteringsystem(Castlerea,Haverfordwest,andouranalysesassumethatwehavecorrectlyidentifiedthesourcepopulations.If,forexample,therealconti-Llangefniversustherest),avalueof7.48%wascalcu-lated,oneofthehighestvaluesobtained,amongmulti-nentalinvadershadacompositionmoresimilartotheindigenousBritishthanourcandidatesampleset,ourplealternativeclusteringsystems(notshown).Thus,theindigenous/nonindigenousdistinctionappearstobetheresultswouldsystematicallyunderestimatetheconti-nentalinput.Similarly,anyContinentalinputintoourmostimportantfactorinfluencinggeographicpatternsofYchromosomevariationintheBritishIsles.Castlereasamplewouldbiasourinferences,buttheverysimilarcompositionoftheBasqueandCastlereaInsummary,ourresultsshowthatNorwegianinvadersheavilyinfluencedthenorthernareaoftheBritishIsles,samplessuggeststhatthishasbeenminimal.Withre-gardtosourcepopulations,wenotethatWealeetal.butthisgrouphadlimitedimpactthroughmostofmain-landScotland(excepttheextremenorth).Instead,main-[7]recentlyusedFrieslandasanAnglo-Saxonrepresen-tativesourcepopulationandsuggestedasubstantiallandScotlandwasmoreinfluencedbytheGerman/Dan-ishinput.Despitetheirwell-knownactivitiesintheIrishreplacementofpre-Anglo-SaxonpaternallineagesincentralEngland.WethereforecomparedFrisianstoourSea,Norwegianinputinadjoiningareasismodest.SomeisindicatedintheIsleofMan,andasmalleramountisNorthGerman/Danishsampleandfoundthatthetwosetsarenotsignificantlydifferentfromeachother(pindicatedinIreland.Perhapsthemostsurprisingconclu- YChromosomesintheBritishIsles Figure4.PrincipleComponentsPlotofSimulatedPopulationsAPrincipleComponentsplotofsimulatedpopulationsofn50comprising,atadmixturesof,respectively,20%,40%,and60%,theindigenousBritishandtheGerman/DanishandNorwegiansets.Thecirclesgroupsimulatedpopulationswiththesamecontinentalproportions.ThearrowsindicatethedirectionsalongwhichthesimulatedpopulationtendstomoveaccordingtotherelativeproportionofContinentalinput.0.3,datanotshown).WhenincludedinthePCanalysis,gradual,whichwasnotvisibleinthesamplesanalyzedintheWealeetal.studytheFrisiansweremore“Continental”thananyoftheBritishsamples,althoughtheyweresomewhatcloserMoststudiesinhumanevolutionandgenetichistoryhaveusedsamplesfromveryfewlocations,oftenneartotheBritishonesthantheNorthGerman/Denmarksample.Forexample,thepartofmainlandBritainthatmajormetropolitanareas.Here,weshowthatdetailedsamplesfrommultiplesmall,urbanareaswithageo-hasthemostContinentalinputisCentralEngland,butevenheretheAMH1frequency,notbelow44%(South-graphicallystructuredsamplingdesignrevealpatternsthatcouldnotbedetectedwithtypicalsamplingwell),ishigherthanthe35%observedintheFrisians.Theseresultsdemonstratethatevenwiththechoiceofschemes.Forexample,analysesofmultiplesetshaveconfirmedhighercontinentalinputincentralEnglandFrisiansasasourcefortheAnglo-Saxons,thereisaclearindicationofacontinuingindigenouscomponentandthenorthernmostsamples(Durness,onthenorthcoastofScotlandandtheScottishIsles)andalowerintheEnglishpaternalgeneticmakeup.WealsonotethatouranalysisincludesrepresentativesoftheDanishlevelofcontinentalintrogressioninsouthernEnglandandLowlandScotland.Inaddition,multiplesamplesetsVikings,whichwerenotavailableintheWealeetal.study.ConsiderationofDanishVikinginputisimportantrevealedheterogeneityinWales.Iberian,French,andCentral-NorthernItalianpopula-becausetheiractivitiesontheBritisheasterncoastarewelldocumented[1].OurevaluationoftheDanishandtionshavebeenshowntohavesimilarYchromosomecompositions,presumablyreflectingtheircommonheri-Anglo-Saxonsourcepopulations,however,showsthatthecontributionsofthesegroupsareunlikelytobedis-tageintheEuropeanPalaeolithic[14];Wilsonetal.[4]notedthatAMH1haplotypesathighfrequencyaretinguishablebyusingtheresolutionavailableinouranal-yses.WhateverlevelofreplacementtookplaceinEn-associatedwiththeEuropeanPalaeolithic.Here,wenotethatanotherhaplogroup(I1b2)isfoundalmostex-gland,itcouldhavebeendueto“Anglo-Saxons,”Danes,oracombinationofbothgroups.clusivelyinBritishpopulationsthathaveexperiencedlittleornocontinentalgeneticinput(Tables1andS1).Intriguingly,earlierstudieshaveshownthatitispresentintheIberianPeninsulaatlowfrequencies(0%–5.4%)ThedetailedsamplingschemeusedhereidentifiedotherandinSardiniaatasignificantpercentage(35.1%)[9,previouslyunknownregionalpatternsinthedegreeof14].ThisgroupmightbeanotherconstituentoftheEuro-continentalinput.Forexample,theCentral-EasternpartpeanPalaeolithic.ofEnglandexperiencedthemostcontinentalintrogres-Finally,wenotethatforensicanalysesbasedonthesion.Inaddition,ourinclusionofsamplesfromWalesYchromosomegenerallyassumehomogeneityofYadditionaltothoseofWealeetal.[7]indicatesthatthetransitionbetweenEnglandandWalesissomewhatchromosomehaplotypesthroughoutmostofEurope CurrentBiology6.Berry,R.J.,andFirth,H.N.(1986).ThePeopleofOrkney(Kirk-[17].Ourfine-scaleinvestigationofYchromosomevari-wall:OrkneyPress).ationdemonstratesappreciablefrequencydifferences7.Weale,M.E.,Weiss,D.A.,Jager,R.F.,Bradman,N.,andThomas,ofYchromosomehaplotypesoverrelativelyshortgeo-M.(2002).YchromosomeevidenceforAnglo-Saxonmassmi-graphicdistances.Haplotype121311162511(hggration.Mol.Biol.Evol.,1008–1021.R1a1)(numberofrepeats,lociasfollows:DYS388,393,8.Bosch,E.,Calafell,F.,Santos,F.R.,Perez-Lazaun,A.,Comas,D.,Benchemsi,N.,Tyler-Smith,C.,andBertranpetit,J.(1999).392,19,390,391)ispresentatfrequenciesaround5%Variationinshorttandemrepeatsisdeeplystructuredbyge-inShetlandandOrkney,whileitisalmostcompletelyneticbackgroundonthehumanYchromosome.Am.J.Hum.absentfromtheothercollections.Similarly,haplotype,1623–1638.141311142210(hgIxI1b2)wasrecordedat6%–7%9.Bosch,E.,Calafell,F.,Comas,D.,Oefner,P.J.,Underhill,P.U.,intheCentral-EastEnglishsamples,butitwasabsentandBertranpetit,J.(2001).High-resolutionanalysisofhumanY-fromIrish,Welsh,andScottishpopulations.chromosomevariationshowsasharpdiscontinuityandlimitedgeneflowbetweennorthwesternAfricaandtheIberianPenin-ExperimentalProceduressula.Am.J.Hum.Genet.,1019–1029.10.Forster,P.(1995).EinwanderungsgeschichteNorddeutsch-MicrosatelliteandUEPAnalysislands(ImmigrationhistoryofNorthGermany).InNorth-WesternYchromosomemicrosatellitesDYS388,393,392,19,390,and391EuropeanLanguageEvolution,V.F.Faltings,A.G.H.Walker,andanalysiswasperformedbyfollowingtheprotocolsdescribed[12].O.Wilts,eds.(Odense,Denmark:UniversityofOdense),pp.UEPanalysiswasbasedonaPCR-RFLPapproach.ProtocolswillbepublishedelsewhereandareavailablefromC.C.uponrequest.11.Schneider,S.,Kueffer,J.-M.,Roessli,D.,andExcoffier,L.Briefly,theDNAregioncontainingthechosenpolymorphicnucleo-(1997).ARLEQUIN,APopulationGeneticDataAnalysisPro-tideswasPCRamplifiedandthenscreenedbyusingappropriategramme.(Geneva:GeneticsandBiometeryLaboratory,Univer-restrictionendonucleases.DigestedPCRproductswereloadedonsityofGeneva).a377ABIautomatedsequencerupdatedto96lanes,andalleles12.Thomas,M.G.,Bradman,N.,andFlinn,H.M.(1999).Highwerecalledaccordingtofragmentsize.throughputanalysisof10microsatelliteand11diallelicpoly-morphismsonthehumanY-chromosome.Hum.Genet.DataAnalysisPrincipalComponentsanalysiswasperformedbyusingthe13.Rosser,Z.H.,Zerjal,T.,Hurles,M.E.,Adojaan,M.,Alavantic,D.,POPSTRsoftware(H.Harpending,personalcommunication).TheAmorim,A.,Amos,W.,Armenteros,M.,Arroyo,E.,Barbujani,apportionmentofgeneticvariationandFisher’sExactTestanalogG.,etal.(2000).Y-chromosomaldiversityinEuropeisclinalandwereinferredbyusingtheArlequinpackage[11].influencedprimarilybygeography,ratherthanbylanguage.Am.J.Hum.Genet.,1526–1543.14.Semino,O.,Passarino,G.,Oefner,P.J.,Lin,A.A.,Arbuzova,S.,SupplementalDataBeckman,L.E.,DeBenedictis,G.,Francalacci,P.,Kouvatsi,A.,SupplementalDataincludingTableS1areavailableathttp://images.Limborska,S.,etal.(2000).ThegeneticlegacyofPaleolithicHomosapienssapiensinextantEuropeans:aYchromosomeperspective.Science,1155–1159.15.Reaney,P.H.(1927).AGrammaroftheDialectofPenrith(Cum-berland):DescriptiveandHistorical,withSpecimensandGlos-WethankalltheindividualswhocontributedDNAsamples.Wealsosary(Manchester,UK:TheUniversityPress).thanktheBritishBroadcastingCorporation;TheUKNationalBlood16.Chikhi,L.,Bruford,M.W.,andBeaumont,M.A.(2001).Estima-Service,inparticularElizabethCaffrey,AngelaGorman,GabraGa-tionofadmixtureproportions:alikelihood-basedapproachus-mal,CatherineChapman,JamesVirge,AndewHerborn,JuliaTaylor,ingMarkovchainMonteCarlo.Genetics,1347–1362.TomCrusz,JohnWitcher,SergeSix,andallthecollectionunitsthat17.Roewer,L.,Krawczak,M.,Willuweit,S.,Nagy,M.,Alves,C.,kindlysupportedthiswork;theWelshBloodService,especiallyAmorim,A.,Anslinger,K.,Augustin,C.,Betz,A.,Bosch,E.,etal.AngusMacmillanDouglas,BarbaraHancock,ElizabethMeech,and(2001).OnlinereferencedatabaseofEuropeanY-chromosomalSianGorst;theGermanBloodservicecollection(DeutschesRoteshorttandemrepeat(STR)haplotypes.ForensicSci.Int.Kreuz,BlutspendedienstNord),theHistoryDepartmentattheUni-versityofCopenhagen,andSanneJacobsenandThomasOldrup;18.YChromosomeConsortium(2002).AnomenclaturesystemforSoniaBortoletto;F.FalleandW.GallienneforhelpingwithDNAthetreeofhumanY-chromosomalbinaryhaplogroups.GenomecollectionintheChannelIslands.Finally,wethankPeterForsterfor,339–348.suggestionsandcomments,ChrisTyler-Smithforinformationpriortopublication,andElenaBoschforprovidingthecompleteBasquemicrosatelliteandUEPsdataset.D.G.isaRoyalSociety/WolfsonResearchMeritAwardholder.Received:October29,2002Revised:March7,2003Accepted:April16,2003Published:May27,20031.Davies,N.(1999).TheIsles:AHistory(London:Macmillan).2.Graham-Campbell,J.,andBatey,C.(1998).VikingsinScotland(Edinburgh:EdinburghUniversityPress).3.Richards,J.D.(2000).VikingAgeEngland(Stroud:Tempus).4.Wilson,J.F.,Weiss,D.A.,Richards,M.,Thomas,M.,Bradman,N.,andGoldstein,D.B.(2001).GeneticevidencefordifferentmaleandfemalerolesduringculturaltransitionsintheBritishIsles.Proc.Natl.Ac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