Rare dental trait provides morphological evidence of archaic introgression in Asian fossil record


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Rare dental trait provides morphological evidence of archaic introgression in Asian fossil record

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Rare dental trait provides morphological evidence of archaic introgression in Asian fossil record
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PNAS
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Bailey, Shara E.
Hublin, Jean-Jacques
Anton, Susan C.
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National Academy of Sciences
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The recently described Denisovan hemimandible from Xiahe, China [F. Chen et al., (2019) Nature 569, 409–412], possesses an unusual dental feature: a 3-rooted lower second molar. A survey of the clinical and bioarchaeological literature demonstrates that the 3-rooted lower molar is rare (less than 3.5% occurrence) in non-Asian Homo sapiens. In contrast, its presence in Asian-derived populations can exceed 40% in China and the New World. It has long been thought that the prevalence of 3-rooted lower molars in Asia is a relatively late acquisition occurring well after the origin and dispersal of H. sapiens. However, the presence of a 3-rooted lower second molar in this 160,000-y-old fossil hominin suggests greater antiquity for the trait. Importantly, it also provides morphological evidence of a strong link between archaic and recent Asian H. sapiens populations. This link provides compelling evidence that modern Asian lineages acquired the 3-rooted lower molar via introgression from Denisovans.
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PNAS, Vol. 116, no. 30 (2019-07-08).

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Raredentaltraitprovidesmorphologicalevidenceof archaicintrogressioninAsianfossilrecord SharaE.Bailey a,b,1 ,Jean-JacquesHublin b,c ,andSusanC.Antón a a CenterfortheStudyofHumanOrigins,DepartmentofAnthropology,NewYorkUniversity,NewYork,NY10003; b DepartmentofHumanEvolution,Max PlanckInstituteforEvolutionaryAnthropology,04103Leipzig,Germany;and c CollègedeFrance,75005Paris,France EditedbyJamesF.O ’ Connell,UniversityofUtah,SaltLakeCity,UT,andapprovedJune12,2019(receivedforreviewMay3,2019) TherecentlydescribedDenisovanhemimandiblefromXiahe, China[F.Chenetal.,(2019) Nature 569,409 – 412],possessesan unusualdentalfeature:a3-rootedlowersecondmolar.Asurvey oftheclinicalandbioarchaeologicalliteraturedemonstratesthat the3-rootedlowermolarisrare(lessthan3.5%occurrence)innonAsian Homosapiens .Incontrast,itspresenceinAsian-derivedpopulationscanexceed40%inChinaandtheNewWorld.Ithaslong beenthoughtthattheprevalenceof3-rootedlowermolarsinAsia isarelativelylateacquisitionoccurringwellaftertheoriginand dispersalof H.sapiens .However,thepresenceofa3-rootedlower secondmolarinthis160,000-y-oldfossilhomininsuggestsgreater antiquityforthetrait.Importantly,italsoprovidesmorphological evidenceofastronglinkbetweenarchaicandrecentAsian H.sapiens populations.Thislinkprovidescompellingevidencethatmodern Asianlineagesacquiredthe3-rootedlowermolarviaintrogression fromDenisovans. Denisovan | introgression | dentalanthropology | rootmorphology | Pleistocene Homo T henewDenisovanhemimandiblefromXiahe,China(1), exhibitsa3-rootedlowermolar,providingadirectmorphologicallinkbetweenarchaicandrecentAsian Homosapiens populations.Althoughmandibularmolarsaremostcommonly 2-rootedinthegenus Homo ,rootnumbervariesfrom1to3(2)or more(3).Three-rootedlowermolarsmaintainbothmesialand distalroots,withathirdaccessoryrootoneitherthedistolingual aspectorlinguallybetweenthemesialanddistalroots(Fig.1). Thethirdrootisnotasimplebifurcationofeitherthemesialor distalroottips.Whiletheaccessoryrootcanbequitesmall,itis usuallyaboutone-thirdthesizeofthenormalroots(2).Inrecent humans,thethirdrootusuallyoccursonthemandibularfirst molar(referredtoasa3RM1)butmayalsooccuronthelower secondandthirdmolars;werefertothesecollectivelyas3RM (4 – 6).The3RMmayappeareitherunilaterallyorbilaterally;the singletwinstudyofwhichwear eawareshowsbilateraldevelopmentinbothtwins,suggestingageneticunderpinning(7).The 3RMenteredtheclinicalliteraturein1844(8),beingcalledradix entomolarisbyBolk(9);itwascodifiedintotheArizonaState UniversityDentalAnthropologySystemin1991(2). Extensiveclinicalandbioarchaeologicalstudiesconfirmthe rarityof3RMoutsideofAsiaandtheNewWorld( DatasetS1 ). InAsian-derivedpopulations,thefrequencyofthe3RMcan exceed40%(Aleut,NeolithicChina),whereas,innon-Asian derivedpopulations,thefrequencyrangesfrom0to3.4%.The rarityofthe3RMinnon-Asian H.sapiens islowenoughtobe explainedbymutationalone(2).Thehighfrequenciesof3RMin northeastAsiansandNativeAmericansisakeyfeaturelinking NativeAmericanoriginstoAsia(10). DespiteitshighfrequencyinrecentAsian-derivedpopulations, the3RMhasnotbeenreportedintheearliest H.sapiens from Asia(11),norhaveweobservedthetraitinearly H.sapiens from Africaor Homoerectus inAsia.*Wenote,however,thatthelack ofradiographyofmanyspecimensandtheabsenceoftheoriginalZhoukoudianremainsmakethisconclusionpreliminary. Beforetherecentdiscoveries,theearliestexampleofa3RM camefroman H.sapiens mandiblefromthePhilippines(15), perhapsfromthesiteofTabon,whichhasfossil-bearingstrata datingto9ka,16.5ka,andasmuchas47ka,andmorerecent Jarburials(16,17).Themandible,originallydescribedby Macintoshetal.(18),showsabilateral3RMwithanaccessory rootsituatedlinguallybetweenthemesialanddistalroots(15). Givenalackofearlyevidencefor3RM,oneexplanationforits highfrequencyinAsiahasbeenarelativelyrecentacquisition postdatingtheoriginof H.sapiens andoccurringwellaftertheir dispersalintoEurasia. Tworecentlydescribedmandiblessuggestamoreancient Asianoriginfor3RM,andonethatprecedes H.sapiens inthe region.ThenewlydiscoveredindividualfromXiahe,China — identifiedasDenisovanthroughpaleoproteomics(1) — possessesa3-rootedlowersecondmolar(3RM2)(Fig.1). † This individualisdatedto160ka.TherecentlydescribedPenghu1 mandiblefromTaiwan(190to10ka)alsoexhibitsa3RM2(19). Althoughtheauthorssuggestthe3RM2differsfromthatdescribedbyTurneretal.(2),itisclearthatthemorphologyof Penghu1fallswithinthevariationdescribedbypreviousstudies (2,10):Thethirdrootappearslinguallyasanaccessoryroot betweenthemesialanddistalroots.ThePenghumandibleretains “ archaic ” features,includingarecedingsymphysisthat lacksachin,athickmandibularcorpus,andlargemolarcrowns similarinsizetoDenisovans(20).LikeXiahe,theseexceptionallylargemolarsarecoupledwithagenesisofthethirdmolar (19).Forthesereasons,Chenetal.(1)suggestthatPenghu1 mayalsobecloselyrelatedtoDenisovans.Bothmandiblesshow thatthe3RManomalyexistedinarchaicAsianhomininsbefore H.sapiens intheregion. These2recentlyreportedfossilssuggestthatthe3RM1)very likelyoriginatedinAsiaand2)evolvedinapresapiens population.Moreover,untila3RMisfoundinmorearchaichominins, itshouldbeunderstoodasamorphologicaltraitthatwas transferredto H.sapiens throughgeneflowwithDenisovans. Geneflowbetween H.sapiens andDenisovanshasbeendocumented,includingamutation(atEPAS1)relatedtohigh-altitude adaptationsharedbyaSiberianDenisovanandmodernTibetans Authorcontributions:S.E.B.designedresearch;S.E.B.andS.C.A.performedresearch; J.-J.H.contributeddata;S.E.B.analyzeddata;andS.E.B.,J.-J.H.,andS.C.A.wrote thepaper. Theauthorsdeclarenoconflictofinterest. Thisopenaccessarticleisdistributedunder CreativeCommonsAttribution-NonCommercialNoDerivativesLicense4.0(CCBY-NC-ND) . 1 Towhomcorrespondencemaybeaddressed.Email:sbailey@nyu.edu. Thisarticlecontainssupportinginformationonlineat www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1907557116/-/DCSupplemental . PublishedonlineJuly8,2019. *WuandXianglong(12)reportthepresenceofa3RM1inthe1959Zhoukoudianmandible(PA86)basedonobservationsofitsleftM1rootsocket.Publishedphotographs (13,14),however,showasmallseptumofthemesialrootsocket(thatmayrepresenta bifurcatedmesialroot)butnoevidenceofalingualaccessoryroot.The3RManomaly requiresthattheaccessoryrootoccursbetweenthemesialanddistalrootorasalingual accessoryofthedistalroot. † Thefirstmolarinthisindividualhas2roots. 14806 – 14807 | PNAS | July23,2019 | vol.116 | no.30www.pnas.org/cgi/doi/10.1073/pnas.1907557116

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(21).Importantly,Nepalalsoshowsoneofthehighestoccurrences(25%)of3RMinEastAsia( DatasetS1 ).Likethehighaltituderelatedmutation,whichisretainedduetopositiveselection(21),theretentionof3RMathighfrequencyinAsiamay berelatedtoselectionformolarretentioninpopulationswith heavymasticatoryloading(22).Suchselectionalsoexplainsthe lowerfrequencyof3RMinrecentpopulationswithhigher Denisovanintrogression(e.g.,Australia/NewGuinea)butdemonstrablylessmasticatoryrobusticity(23).Alternatively,3RM frequenciesmayreflectanindirectinfluenceresultingfromselectiononanothertraitunderhighselection,ashasbeensuggestedtobethecaseforincisorcrownmorphologyandEDAR inNorthandEastAsiansandintheNewWorld(24).Whatever thecause,wearguethatthe3RManomalyisanexampleofa morphologicalcharacterinrecenthumansthatcanbeclearly tracedtothisarchaicadmixture. The3RMisanAsian-derivedcharacterthatwecandefinitivelytracetoDenisovans.Thus,wenowhaveveryclearevidencethatgeneflowbetweenarchaicgroupsand H.sapiens resultedinthetransferofidentifiablemorphologicalfeatures. TherehavebeenanumberofAsian H.sapiens fossilsdescribed recentlythatpointtoadmixturewitharchaichumansasanexplanationforthepresenceofprimitivetraits[e.g.,Dushan(11) andTianyuan(25)].Ifthe3RMwastransferredfromarchaic humansto H.sapiens, othertraitsmayhavebeenaswell.Indeed, thepresenceof “ archaicfeatures ” inrecentAsiansthatwere onceusedtosuggestcontinuityfromPleistoceneAsian H.erectus (26 – 28)mayalsohavebeenobtainedbyintrogressionfrom Denisovans. 1.F.Chen etal .,AlateMiddlePleistoceneDenisovanmandiblefromtheTibetanPlateau. Nature 569 ,409 – 412(2019). 2.C.G.Turner,II,C.R.Nichol,G.R.Scott, “ Scoringproceduresforkeymorphological traitsofthepermanentdentition:TheArizonaStateUniversityDentalAnthropology System ” in AdvancesinDentalAnthropology ,M.Kelley,C.Larsen,Eds.(WileyLiss, NewYork,NY,1991),pp.13 – 31. 3.S.J.Sidow,L.A.West,F.R.Liewehr,R.J.Loushine,Rootcanalmorphologyofhuman maxillaryandmandibularthirdmolars. J.Endod. 26 ,675 – 678(2000). 4.J.A.B.Ferraz,J.D.Pécora,Three-rootedmandibularmolarsinpatientsofMongolian, CaucasianandNegroorigin. Braz.Dent.J. 3 ,113 – 117(1993). 5.O.Carlsen,V.Alexandersen,Radixentomolaris:Identificationandmorphology. Scand.J.Dent.Res. 98 ,363 – 373(1990). 6.A.Erkman,F.Kaya,Morphologicalvariationsinthree-rootedmandibularmolarsin AncientAnatolianpopulations(DilkayaMound,Van,Turkey):Aliteraturereviewon worldpopulations. Mediterr.Archaeol.Archaeom.Int.J. 14 ,1 – 11(2012). 7.A.C.Gabriel, “ Genetictypesinteeth ” in EssaysinBiology ,A.N.Burkitt,Ed.(AustralianMedicalPublishing,Sydney,NSW,Australia,1948),pp7 – 61. 8.G.Carabelli, SystematischesHandbuchderZahnheilkunde (BraumüllerandSeidel, Vienna,Austria,1844). 9.L.Bolk,BemerkungenüberWurzelvariationenammenschlichenunterenMolaren. Z. Morphol.Anthropol. 17 ,605 – 610(1915). 10.C.G.Turner,II,Three-rootedmandibularfirstpermanentmolarsandthequestionof AmericanIndianorigins. Am.J.Phys.Anthropol. 34 ,229 – 241(1971). 11.W.Liao etal .,MosaicdentalmorphologyinaterminalPleistocenehomininfrom DushanCaveinsouthernChina. Sci.Rep. 9 ,2347(2019). 12.L.Wu,Z.Xianglong,Preliminaryimpressionofcurrentdentalanthropologyresearch inChina. DentalAnthropologyNewsletter 9 ,1 – 5(1995). 13.X.Wu,F.E.Poirier, HumanEvolutioninChina.AMetricDescriptionoftheFossilsand aReviewoftheSites (OxfordUniversityPress,Oxford,UK,1995). 14.J.Wu,T.Chao,Newdiscoveryofa Sinanthropus mandibleinChoukoutien. PaleovertebrataetPaleoanthropologia 1 ,155 – 158(1959). 15.B.Barker,DentalfeaturesoftheTabonMandible:Anappendix. Archaeol.Phys. Anthropol.Ocean. 13 ,160 – 166(1978). 16.E.Dizon,NewdirectdatingofthehumanfossilsfromTabonCave,Palawan, Phillipines. Proc.Soc.Philipp.Archaeologists 1 ,63 – 67(2003). 17.J.Corny, “ Lesresteshumainsdelagrottede Tabon(Palawan,Philippines): Répartitionspatialeetétuded ’ unecollectiond ’ ossementsinédite, ” MSthesis,Muséumnationald ’ Histoirenaturelle,Paris,France(2008). 18.N.MacIntosh,B.Barker,S.Larnach,TheTabonCavemandible. Archaeol.Phys.Anthropol.Ocean. 13 ,143 – 159(1978). 19.C.-H.Chang etal .,Thefirstarchaic Homo fromTaiwan. Nat.Commun. 6 ,6037(2015). 20.D.Reich etal .,GenetichistoryofanarchaichominingroupfromDenisovaCavein Siberia. Nature 468 ,1053 – 1060(2010). 21.E.Huerta-Sánchez etal .,AltitudeadaptationinTibetanscausedbyintrogressionof Denisovan-likeDNA. Nature 512 ,194 – 197(2014). 22.C.G.Turner,II,LatePleistoceneandHolocenepopulationhistoryofEastAsiabased ondentalvariation. Am.J.Phys.Anthropol. 73 ,305 – 321(1987). 23.S.C.Antón,H.Carter-Menn,V.B.DeLeon,Modernhumanorigins:Continuity,replacement,andmasticatoryrobusticityinAustralasia. J.Hum.Evol. 60 ,70 – 82(2011). 24.L.J.Hlusko etal .,Environmentalselectionduringthelasticeageonthemother-toinfanttransmissionofvitaminDandfattyacidsthroughbreastmilk. Proc.Natl.Acad. Sci.U.S.A. 115 ,E4426 – E4432(2018). 25.H.Shang,H.Tong,S.Zhang,F.Chen,E.Trinkaus,Anearlymodernhumanfrom TianyuanCave,Zhoukoudian,China. Proc.Natl.Acad.Sci.U.S.A. 104 ,6573 – 6578 (2007). 26.D.Frayer,M.Wolpoff,A.Thorne,F.Smith,G.Pope,Theoriesofmodernhumanorigins:Thepaleontologicaltest. Am.Anthropol. 95 ,14 – 50(1993). 27.W.Liu, “ ThedentalcontinuityofhumansinChinafromPleistocenetoHolocene,and theoriginsofMongoloids ” in Proceedingsofthe30thAnnualGeologicalCongress (VSPPublishing,Wakefield,UK,1997),vol.21,pp.24 – 32. 28.M.Wolpoff,A.Thorne,F.Smith,D.Frayer,G.Pope, “ Multiregionalevolution:A world-widesourceformodernhumanpopulations ” in OriginsofAnatomically ModernHumans,InterdisciplinaryContibutionstoArchaeology ,M.Nitecki,D.Nitecki, Eds.(PlenumPress,NewYork,NY,1994),pp.176 – 199. Fig.1. The3-rootedlowermolaranomaly.Three-rootedlowerfirstmolaralveolarsocketsshowingdistolingualpositionofaccessoryrootandthe3-rooted lowerfirstmolar(lingualview);( Inset )3-rootedlowersecondmolarofXiaheDenisovanindividual(lingualview). Left and Middle imagescourtesyofChristine Lee(CaliforniaStateUniversity,LosAngeles,CA).M,mesial;L,lingual;D,distal;B,buccal. Baileyetal. PNAS | July23,2019 | vol.116 | no.30 | 14807 ANTHROPOLOGY BRIEFREPORT


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