Ancient DNA Suggests The Leading Role Played by Men in The Neolithic Dissemination

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Ancient DNA suggests the leading role played by men in the Neolithic dissemination
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TheimpactoftheNeolithicdispersalonthewesternEuropeanpopulationsissubjecttocontinuingdebate. Article Alerts
Totraceanddategeneticlineagespotentiallybroughtduringthistransitionandsounderstandtheoriginof Export Citation
the gene pool of current populations, we studied DNA extracted from human remains excavated in a Save for Later
Spanish funeral cave dating from the beginning of the fifth millennium B.C. Thanks to a multimarkers Request Permission
(/site/aboutpnas/rightperm.xhtml)
approach based on the analysis of mitochondrial and nuclear DNA (autosomes and Ychromosome), we
obtained information on the early Neolithic funeral practices and on the biogeographical origin of the
inhumed individuals. No close kinship was detected. Maternal haplogroups found are consistent with pre Share
Neolithicsettlement,whereastheYchromosomalanalysespermittedconfirmationoftheexistenceinSpain
approximately7,000yagooftwohaplogroupspreviouslyassociatedwiththeNeolithictransition:G2aand (/external-ref?
tag_url=http://www.pnas.org/cgi/content/short/108/45/18255&title
E1b1b1a1b. These results are highly consistent with those previously found in Neolithic individuals from
-+Lacan%20et%20al.%20108%20%2845%29%3A%2018255+--+PNAS
FrenchLateNeolithicindividuals,indicatingasurprisingtemporalgenetichomogeneityinthesegroups.The
highfrequencyofG2ainNeolithicsamplesinwesternEuropecouldsuggest,furthermore,thattheroleof (/external-ref?
menduringNeolithicdispersalcouldbegreaterthancurrentlyestimated. tag_url=http://www.pnas.org/cgi/content/long/108/45/18255&title=
-+Lacan%20et%20al.%20108%20%2845%29%3A%2018255+--+PNAS
TheNeolithictransitionwasacrucialstepinthehistoryofEuropeansettlement,buttheexactmodalitiesof
its dissemination are still not totally understood. In western Europe particularly, despite the abundance of
archeologicaldata,therealimportanceoftheMesolithicsubstrateandoftheNeolithicmigrantsinthefirst (/external-ref?
farmersoriginisacrucialpointstilldebatedamongthescientificcommunity(1).Inthiscontext,accessto tag_url=http://www.pnas.org/cgi/content/long/108/45/18255&title=
-+Lacan%20et%20al.%20108%20%2845%29%3A%2018255+--+PNAS
ancient DNA data seems to be a good way to trace and date the dispersal of European genetic lineages
andbetterunderstandtheoriginofcurrentpopulations. (/external-ref?
tag_url=http://www.pnas.org/cgi/content/long/108/45/18255&title=
Presently,fewancientdataareavailableontheNeolithicperiod,andmostofthemconsistofmitochondrial -+Lacan%20et%20al.%20108%20%2845%29%3A%2018255+--+PNAS
DNA data, which are only informative for the maternal origin. These have revealed a particularly high
(/external-ref?
frequency of haplogroup N1a, a haplogroup quite rare currently in central European (2,3) and in Atlantic
tag_url=http://www.pnas.org/cgi/content/long/108/45/18255&title=
coast Neolithic specimens (4), whereas this last was never found in southern European samples (57).
-+Lacan%20et%20al.%20108%20%2845%29%3A%2018255+--+PNAS
ThesefurthermoresuggestedaprobablegeneticcontinuitybetweenancientsouthernNeolithicspecimens
and current populations located in the same areas (6, 7), whereas the ancient central European plains (/external-ref?
samples would share a greater affinity with the modernday Near East and Anatolia (2). The findings tag_url=http://www.pnas.org/cgi/content/long/108/45/18255&title=
-+Lacan%20et%20al.%20108%20%2845%29%3A%2018255+--+PNAS
deducedfromthestudyofmaternalgeneticlineagesseemedconsistentwiththearcheologicalevidencesof
the existence of two distinct routes of neolithization: one along the central plains of Europe and another Published online before print
alongtheMediterraneancoasts. October 31, 2011, doi:
10.1073/pnas.1113061108
PNAS (Proceedings of the National Academy of
Concerning paternal lineages, because of the bad preservation of nuclear DNA in ancient samples, few
Sciences) November 8, 2011 vol. 108 no.
analyses have been performed to date on the Ychromosome of Neolithic specimens, thus few paternal 45 18255-18259
lineages existing at this period have been characterized. The study of only three male specimens Classifications
associatedwiththeLinearPotteryCulture,aNeolithicculturefoundinthecentralEuropeanplains(2),and Biological Sciences
of 22 men buried in a late Neolithic French necropolis (6) permitted data to be obtained on the paternal Anthropology (/search?
lineages existing before the Cooper and Bronze age migrations. Interestingly, they all revealed the tocsectionid=Anthropology&sortspec=date&submit=Submit)
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importanceoftheG2ahaplogroup,whichisrareinmodernEuropeanpopulations.Ofcourse,theseworks Citing This Article
do not provide a complete overview of the Neolithic male diffusion. Additionally, no data are currently Google Scholar
availableonthepaternallineagesexistingintheearlyMediterraneanNeolithic. PubMed
Similar to This Article
In this context, to improve the knowledge of the neolithization of southwestern Europe, we studied DNA
extractedfromhumanspecimensexcavatedintheAvellanercave,anancientfuneralcaveofnortheastern
SUBMITANARTICLE
Spain.Accordingto14Cdatingperformedonbonesandcharcoalsfoundinthecavity,thisfuneralcavewas (HTTP://WWW.PNASCENTRAL.ORG)
usedduringthefirstpartofthefifthmillenniumB.C.(8),whichcorrespondstotheendoftheestablishment
of the Neolithic cultures in Spain (Epicardial Culture). The study of this funeral site is thus particularly
interesting to access directly the gene pool of the first farmers in Spain and to understand the particular
funeralpracticesofthistransitionperiod,whicharestillpoorlyunderstood(9).
Becausemostofbonesfoundinthecavewerefragmentedandpartiallyburned,thefirstchallengeofthis
work was to identify individuals buried. Afterward, we analyzed different and complementary genetic
markers, located on autosomes and Ychromosomal and mitochondrial DNA to characterize any kinship
betweenindividualsandtotracetheirbiogeographicalorigin.
Through these data, the main objectives of this work were to genetically characterize early farmers from
northern Spain and to compare the genetic lineages found with those previously obtained from Neolithic
specimens and those currently present in European populations, to understand the complexity of the
NeolithicdispersalanditsheritageinsouthernEurope.
Results
Autosomal Results. Of the 27 samples studied, 14 permitted acquisition of unambiguous partial or complete
autosomal profiles, which can be related to seven individuals (Table 1). Of the seven individuals clearly
identified, six were male and one was female. No close familial relationship could be highlighted between
theseindividuals.EstimationofthenuclearDNAconcentrationpersamplerangedfrombelowthedetection
capabilityofthekitto34.2pg/L(Table1).
Table1.
In this window (18255/T1.expansion.html) Consensusshorttandemrepeat(STR)autosomal

In a new window (18255/T1.expansion.html) profilesofthesevenancientAvellanerindividuals
Mitochondrial Results. Mitochondrial HVSI sequences were obtained for the seven individuals and can be
classified into four different haplotypes (Table 2). All are still frequent in current European populations
(Table S1 (/lookup/suppl/doi:10.1073/pnas.1113061108//DCSupplemental/pnas.201113061SI.pdf?
targetid=nameddest=ST1)), and three of them were also found in ancient Neolithic samples (Table S2
(/lookup/suppl/doi:10.1073/pnas.1113061108//DCSupplemental/pnas.201113061SI.pdf?
targetid=nameddest=ST2)). These haplotypes permitted the determination that the individuals ave01,
ave02,andave06belongedtoK1a,ave04andave05toT2b,ave03toH3,andave07toU5haplogroups.
Table2.
In this window (18255/T2.expansion.html) MtDNAhaplotypesandhaplogroupsinferredforeach

In a new window (18255/T2.expansion.html) Avellanerspecimen
Forallsamples,typingofmitochondrialSNPsinthecodingregionpermittedconfirmationofthehaplogroup
determinationpreviouslyinferredfromthehaplotypes(Table2).
Y-Chromosomal Results. For the six male samples, two complete and four partial YSTRs haplotypes were
obtained(Table3).Theyallowedclassificationofindividualsintotwodifferenthaplogroups:G2a(individuals
ave01,ave02,ave03,ave05,andave06,whichseemtosharethesamehaplotype)andE1b1b1(individual
ave07). The four markers chosen to confirm belonging to these haplogroups (YE1b1b1M35.1, Y
E1b1b1a1bV13,YG2M287,andYG2aP15)weretypedwitharateof66%,whichpermittedconfirmation
thatfourmaleswereG2aandonewasE1b1b1a1b(Table3).
Table3.
In this window (18255/T3.expansion.html) YhaplogroupsinferredfromYSTRhaplotypesand

In a new window (18255/T3.expansion.html) NRYSNPstypingresultsforthemalespecimens
AnalysisofsharedhaplotypesshowedthattheG2ahaplotypefoundinancientspecimensisrareincurrent
populations: its frequency is <0.3% (Table S3
targetid=nameddest=ST3)). The haplotype of individual ave07 is more frequent (2.44%), particularly in
southeastern European populations (up to 7%). The Ave07 haplotype was also compared with current
Eb1b1a2haplotypespreviouslypublished(1014).Itappearedidenticalatthesevenmarkerstestedtofive
Albanian, two Bosnian, one Greek, one Italian, one Sicilian, two Corsican, and two Provence French
samples and are thus placed on the same node of the E1b1b1a1bV13 network as eastern, central, and
western Mediterranean haplotypes (Fig. S1
targetid=nameddest=SF1)).
Lactase Persistence Result.The LP13910C/T SNP associated with lactase persistence was successfully typed
forallancientsamplestested.Themutatedpositionwouldhaveappearedduringthedisseminationofthe
LinearpotterycultureincentralEurope(15).AllourancientsamplesfromSpainwerehomozygousC/Cfor
thismarker.
Discussion
Results Authenticity. The main difficulty in ancient DNA analyses is to produce authentic data. In this study,
drastic precautions previously described (6, 16) were taken to avoid contaminations, and a multimarkers
approach was used to validate the accuracy of the produced data. For the seven individuals presented
here,despitethefactthatalloftheauthenticitycriteriacouldnotbefullyrespected,resultsobtainedarein
favorofendogenousandreliableoutcomes:extractioncontrols,PCRblanks,andamplificationsfromDNA
extractedfromsheeporgoatremainswithhumanprimerswerealwaysnegative.ThenuclearDNAquantity
recovered and the inverse relationship between the amplification efficiency and length of the amplification
obtainedwerecharacteristicofadegradedancientDNA.Resultsacquiredfromthedifferentamplifications
and from cloning were always consistent between each other, and results of SNP typing were also 100%
concordant with mitochondrial and Ychromosome haplotypes previously deduced. The absence of the
polymorphism associated with the lactase persistence is also coherent with results previously published
fromancientMesolithicandNeolithicsamples(6,17,18).
Avellaner Genetic Diversity.Regarding the biogeographical origin of Avellaner individuals, mitochondrial and Y
chromosomalresultssuggestdifferentoriginsofmaternalandpaternallineages.Mitochondrialhaplogroups
found(U5,K1a,T2b,andH3),whicharequitecommoninwesternEurasia,arerelativelyuninformativefor
identifyingcleargeneticaffiliationswithdemographicmovements.However,theysuggestedafairlydiverse
origin of Avellaner maternal lineages, consistent with an early Neolithic group: a Paleolithic origin from
Middle East for haplogroup K1a, T2b, and U5 and a relation with the postglacial expansion from
southwesternEuropefortheH3haplogroup(19,20).Additionally,haplotypesidenticaltothoseassignedto
H3, K1a, and T2b haplogroups were previously found in samples related to central and Mediterranean
Neolithic cultures (Table S2
targetid=nameddest=ST2)). Only the U5 haplotype was never found in ancient specimens, but it differs at
onlyoneposition(np16051)fromanotherMesolithichaplotype(21).Thisfindingalsoobservedinotherlate
NeolithicsamplescouldindicateagreaterdiversityoftheU5clusterattheNeolithicperiod,consistentwith
anancientoriginofthislineage(6).
Concerningpaternallineages,onlytwodifferenthaplogroupswereidentified:G2aandE1b1b1a1b.
G2a is common in modern populations of Caucasus (10) but is quite rare in current western European
populations.Itrepresentsonlyapproximately4%ofthehaplogroupsfoundintheSpanishpopulation(22).It
seems nevertheless much more common in Neolithic samples because it was previously found in ancient
NeolithicsamplesfromthelinearpotterycultureinGermany,aswellasinlateNeolithicFrenchsamples(2,
6).Thus,itrepresentsoneofthemainYhaplogroupsfoundinNeolithicindividuals.Ofcourse,therearestill
toofewdatatoconfirmtheoverrepresentationoftheG2ahaplogroupamongwesternNeolithicpopulations,
butthisG2ainearlySpanishNeolithicsamplesisstrongevidenceofalinkpreviouslysuggestedbetween
NeolithicmigrationandG2adispersioninEurope(6).AdditionalG2ahaplotypeswill,however,beneededto
determine whether the G2a found in the male individual associated with dispersal of Neolithic in central
EuropeandthoselinkedwiththeMediterraneanroutesharedasameNeolithicMiddleEasternorigin.
For E1b1b1a1b, the link between this haplogroup and the Neolithic expansion could also be made. This
haplogroup,whichisthemainEuropeancladeofhaplogroupE,hasbeendescribedashavingspreadinto
westernEuropefromthesouthernBalkans(10,14,23),buttheexactperiodatwhichthisexpansionwould
beheldisstilldebated.Ithasbeenpreviouslyrelatedtoseveraldemographicevents,suchastheNeolithic
dispersal in direction of the eastern Adriatic (10) or along the VardarMoravaDanube rivers into central
Europe(24)orthemigrationsduringtheBronzeage(13,23,25). The presence of this haplogroup in an
early Neolithic sample in Spain confirms, therefore, that this marker may be related to the Mediterranean
Neolithic expansion, even if it does not permit quantification of the real importance of the Neolithization
contributioninthespreadofthishaplogroupinwesternEurope.Itconfirms,furthermore,thattheNeolithic
dispersalwasnot a uniform movement from the Middle East but that it was more probably an arrhythmic
phenomenonpunctuatedbyrapidexpansionphasesandperiodsofbreaksrelatedtoculturalchangeslike
theonepreviouslyidentifiedbyarcheologistsintheBalkansarea(2628).
Unusual Neolithic Burial Cave. Because of the fragmented state of skeletons, few data could be previously
obtained from the physical analysis of remains. Thanks to ancient DNA data, we prove that among the
sevenindividualsclearlyidentified,sixweremale.Nocloserelationshipcouldbedemonstrated,butfiveof
thesixmalesburiedseemtobelongtothesamepaternallineage,whichsuggestsafuneralrecruitmentof
individualsfromthesamegroup.Accordingtoarchaeologicalevidence,fewburialplaceswerefoundatthe
recentphasesoftheEarlyNeolithiccomparedwiththeputativepopulationdensityatthisperiod.Epicardial
burialswerefurthermoreusuallyindividualinnaturalcavitiesliketheGazelcave,Aude,France,orinopen
airsiteslikeCal'Estrada,Catalonia(1).CollectiveburialsappearedlaterduringtheLateNeolithicperiod(IV
andIIImillenniaB.C.).Inthiscontext,thefuneralrecruitmentoftheAvellanercaveseemsveryunusualfor
theearlyNeolithicperiod(1,29).Theabsenceofanysignificantgravegoodsinthecavitiesisnotinfavorof
funeral recruitment according to potential social elite. According to archaeological hypotheses, it could
ratherreflectacontinuanceoffuneraryritesfromthelateMesolithicperiod(1).Thepresenceofindividuals
carrying paternal lineages linked with the Neolithic expansion in a funeral cave where Mesolithic funeral
practices were used could suggest the maintenance of the Mesolithic traditions during the early stages of
thewesternEuropeNeolithic.NogeneticdatafromMesolithicgravespecimensarecurrentlyavailabletobe
compared with the genetic structure obtained. Further genetic analyses of ancient southern European
graveswillbenecessarytovalidatethishypothesisandpotentiallyprovideabetterideaabouttheoriginof
thisparticularburial.
Avellaner and the Neolithic Transition.Alloftheresultsobtainedareconcordantwiththosepreviouslypublishedfor

Avellaner and the Neolithic Transition.Alloftheresultsobtainedareconcordantwiththosepreviouslypublishedfor
ancient Neolithic specimens. The mitochondrial lineages found are consistent with a genetic continuity in
southern Europe, at least since Neolithic times, and the absence of the N1a haplogroup widespread in
centralEuropeconfirmsfurthermorethearchaeologicalevidenceoftheexistenceoftworoutesofNeolithic
dispersal in Europe. Moreover, the paternal lineages characterized and their current repartition along the
Mediterraneancoastsconfirmthisassumption.
The sexspecific diversity observed in Avellaner specimens is finally broadly similar to that previously
observed in the samples of the Treilles cave, a French funeral cave 2,000 y more recent than the one
presentedhere.Inbothstudies,thePaleolithicoriginofmostofthematernallineagescoupledwithamore
recent paternal ancestry as well as the G2a presence could thus suggest a common origin of the two
Neolithic groups and a probable genetic continuity in the western Mediterranean area from 5000 to 3000
B.C.
The high frequency of G2a haplogroup in Neolithic specimens, whereas this haplogroup is very rare in
currentpopulations,alsosuggeststhatmencouldhaveplayedaparticularlyimportantroleintheNeolithic
disseminationthatisnolongervisibletoday.ThiswouldimplythatintraEuropeanmigrationsrelatedtothe
metalagesmayhavestronglyaffectedthemoderngenepool.
Conclusion
ThisworkoffersadirectoverviewofthegeneticlineagesofthefirstnorthernSpanishfarmers.Itrevealsthe
complexityoftheimplementationofagricultureinSpainandtheprobablehighlevelofheterogeneityofthe
NeolithicdisseminationinEurope.Ithighlightsfurthermorethatmaternalandpaternallineagescouldhave
had different histories, which complicates even more the different scenarios issued on the Neolithic
transitioninEurope.Thisstudy,whichwasperformedononlysevenindividuals,isofcoursenotsufficientto
estimate the real importance of the arrival of men in the Neolithic transition, and new investigations on
ancientsouthernspecimenswillbenecessarytoimproveourknowledgeonthiscrucialperiod.
Materials and Methods

TheAvellanercaveisasmallburialcavelocatedinCatalonia,innortheasternSpain.Themaincavityisin
fact divided into three independent areas separated by stone walls, each containing several successive
primaryorsecondaryburials.Skeletonsfoundwerenotinanatomicconnection,whichdidnotpermitformal
individualizationofeachindividualhowever,theminimumnumberofindividualscouldbeestimatedat19
(8).Becauseofthefragmentationandthemixofboneswithineachsepulchralplace,wedecidedtowork
fromteethstillfixedonthefourmandiblefragmentsavailable(twoorthreeteethforeachfragment),onthe
mostwellpreservedscatteredteeth,andthreefemoralshafts.Inall,weanalyzed27humansamplestaken
in the three cavities, as well as two nonhuman material (two sheep teeth) taken at the same time with
humanremainstodetectpossiblecontaminationeventsduringexcavation.
Sample Preparation and DNA Extraction. Bones samples were first abraded with sterile equipment before UV
exposure and grinding into a liquid nitrogen environment. Teeth were also crushed after decontamination
with bleach and UV exposure 30 min on each side. DNA was then extracted according to a protocol
previouslydescribed(30).Fourtofiveextractionswererealizedoneachsample,accordingtothepowder
quantityrecovered.
Nuclear DNA Analysis.For at least one extract per sample we determined the nuclear DNA quantity extracted
usingtheQuantifilerHumanDNAQuantificationKit(AppliedBiosystems).
Autosomal profiles were determined using both AmpFlSTR Identifiler Plus and the MiniFiler PCR
Amplification Kits (Applied Biosystems) on a 3500 Genetic Analyzer. STRs profiles were analyzed with
GeneMapper4.1software.TwoamplificationswereperformedoneachDNAextract.
Haplotype Determination.Mitochondrial haplotypes were obtained by the sequencing of 381 base pairs of the
HVSI region of the mtDNA in two overlapping fragments, as previously described (16). To meet the
authenticity criteria, we also cloned the amplicons obtained during the analyses of 5 of the 27 samples.
Cloning was performed using the pGEMT Easy Vector system II kit (Promega), according to the
manufacturerprotocol.Between16and28cloneswereanalyzedforeachsample.Allsequencesobtained
wereusedtodeducemitochondrialhaplogroupsaccordingtothelatestmtDNAphylogeny(31).
Formaleindividuals,Ychromosomalhaplotypeswereobtainedfromtheanalysisof17YSTRslociusing
the AmpFlSTR Yfiler PCR Amplification Kit (Applied Biosystems). They were used to estimate Y
haplogroupsthankstotheHaplogroupPredictorsoftware(32).
Haplogroup Assignment and Typing of an SNP Associated with Lactase Persistence.Toclarifythehaplogroupstatusinferred

from HVSI sequences and Ychromosomal haplotypes, we analyzed supplemental SNPs localized on the
mitochondrialcodingregionandthenonrecombiningregionoftheYchromosome(NRY).SNPtypingwas
performed using iPLEX Gold technology (Sequenom), which seems to be a very sensitive and effective
typingtechnologyfordegradedDNAanalyzes(30).Twomultiplexescontainingatotalof17SNPslocated
onmtDNA,theNRY,andtheMCM6gene(SNPassociatedwiththelactasepersistence)weredesignedwith
MassArrayAssaydesignsoftware(version4.0).Thetypingreactionswereperformedtwiceontwodifferent
DNAextractspersample.
Statistical Analysis. The putative genetic relationships were investigated from autosomal STR profiles with
DNAVIEWSoftware(33).
To compare ancient Spanish genetic lineages obtained and those current in European populations,
analyses of shared haplotypes were performed thanks to two personal databases comprising 14,645
mitochondrial HVSI sequences and 14,166 Yhaplotypes. Mitochondrial profiles obtained were also
compared with ancient Neolithic haplotypes previously published. Detailed compositions of the different
datasets are available in Table S2
targetid=nameddest=ST2) and Table S4
Navigate This Article
Top
targetid=nameddest=ST4). To allow maximum comparability among all populations, Yshared haplotype
analyses were performed on only seven YSTRs markers (DYS19, DYS390, DYS391, DYS392, DYS393, Abstract
DYS389I,andDYS389II).
Results
AhaplotypenetworkwasgeneratedforNRYhaplogroupEV13viathemedianjoiningalgorithmofNetwork,
Discussion
version 4.5.1.6. To obtain the most parsimonious networks the reticulation permissivity was set to zero.
DatasetswerepreprocessedusingthestarcontractionoptioninNetwork,version4.5.1.6(5).ThesevenY Conclusion
STRlociusedwereweightedaccordingtotheobservedSTRallelicvariance,asdescribedbyQamaretal.
(34). Materials and Methods
Acknowledgments
Acknowledgments Footnotes
We thank Xevi Roura (Museu Comarcal) for access to the ancient samples, and Angela Gonzalez for her References
helpwithSequenomtechnology.
Footnotes
1
Towhomcorrespondenceshouldbeaddressed.Email:lacan.marie@netcourrier.com
(mailto:lacan.marie@netcourrier.com).
Authorcontributions:M.L.designedresearchM.L.performedresearchJ.T.andA.B.contributednewreagents/analytic
toolsM.L.analyzeddataandM.L.,C.K.,F.X.R.,N.B.,J.G.,E.C.,andB.L.wrotethepaper.
Theauthorsdeclarenoconflictofinterest.
ThisarticleisaPNASDirectSubmission.
Thisarticlecontainssupportinginformationonlineat
www.pnas.org/lookup/suppl/doi:10.1073/pnas.1113061108//DCSupplemental
(/lookup/suppl/doi:10.1073/pnas.1113061108//DCSupplemental).
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Ancient DNA Suggests The Leading Role Played by Men in The Neolithic Dissemination

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Totraceanddategeneticlineagespotentiallybroughtduringthistransitionandsounderstandtheoriginof Export Citation

In this window (18255/T1.expansion.html) Consensusshorttandemrepeat(STR)autosomal

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9.MartinA,EdoE,TarrusJ,ClopX (2010)MmoiresLIdelaSocitPrhistoriqueFrancaise ,Le

27.MazurideKeroualinK (2003)GenseetDiffusiondel'AgricultureenEurope (ditionsErrance,

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