Did Our Species Evolve in Subdivided Populations across Africa, and Why Does It Matter?

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Did Our Species Evolve in Subdivided Populations

across Africa, and Why Does It Matter?

Eleanor Scerri, Mark Thomas, Andrea Manica, Philipp Gunz, Jay Stock,

Chris Stringer, Matt Grove, Huw Groucutt, Axel Timmermann, G. Philip

Rightmire, et al.

To cite this version:

Eleanor Scerri, Mark Thomas, Andrea Manica, Philipp Gunz, Jay Stock, et al.. Did Our Species

Evolve in Subdivided Populations across Africa, and Why Does It Matter?. Trends in Ecology and

Evolution, Elsevier, 2018, 33 (8), pp.582-594. �10.1016/j.tree.2018.05.005�. �hal-02347261�

Opinion

Did

Our

Species

Evolve

in

Subdivided

Populations

across

Africa,

and

Why

Does

It

Matter?

Eleanor

M.L.

Scerri,

* Mark

G.

Thomas,

Andrea

Manica,

Philipp

Gunz,

Jay

T.

Stock,

Chris

Stringer,

Matt

Grove,

Huw

S.

Groucutt,

Axel

Timmermann,

G.

Philip

Rightmire,

Francesco

d

’Errico,

Christian

A.

Tryon,

Nick

A.

Drake,

Alison

S.

Brooks,

Robin

W.

Dennell,

Richard

Durbin,

Brenna

M.

Henn,

Julia

Lee-Thorp,

Peter

deMenocal,

Michael

D.

Petraglia,

Jessica

C.

Thompson,

Aylwyn

Scally,

and

Lounès

Chikhi

Wechallengetheviewthatourspecies,Homosapiens,evolvedwithinasingle populationand/or region of Africa. Thechronologyand physical diversity of Pleistocene human fossils suggest that morphologically varied populations pertainingtotheH.sapienscladelivedthroughoutAfrica.Similarly,theAfrican archaeologicalrecorddemonstratesthepolycentricoriginandpersistenceof regionallydistinctPleistocenematerial culturein avarietyofpaleoecological settings.Genetic studies alsoindicatethatpresent-day populationstructure withinAfricaextendstodeeptimes,parallelingapaleoenvironmentalrecordof shiftingandfracturedhabitablezones.We arguethatthesefieldssupportan emergingviewofahighlystructuredAfricanprehistorythatshouldbe consid-eredinhumanevolutionary inferences,promptingnewinterpretations, ques-tions,andinterdisciplinaryresearchdirections.

ADifferentViewofAfricanOrigins

ThelineageofHomosapiensprobablyoriginatedinAfricaatleast500thousandyearsago

(ka)[1], andthe earliestobservedmorphological manifestations ofthis clade appearedby

300ka[2].EarlyH.sapiensfossilsdonotdemonstrateasimplelinearprogressiontowards

contemporaryhumanmorphology.Instead,putativeearlyH.sapiensremainsexhibit

remark-ablemorphologicaldiversityandgeographicalspread.Togetherwithrecentarchaeologicaland

geneticlinesofevidence,thesedataareconsistentwiththeviewthatourspeciesoriginated

anddiversifiedwithinstronglysubdivided(i.e.,structured)populations,probablylivingacross

Africa,that were connectedbysporadicgeneflow [1,3–8].Thisconcept of‘African

multi-regionalism’ [1] may also include hybridization between H. sapiens and more divergent

hominins(seeGlossary)living indifferentregions[1,9–12].Crucially,suchpopulation

sub-divisionsmayhavebeenshapedandsustainedbyshiftsinecologicalboundaries[7,13,14],

challengingtheviewthatourspecieswasendemictoasingleregionorhabitat,andimplyingan

oftenunderacknowledgedcomplexitytoourAfricanorigins.

Inthis paperweexamine andsynthesizefossil,archaeological, genetic,and

paleoenviron-mentaldatato refine ourunderstandingof thetime-depth, character,and maintenanceof

Pleistocenepopulationstructure.Indoingso,weattempttoseparatedatafrominferenceto

stressthat using models ofpopulation structure fundamentally changes interpretations of

recenthumanevolution.

Highlights

TheviewthatHomosapiensevolved fromasingleregion/populationwithin Africahasbeengivenprimacyin stu-diesofhumanevolution.

However,developmentsacross multi-plefieldsshowthatrelevantdataare nolongerconsistentwiththisview.

WeargueinsteadthatHomosapiens evolved within a set of interlinked groups living across Africa, whose connectivitychangedthroughtime.

Genetic models therefore need to incorporateamorecomplexviewof ancientmigration anddivergence in Africa.

We summarize this new framework emphasizingpopulationstructure, out-linehowthischangesour understand-ing ofhuman evolution,andidentify newresearchdirections.

1

SchoolofArchaeology,Universityof Oxford,SouthParksRoad,Oxford OX13TG,UK

2

DepartmentofArchaeology,Max PlanckInstitutefortheScienceof HumanHistory,KahlaischeStreet10, D-07745Jena,Germany

3

ResearchDepartmentofGenetics, EvolutionandEnvironment,and UniversityCollegeLondon(UCL) GeneticsInstitute,UniversityCollege London,GowerStreet,LondonWC1E 6BT,UK

4

DepartmentofZoology,Universityof

Cambridge,CambridgeCB23EJ,UK 5

DepartmentofHumanEvolution,Max PlanckInstituteforEvolutionary Anthropology,DeutscherPlatz6, D-04103Leipzig,Germany

6

DepartmentofArchaeology, UniversityofCambridge,Pembroke Street,Cambridge,CB23DZ,UK 7

DepartmentofAnthropology, UniversityofWesternOntario, London,ON,N6A3K7,Canada 8

DepartmentofEarthSciences,The NaturalHistoryMuseum,Cromwell Road,LondonSW75BD,UK 9

DepartmentofArchaeology,Classics andEgyptology,Universityof Liverpool,12-14AbercrombySquare, LiverpoolL697WZ,UK

10

CenterforClimatePhysics,Institute forBasicScience,Busan,South Korea

11

PusanNationalUniversity,Busan, SouthKorea

12

DepartmentofHumanEvolutionary Biology,HarvardUniversity, Cambridge,MA02138,USA 13

CentreNationaldelaRecherche Scientifique(CNRS)UnitéMixtede Recherche(UMR)5199PACEA(Dela Préhistoireàl'actuel:Culture, EnvironnementetAnthropologie), UniversitédeBordeaux,Bâtiment B18,AlléeGeoffroySaintHilaire,CS 50023,F-33615PessacCEDEX, France

14

SenterforFremragendeForskning (SFF)CentreforEarlySapiens Behaviour(SapienCE),Universityof Bergen,Øysteinsgate3,Postboks 7805,5020,Bergen,Norway 15

DepartmentofAnthropology, HarvardUniversity,Cambridge,MA 02138,USA

16

Geography,King’sCollegeLondon, Strand,London,WC2R2LS,UK 17

DepartmentofAnthropology,Center forAdvancedStudyofHominid Paleobiology,TheGeorgeWashington University,2110GStreetNorthWest, Washington,DC20052,USA 18

DepartmentofArchaeology, UniversityofExeter,Exeter,UK 19

DepartmentofGenetics,University ofCambridge,DowningStreet, CambridgeCB23EH,UK 20

WellcomeTrustSangerInstitute, WellcomeTrustGenomeCampus, Hinxton,UK

21

DepartmentofAnthropologyandthe GenomeCenter,Universityof California,Davis,CA95616USA 22

DepartmentofEarthand EnvironmentalSciences,Columbia University,Lamont-DohertyEarth Observatory,61Route9West, Palisades,NY10964-1000,USA

TheMorphological DiversityandSpreadoftheHomosapiensClade

Theconstellationof morphologicalfeatures characterizing H.sapiens isdebated. Thishas

stronglyimpactedoninterpretationsofrecenthumanoriginsbyvariablyincludingorexcluding

differentfossilsfrominterpretativeanalyses.Forexample,differentmorphologicalcriteriaand

analyticalmethodshavebeenusedtosupportbothagradual,mosaic-likeprocessof

mod-ernizationofourspeciesor,conversely,apunctuatedspeciation(e.g.,[1]).

Extanthumancraniaarecharacterizedbyacombinationoffeaturesthatdistinguishusfromour

fossilrelativesandancestors,suchasasmallandgracileface,achin,andaglobularbraincase.

However,thesetypicalmodernhumanfeaturesemergeinamosaic-likefashionwithintheH.

sapiensclade.TheoldestcurrentlyrecognizedmembersoftheH.sapiensclade,fromJebel

IrhoudinNorthAfrica,haveafacialmorphologyverysimilartoextantH.sapiens,aswellas

endocranialvolumesthatfall withinthecontemporaryrangeofvariation[2].However,their

braincaseshapesareelongated ratherthanglobular,suggestingthatdistinctivefeaturesof

brainshape,andpossiblybrainfunction,evolvedwithinH.sapiens[2,5](Figure1).Otherearly

H.sapiensfossilsfromFlorisbadinSouthAfrica(260ka),OmoKibish(195ka)andHerto

(160ka),both inEthiopia,aremorphologically diverse[1,16].Thisdiversityhasledsome

researcherstoproposethatfossilssuchasJebelIrhoudandFlorisbadactuallyrepresenta

moreprimitivespecies called‘H.helmei’, usingthe binomen given to theFlorisbad partial

craniumin1935[17,18].Inasimilarvein,thefossilcraniafromHerto[19],whichcombinea

relativelyglobular braincase witha robust occipitaland largeface, were described as the

subspeciesH.sapiensidaltubecausetheyfalloutsidethevariationofrecenthumans.

However,weviewH.sapiensas anevolvinglineagewithdeep Africanroots,andtherefore

preferto recognizesuchfossils aspart ofthediversityshown byearlymembersoftheH.

sapiensclade.Thefullsuiteofcranialfeaturescharacterizingcontemporaryhumansdoesnot

appearuntilfairlyrecently,betweenabout100–40ka[20].Thecharacterandchronologyof

earlyH.sapiensfossils,togetherwiththeirgeographicdistributionacrossAfrica,suggeststhat

evolutionmayattimeshaveprogressedindependentlyindifferentregions,inpopulationsthat

wereoftensemi-isolatedformillenniabydistanceand/orecologicalbarriers,suchashyperarid

regionsortropicalforests.

1 cm

Figure1.EvolutionaryChangesofBraincaseShapefromanElongatedtoaGlobularShape.Thelatterevolves withintheH.sapienslineageviaanexpansionofthecerebellumandbulgingoftheparietal.(Left)Micro-computerized tomographyscanofJebelIrhoud1(300ka,NorthAfrica).(Right)Qafzeh9(95ka,theLevant).

FurtherinsightsintothegeographicextentandpotentialhabitatdiversityofearlyH.sapiens

populationscanbegainedfrommorerecentforagerpopulationsinAfrica,whichwerealso

stronglystructured.Forexample,LaterStoneAge(LSA)humanremainshighlightboththe

retentionof‘archaic’traitsandthemaintenanceofconsiderablemorphologicaldiversityintothe

terminalPleistocene[11,21].IntheHolocene,theskeletalrecordbecomesmuchricher,but

thereremainsconsiderablespatialvariationinmorphology.Variationbetweenpopulationsin

differentregionsandenvironmentsofAfricamayhavebeenshapedbyisolation-by-distance

andlocal environmentaladaptations[22–26]. Forexample,challengingenvironments(e.g.,

deserts,rainforest)andisolationhavelikelyplayedasignificantroleinshapingthepopulation

structureofHoloceneAfricanforagersandisolatedhunter-gatherersacrossthetropics[25,27].

23

DepartmentofAnthropology,Emory University,1557DickeyDrive,Atlanta, GA30322,USA

24

LaboratoireÉvolution&Diversité Biologique(EDBUMR5174), UniversitédeToulouseMidi-Pyrénées, CNRS,IRD,UPS.118routede Narbonne,Bat4R1,31062Toulouse cedex9,France

25

InstitutoGulbenkiandeCiência, P-2780-156,Oeiras,Portugal *Correspondence: eleanor.scerri@rlaha.ox.ac.uk (EleanorM.L.Scerri). (A) (X) (W) (Y) (Z) (V) (L) (M) (N) (O) (P) (Q) (U) (T) (S) (R) (B) (K) (C) (E) (D) (F) (G) (H) (I) (j) 1 cm (Aa) (Ac) (Ab)

Figure2.MiddleStoneAgeCulturalArtefacts.(A–D)BifacialfoliatesfromnorthernAfrica(A,MugharetelAliya;B–D,AdrarBous).(E–G)Bifacialfoliatesfrom southernAfrica(BlombosCave).(H,I)TangedtoolsfromnorthernAfrica.(J)SegmentedpiecebearingmasticresiduefromsouthernAfrica(Sibudu).(K)Engravedochre fragment(BlombosCave).(L–N)EngravedostricheggshellfragmentsfromsouthernAfrica(Diepkloof).(O,P)BonepointsfromsouthernAfrica(SibuduandBlombos Cave,respectively).(Q)BonepointfromnorthernAfrica(ElMnasra).(R–V)PerforatedTriviagibbosulashellsfromnorthernAfrica(R,S,GrottedePigeons;T–V,Rhafas, Ifrin’Ammar,andOuedDjebbana,respectively).(W–Aa)PerforatedNassariuskraussianusshellsfromBlombosCave.(Ab)Conusebraeusshellbead(Conus2)from southernAfrica(BorderCave).(Ac)OchrefragmentshapedbygrindingfromsouthernAfrica(BlombosCave).Allscalesare1cm.Boxeditemsindicaterescaled artefacts.Imagesreproduced,withpermission,from(A–D,H,I)TheStoneAgeInstitute;(E–G,J–P,Ac)from[35];(Q)from[47];and(R–Ab)from[35,47,48].

Glossary

Allele-frequencyspectrum(AFS): alsoknownasorsite-frequency spectrum(SFS),AFSisahistogram representingthefrequenciesofthe allelesfrommultipleloci(e.g.,SNPs). Assumesthatlociarebiallelic,andis usedasasummaryofgenomicdata fordemographicinference. Archaichominin:umbrellatermfor anyofabroadgroupofnon-Homo sapienshumans,suchasthe NeanderthalsorHomo

heidelbergensis(seebelow).Archaic featureswithinourspeciesrefersto theretentionofparticulartraits typicallyassociatedwitharchaic hominins,suchasanelongated (versusamodernglobular) braincase.

Core-and-flaketechnology:stone tooltechnologyfocusedonthe removalofflakesasdesired productsfromablockofraw material,whichisultimately discardedaswaste.Thisstandsin contrasttotechnologyinvolvingthe shapingofrawmaterialintoa product(e.g.,ahandaxe),wherethe shapingflakesarediscardedas waste.

Effectivepopulationsize(Ne):a measureofgeneticdrift,and indirectlyofsomemeasureof populationgeneticdiversity.Ne representsthesizeoftheideal populationthatwouldhavethesame driftpropertiesastherealpopulation. Dependingonthepropertiesofthe geneticdatainwhichweare interested,differenteffectivesizes maybedefined.Inanideal population,thedifferentNevalues shouldbethesame,butinreal populationsthismaynotbethe case.Necanbeseenasthenumber ofindividualsactuallycontributingto thenextgeneration,asopposedto thetotalnumberofindividualsina population(whichisusuallymuch larger).

Hafting:theprocessofattachinga stoneorabonetooltoahaft, typicallybutnotalwaysconstructed fromwood,eitherthroughadhesives (gum,resin),bindings,orboth. Holocene:therecentgeological epochwhichbeganataround 11.7kaandwhichisassociated withthecurrentwarmperiod. Homoheidelbergensis:originally namedfortheMauermandiblein

Ultimately, the processes underlying the emergence of any ‘package’ of derived features

diagnosticofearlyH.sapiensanatomyremainincompletelyunderstood.However,thedata

do not seem to be consistent with the long-held view that human ancestry is derived

predominantlyfromasingleAfricanregionhostingapanmicticpopulation.Instead,H.sapiens

likelydescendedfromashiftingstructuredpopulation(i.e.,asetofinterlinkedgroupswhose

connectivity changed throughtime), each exhibiting differentcharacteristics of anatomical

‘modernity’.Thediscoverythattheprimitive-lookingH.naledidatestobetween335kaand

236ka[28],andthattheBrokenHill1Homoheidelbergensisskullmaydateto300–125ka

[29],alsoshowsthatotherhomininspeciesinAfricacoexistedwithH.sapiens,raisingthe

possibilityofAfricanarchaicinterbreeding.Futureresearchshouldattempttodeterminewhich

featuresevolvedbeforetheappearanceofourspeciesandwhichprimarilydevelopedwithin

theevolutionaryhistoryofourspecies.Anotherkeyareaconcernsunderstandingtheextentto

whichdifferentprocessesshapedobservedchanges.Forexample,thenarrowingofthepelvis

mayreflectdifferentprocessesincludingneutralgeneticdrift,adaptationtoecologicalvariation,

andlife-historyvariation.

APan-AfricanCulturalPatchwork

AcrossAfrica,thevirtualabandonmentofhandheldlargecuttingtoolssuchashandaxes,

andanincreasedemphasisonpreparedcoretechnologiesandhafting,markedaprofound

technologicalreconfigurationofhomininmaterialculture.Thesetechnologicalchanges,which

definethetransitiontotheMiddleStoneAge(MSA),seemtohaveoccurredacrossAfricaata

broadlysimilartime;forexampleat300kabothatJebelIrhoud,wheretheyarefoundwith

earlyH.sapiensfossils[16],andatOlorgesailieinEastAfrica[30],andat280kainsouthern

AfricaatFlorisbad[31].Currently,theearliestdatesinWestAfricaareyounger,at180ka,but

theregion remainsverypoorlycharacterized[32].TheMSA isassociatedwithH. sapiens

fossils,but both H. nalediand H.heidelbergensis probablypersisted intothe late Middle

Pleistocene.

Clearregionallydistinctivematerialculturestyles,typicallyinvolvingcomplexstonetools,first

emergedwithin theMSA.Forexample,theCentral AfricanMSA includesheavy-dutyaxes,

bifaciallanceolates,backedflakesandblades,picksandsegments,probablyfromatleastthe

lateMiddlePleistocene[33].IntheLatePleistocene,grasslandandsavannahexpansionin

NorthAfricaledtodensehumanoccupationassociatedwithspecificregionaltechnological

featuressuchastangedimplements(Figure2)[34].Atapproximatelythesametimethere

wasanemergenceofcomparablydistinctiveindustriesinpartsofsouthernAfrica.AsinNorth

Africa,someoftheseindustriesarealsoassociatedwithotheraspectsofcomplexmaterial

culturesuchasochre,bonetools,shellbeads,andabstractengravings(Figure2)[35].

Suchregionalizationistypicallylinkedwiththeemergenceof‘modern’cognition.However,it

arguablyalsoreflectstheinteractionbetweendemographicvariables(e.g.,increased

popula-tiondensity)[36–38]andthelearnedtraditionsoflong-livedregionalsubpopulationsordemes

(Figure2).Forexample,northernandsouthernAfrica,apartfrombeinggeographicallydistant,

were also separated by environmental factors as a consequence of the expansion and

contractionofforestsinequatorialAfrica, synchronouswithameliorationinnorthernAfrica.

Otherfactors,suchashabitatvariabilityandadaptationtolocalenvironmentalconditions,are

alsolikelytoplaysomeroleinmaterialculturediversification.

Althoughgeographicaldifferencesareclearatthecontinentalscale,localizedspatialpatterning

isharder to discern. Similaritiesbetweenregions may have been producedby occasional

example,althoughthereiscertainlysomevariation,thereappearstobeunderlyingcontinuityin

material culture throughoutmuchof the MSA (e.g.,[39]). Inmany regions, ‘generic’MSA

assemblagesthat do notcarryan obvioussignal of regionalizationare common[40]. Ina

cognitivemodel,thesedifferencessuggestthatnotalltheseearlypopulationsmanifesteda

‘modernmind’.However,suchassemblagesareaugmentedbyshiftingfrequenciesoftool

typesthatappeartobespatiallyortemporallyindicative,andlikelyreflectdemographicfactors.

In someparts ofAfrica, the full suiteof generalized MSA characteristics continues largely

unchangeduntilthe Pleistocene/Holoceneboundary[41],matchingthemorphological

pat-terns,andsuggestingthattheendoftheMSAmayhavebeenasstructuredandmosaic-likeas

itsbeginnings.ThisviewhassupportfromLSAmaterialculture.Despitesuperficialsimilaritiesin

LSAlithicminiaturization,theculturalrecordshowscontinueddifferentiationandderivationinto

theHolocene,supportingthebiologicalevidenceforvariablepopulationdynamicsthatdidnot

resultinwide-scalehomogenization[42].

Thereasonsfor,andthereforeimplicationsof,thegeographicandtemporalstructuringofMSA

culturaldiversityarestillpoorlycharacterizedandlikelyreflectseveralprocesses.Theseinclude

adaptationstodifferentenvironments[43].Long-term,large-scalepopulationseparationmay

alsohavebeenthenormformuchofPleistoceneAfrica(Box1;i.e.,isolationbydistanceand

isolationbyhabitat,representingnullmodelstoberejected).Rareandspatiallyexplicitmodels

exploring Pleistocene technological innovations have also linked cultural complexity with

variation in regional patterns of population growth, mobility, and connectedness (e.g.,

[36,44,45]),supportedbyevidenceoflong-distancetransferofstonerawmaterial(e.g.,[46]).

Majornewarchaeologicalresearchdirectionsshouldinclude:(i)unravelingthe relative

con-tributionsof differentAfricanregions/habitatsto recent human evolution; (ii)understanding

shiftingpatternsofpopulationstructurethroughthedifferentialappearance,expansion,

con-traction,anddisappearanceofregionallydistinctartefactforms(Box1);and(iii)exploitingthe

growinginterface betweenarchaeology,ecology,morphology,andgeneticsto explorethe

1908.Someresearchers(e.g.,[15]) havearguedthatthisspecieswas widespreadinEurasiaandAfrica duringtheMiddlePleistocene. Othersprefertodistinguishthe AfricansamplesasH.rhodesiensis, basedontheBrokenHillcranium foundin1921.

Instantaneousinverse

coalescencerate(IICR):theIICRis atime-andsample-dependent parameter.Inapanmicticpopulation, theIICRisproportionaltoNe.In structuredpopulations,theIICRcan bestronglydisconnectedfrom changesinNe.

Intertropicalconvergencezone (ITCZ):azoneneartheequator wherethenorthernandsouthernair massesconverge,typicallyproducing lowatmosphericpressureand considerableconvectiverainfall. Largecuttingtools:blocksof stonethatwereshapedintolarge handheldtoolsforcuttingfunctions, suchasstoneaxes.Theflakes chippedoffthestoneblockare referredtoasthinningflakesand weretypicallywasteproducts. LastInterglacial:theprevious interglacialtothecurrentone;this beganat125kaandendedat 109ka.Interglacialsarewarm periodscharacterizedbyrecedingice sheetsinthehigherlatitudesand increasedhumidityinthemid-latitude aridbelt.

LatePleistocene:thefinalpartof thePleistocenegeologicalepoch, beginningwiththeLastInterglacial at125kaandlastinguntilthe beginningoftheHoloceneat 11.7ka.

LaterStoneAge(LSA):a cultural-technologicalphaseinAfricadating broadlyfrom60kato5ka.While highlyvariableandpoorlydefined, theLSAischaracterizedbyafocus ontheproductionofsmalltools, suchasbladesandbladelets,and geometricmicroliths.

MiddlePleistocene:themiddlepart ofthePleistocenegeologicalepoch, beginningat781kaandending withthebeginningoftheLast Interglacialat125kaago.The MiddlePleistoceneisassociatedwith theemergenceofHomosapiensand Homoneanderthalensisat>300ka. MiddleStoneAge(MSA):a cultural-technologicalperiodinAfrica characterizedbythewidespreaduse Box1.IsolationbyDistance(IBD)

IBDistheexpectationthatgeneticdifferencescorrelatepositivelygeographicdistancesasaconsequenceofthefact thatmatingismorelikelytooccuratshorterthanlongerdistances.Thisconcept,althoughwellestablishedingenetics, israrelyappliedtoPleistocenearchaeologicalandhumanfossilmaterial,despiteitspotentialvalueasanullmodelfor observedculturalormorphologicaldifferencesbetweenmaterialsfromdifferentsites[49].

Becausearchaeologicalproblemsareconcernedwithidentifyingtheprocessesthatgenerateobservedpatternsof culturalvariation overtimeandspace, thelackofequivalent nullmodelsisparticularlyproblematic.Processes generatingculturalvariationconstituteacomplexbalancebetweenpatternsofinheritedknowledge,localinnovation, modesofculturaltransmission,localadaptation,andshiftingpopulationdynamics(e.g.,populationsize,density,or mobility[36]).Withoutnullmodelsof‘culturalsimilarity’asabaseline,itisdifficulttoescapesimplistic,narrative inferencesaboutthepast.Similarly,humanfossildatacanbeinterpretedinseveralwaysdependingonthetaxonomy employed,butspatialvariationislikelytorelatetothesamefactorsthatinfluencegeneticsimilaritiesbetweenregional populations[50].

Inanarcheologicalcontext,theexpectationofanIBDmodelisthatculturalsimilaritywilldecreasewithdistance,witha degreeofspatialautocorrelation(e.g.,[51]).Thisexpectationrepresentsthesimplestexplanationoftheobserved variation.Ifthisnullmodeldoesnotprovideanadequateexplanationofthedata,morecomplexmodelscanbeinvoked toexplainpatternsobservedeitherintheresidualsfromthenullmodelorintherawdataasawhole.Forexample,a morecomplex population structurecan be theoreticallydifferentiated fromanIBD modelifpatterns ofspatial autocorrelationarediscreteratherthancontinuous(FigureI),pointingtowardstheformationofdistinctbiologicalor culturalclusterswhichmaycorrelatewithotherfeatures(e.g.,genetic,morphological,orenvironmental).Manyfactors couldpromotetheformationofsuchclusters,includingassortativitybyculturalsimilarity,orconformitytolocalnormsof, forexample,toolproduction.

ofcore-and-flaketechnologies, whichwereoftenhafted,ataround 300ka.TheMSAgavewaytothe LSAoveraprotractedperiodbroadly between60kaand20kawhich featuredthereplacementofclassic core-and-flaketechnologieswith smallandoftengeometricmicrolithic tools.TheMSAisingeneralsimilar tothecontemporaneousMiddle PaleolithicofEurasia.

Milankovitchforcing:theeffecton climateofslowchangesinthetiltof theEarth’saxisandshapeofitsorbit thatchangetheamountand distributionofsunlightreachingthe Earth.

PairwisesequentiallyMarkovian coalescent(PSMC):amethod(and associatedprogram)producinga plotshowingchangesinNefroma singlediploid(ortwohaploid) genome(s)[16].ThePSMCactually estimatestheIICRandhasbeen usedonmanyspecies. Panmixia:randompatternsof matingwithinapopulation. Precession:climaticallyrelevant changeoftheEarth’srotationwitha periodof26000years.In

combinationwiththeslowrotationof Earth’sellipticalorbitaroundtheSun, themainsolarincomingradiation changesvarywithaperiodicityof 21000years.Theeffectof precessionontheclimatesystem occurspreferentiallyforlargeelliptic orbits.

Preparedcoretechnology:aform ofcore-and-flaketechnology wherethecoreisshapedinsuchas awayastopredeterminetheshape ofsubsequentflakeremovals.Itwas thedominanttechnologyoftheMSA. Themosticonicformofprepared coretechnologyisLevallois technology.

Refugia:regionsorareasthat remainconsistentlyhabitablebya speciesorassociationofspecies throughanentireglacialand interglacialclimaticcycle. Tangedimplements:stonetools characterizedbyastemoratangat thebaseofthetool,whichisthought tobeinsertedintothesocketofa woodenhaft.Thiswouldallowstone spearpointstobeattachedto woodenshafts,forexample. UpperPaleolithic:a cultural-technologicalperiodinEurasia between45kaand10kathatis

extenttowhichmaterialculturepatterningiscoupledordecoupledfromtheseassociated(but

potentiallyindependent)axes.

WhyGenetic ModelsMustIncorporateaMoreComplexViewofAncient

MigrationandDivergenceinAfrica

Thestartingpointformostgeneticstudiesofhumanoriginshasbeentoinvestigatethedepthof

present-daydiversitybetweenandwithinAfricanpopulations.Moststudieshaveusedsimple

‘tree-like’demographicmodelstoinferpopulationsplittimes,neglectingorsimplifying

popu-lationstructure,evenifsometimesconsideringadegreeofgeneflowbetweenbranches(Box

2).Suchstudieshaveproducedavarietyofsplit-timeestimates,withtheKhoeSanpopulations

ofsouthernAfrica,whoretainthegreatestlevelsofgeneticdiversityamonghumanpopulations

today,comprising onebranch ofthe deepestdivergence inferred, at150–300ka [52–58].

Someauthorshaveinterpretedthis,inconjunctionwithagradientofsouthtonorthdecreasing

geneticdiversitywithinAfrica,asfavoringasingle-originmodelformodernhumanswithalocus

insouthernAfricaratherthanineasternAfrica[59,60].Variationininferredsplittimesreflectsa

varietyofdifferentmethodologies,modelassumptions,anddatasources,withageneraltrend

formorerecentanalysestoinferolderdates.Inadditiontoancientgeneflowandstructure,

morerecentpopulationmovementswithinAfrica,suchastheexpansionofBantu-speaking

peoplesfromWestAfricaat2–1.5ka[52,61],willhaveobscuredsignaturesofolder

demo-graphic processes, as will have episodes of ‘back-to-Africa’ migration from Europe and

southwestAsiaintoseveralregionsofthecontinent[60,62–65].

Modelsincorporatingmorecomplexpopulationstructurecanbeconsiderablymore

parame-ter-rich and therefore more difficult to test computationally, particularly with limited data.

However,theydoofferamoregeneralizedandflexibleviewofpastdemography–onethat

canaccommodate,butnotbelimitedto,moretraditionalpopulationtreemodels.Furthermore,

theincreasedavailabilityofgenomicdataanddevelopmentsinanalyticalmethodologiesnow

High High Similarity Distance Isolaon by distance Structured populaon Low Low

FigureI.SimpleIBDModelwithCulturalData.Notethatsimilaritycanincreasewithdistanceundersome circumstances,forexamplewhensimilarhabitatsareseparatedbyconsiderabledistances,withareasofdifferent habitattypesbeinglocatedbetweenthem.

permitinferenceundermorecomplexandrealisticmodels.Thesedevelopmentshaveshown

thatstructurecannotbeneglected,andcancausepatternsingeneticdatathataresimilarto

thosegeneratedbyotherformsofdemographicchange(e.g.,[66,67]).Forexample,inferred

changesineffectivepopulationsize(Ne)mayresultfromchangesinconnectivitybetween

ancientpopulationsratherthanfrom,orinadditionto,changesincensuspopulationsize[7,68].

Indeed,therelationshipbetweeninferredNeandcensuspopulationsizeisnotstraightforward,

andmayevenbecounterintuitivewhenstructureexists[7,66,68].Thegeographicalscaleat

whichpopulationgeneticstructuremayhaveexistedisalsodifficulttoinfer.Forexample,one

recentgenomicstudyshowedsubstantialstructurebetweenpre-agriculturalhuman

popula-tionsseparatedbyonlytensorhundredsofkilometers[69].Theseinsightschallengetheview

thattheearlyprehistoryofourspeciescanbewellapproximatedbypopulationgrowthwithina

singlelineage[70].

Althoughmodern genomicdatahave beenshaped by,and thuscontainlarge amountsof

informationon,pastdemography,thesedatacanbeexplainedbymanydifferentmodelsof

populationhistory(equifinality). Moreover,allsuchmodelsare necessarilyabstractions and

simplificationsofthetruepopulationhistories,andthediscrepanciesinvolvedmaybe

particu-larly problematic for certain questions about the past (mis-specification). Thismeans that

structure can be difficult to unambiguously detect, and even harder to reconstruct. For

example,severalstudiesonAfricanpopulationshaveidentifiedgeneswithcoalescencetimes

generallycharacterizedbyan emphasisonbladeandbone technology,caveart,carvings,varied personalornaments,andelaborate burials.InEuropeitistypically regardedasamarkerofHomo sapiens.

Box2.ModelingPopulationStructure

Populationgeneticmodelingfordemographicinferenceoftenassumespanmixia,whereinallindividualsinapopulation haveanequalchanceofmatingwithoneanother.Insuchcasesthereisoftenanimplicitassumptionthatpanmixia occursatthewhole-specieslevel.However,realpopulationsrarelymeetthiscondition,owingtotheexistenceofspatial structureatthespecieslevelorotherstratificationofindividualswithinthepopulation.Populationstructureandits consequencesforgeneticdatacanbemodeledinvariousways.Forexample,Wright’sn-islandmodelassumesthat populationsaresubdividedintondifferentislands/demesthatareconnectedthroughgeneflow.Thissimplemodel assumesthatalldemesarepanmictic,havethesamesize,andexchangegeneswithallotherislandsatthesamerate. Othermodelsincludetreemodelsinwhichanancestralpopulationsplitsintotwoormorepopulationsthatmay themselveslatersplit.Then-islandmodelignoresspace(i.e.,differinglevelsofconnectivitybetweenpopulations), whereasintreemodelsgeographiclocationmaybeimplicitbutisnotexplicitlymodeled.Forexample,twopopulations thataregeographicallyclosemaybeassumedtoshareamorerecentsplittingeventthanpopulationsthataremore distant.Othermodels(e.g.,steppingstone)mayincorporategeographicspaceexplicitlybyconnectingdemesviagene flowonlywiththeirspatialneighbors.

Anotherdistinctionamongmodeltypesiswhethertheyincorporatechangeovertime.Thestepping-stoneandn-island modelshavenotemporalaspect.Conversely,treemodelsmaygenerateverydifferentresultsdependingonthetiming ofsampling inrelationtothesplitting eventsandgeneflowbetweenpopulations.Morecomplex modelsallow demographicexpansionsorcontractionsinspace,oftenbasedonsimulations[71,72].Finally,theclassof ‘meta-populationmodels’includedemesofvariablesizesthatcanbeconnectedbygeneflowandcolonizationevents.The populationineachdemecanalsobecomeextinctandberecolonizedbyindividualscomingfromoneorseveralother populations.

Thisdiversityinrangeofstructuredpopulationdemographicmodels,withvaryinglevelsofcomplexity,leadstosome arbitrarinessinwhichmodelsarechosen.Becauseweknowthatthehumanpastwascomplex,itisoftenassumedthat morecomplexmodelsofthatpastaremorerealistic.However,morecomplexitymeansmoreparametersandmore waysforamodeltodifferfromreality.Thismeansthatunlessinformedaprioribysecureinformation,orfittedto substantialquantitiesofconditioningdata,morecomplexmodelscanbemorewrong,notmorerealistic.Thepasttwo decadeshavealsoseenthedevelopmentofmanydifferentinferencemethodologies,theresultsofwhichareoften difficulttocompare.Thisisbecausetheyoftenmakedifferentassumptions(treesplittingversusspatialdistribution), explaindifferentaspectsofthedata(allele-frequencyspectrum,AFS;versusIICR),andcanbecomputationally demanding–challenginginterpretation,explanatorypower,andvalidation,respectively.Modelsarevaluabletoolsfor understandingandinterpretingdata,butweshouldnotbesurprisedifasinglefamilyofmodelsisunabletoexplainall patternsofhumangeneticdiversity.

ontheorderof1millionyears,whichcouldbeinterpretedasindicatingadmixturewitharchaic

hominins[9,10,73].However,even inasinglepopulationsomeveryoldcoalescencetimes

(>1My)areexpectedforhumans(Figure3),andthereforeinferencesbasedonthetailofthe

distributionofcoalescencetimes,whichareparticularlysensitivetomodelmis-specification,

needtobeinterpretedwithcaution.Indeed,severalauthorshavearguedthatdeep

coales-cencetimesarecompatiblewithasinglehumanlineageinAfricawithdeeppopulationstructure

[7,68,74].

AncientDNA(aDNA)datacanprovideadditionalresolution,andstudiesonHolocene

individu-alsrecentlyrevealedextensivestructureandmigratoryactivityduringthatperiod[8,75].Ancient

Pleistocene-agedaDNAwouldbemoreinformative,butisdifficulttoobtainbecausetropical

(A) (B) (C) (D) Single panmicc populaon Typical coalescent tree Inferred populaon size changes (e.g., IICR, PSMC) Structured populaon Past Present Past Past Present Present Ne Ne Ne Ne Ne Ne Or Or M M M M M M M N N N N N N

Figure3.InferringPopulationSizeChangeinUnstructuredandStructuredPopulations

ForaFigure360authorpresentationofFigure3,seethefigurelegendathttps://doi.org/10.1016/j.tree.2018.05.005 Theprobability,orexpectedrate,ofcoalescenceoflineagesinasinglepanmicticpopulationisinverselyproportionaltothe populationsizeatthetime.Differentpanmicticpopulationsizehistories(A)thereforeshapethetemporaldistributionof coalescentevents(B).Whenestimatedformanyregionsofthegenome,thetemporaldistributionofthesenodescanbe usedtoestimatetheinstantaneousinversecoalescencerate(IICR),whichinasinglepanmicticpopulationisadirect proxyforthepopulationsize(C).SoftwaresuchasthepairwisesequentiallyMarkoviancoalescent(PSMC)orthe multiplesequentiallyMarkoviancoalescent(MSMC)canbeusedtoestimatetheIICR/populationsizechangeinthepast. However,whendataaresampledfromastructuredmeta-populationconsistingofsubpopulationsconnectedbymigration (D),changesinmigrationthroughtime,and/orinsampling,cangenerateanyIICR-inferredpopulationsizehistorywithout anyactualchangeinthemeta-populationsize(Ne).

environmentsaremostlyunfavorableforDNApreservation.However,arecentstudyshowed

that Late PleistoceneaDNA can be retrievedin some African regions [65]. These studies

demonstrate that inferences from patterns of human genomic diversity need to consider

fluctuatingpopulationstructureoverlongperiods,inadditiontotherangeofpanmicticAfrican

populationoriginmodels.

Environmentaland EcologicalDriversofPopulation Structure

Thegenetic,fossil,andarchaeologicaldatadiscussedaboveindicatethatH.sapiensevolvedin

highlystructuredpopulations,probablyacrossmanyregionsofAfrica.Elucidatingthedegree

ofandmechanismsunderlyingpopulationstructurewill requireconsiderationofMiddleand

LatePleistoceneenvironmentalvariabilityinbothspaceandtime(e.g.,[13])(Figure4).Refugia

havebeenhighlightedaskeycatalystsofevolutionarychange[76],andcertainlywouldhave

generated population structure. Nevertheless, some regions acting as ‘backwaters’ and

isolatedhabitat islandsmayalsohave beencentralinthepersistenceofrelictpopulations.

Researchhasemphasizedbroad asynchronous environmentalchangesin differentAfrican

regions (e.g., [13,77]). The northernand southern tips of the continentare most strongly

affectedbywinter westerly precipitation, variation inwhich islargely drivenby changes in

AtlanticOceancirculation.However,mostofAfricaexperiencesmonsoonalrainfallassociated

withtheintertropicalconvergencezone(ITCZ),thestrengthandlocationofwhichvaries

according to changes in insolation that are driven primarily by precessional aspects of

Milankovitchforcing.Consequently,partsoftropicalAfricathatarecurrentlyhumidlikely

experiencednumerousepisodesofextremearidityinthepast[78,79].Atthesametimethatthe

monsoonmigrated northwards, the Sahara contracted, and networks of lakes and rivers

expandedacrossmuchofnorthAfrica[80–82],withmatchingconditionsinpartsofsouthwest

Archaeological sites Fossil sites Ag e of f o ssils (k a) 310 300 290 280 270 260 250 240 230 220 210 200 190 180 170 160 500 400 300 200 100 0 500 400 300 200 100 0 500 400 300 200 100 0 500 400 300 200 100 0 20 0 −20 40 20 0 −20 400 200 0 400 200 0

Regional percipitaon changes (% of mean)

Time (ka)

Figure4.MiddleandLatePleistoceneAfricanEnvironmentalVariabilityinSpaceandTime.(Left)MapofAfricawithkeyarchaeologicalandfossilsites discussedinthetext.Coloredboxesindicateaveragedregionsforsimulatedprecipitationchangesfromthetransientglacial/interglacialLOVECLIMclimatemodel experiment[81].(Right)Precipitationchanges(%)relativetothelong-term784thousandyearmeaninthekeyregionshighlightedinleftpanel,assimulatedbytransient 784thousandyear-longLOVECLIMclimatemodelsimulation[81].FromtoptobottomtheregionsareeasternequatorialAfrica,southernAfrica,northwesternAfrica, andthecentralSahararegion.

Asia.Finer-scaleshiftsinthemonsoonarealsoevident.Forexample,inWestAfricatheextent

ofsavannahandforestedareasisstronglyaffectedbysmallchanges inpatternsofrainfall

[83,84].

Climatethereforevariedgreatly,andperiodsofrelativelyincreasedaridityorhumiditywere

asynchronousacross Africa. Crucially,these factorsaremajor drivers of faunal population

structure and speciation [85,86], illustrated by numerous sub-Saharan animals exhibiting

similarphylogenetic patternsintheirdistribution. Forexample,Bertola andcolleagues[87]

showthatdozensofspeciesexhibitdistinctpopulationsinthetwomajorevolutionaryrealmsof

west/centralAfricaandeast/southernAfrica.Manyalsoshowafurthersubdivisionbetween

east Africaandsouthern Africa, signifyingimportant refugesin thesethree regions.These

speciesoccupyarangeoftrophiclevels,suggestingthatclimateaffectedwholeecological

communities.

Therefore,faunalspeciationlargelyappearstohavebeencatalyzedbyclimate-drivenhabitat

fragmentationandinteractionbetweendifferentbiomesovertime.Thisprovidesinsightsinto

howhumanpopulationstructurecouldhavebeenmaintainedoversignificanttimescalesand

geographicareasofAfrica.InAfrica,theconceptof‘refugiumnetworks’hasbeenspecifically

implicatedinPleistocenehumanpopulationsubdivisionsandexpansions[18],andasaresult

suchregionsareofmajorevolutionaryinterest.Althoughfragmentationofsuitablehabitathas

beenhighlightedasamajordriverofpopulationstructureoverandaboveisolation-by-distance

(Box1),isolation-by-habitatcanalsoplayanimportantroleinanimal[84]andprobablyalso

humanpopulationstructure[14,88].

Majorchallengesremaininintegratingfossil,archaeological,andgeneticlinesofevidenceinto

paleoenvironmentalandpaleoecologicalcontexts(butsee[3]and[72]fordiverseattemptsto

doso). Currently,the chronology ofmuchof thepaleoanthropological recordremains too

coarsetoallowanyfirmconclusionstobedrawnabout theroleofenvironmentalchanges.

Promisingnewavenuesofresearchincludegenomicanalysesoffauna,includingtheidenti

fi-cationofcommensalspeciesandreconstructionsofhumanhabitatsthroughstable-isotope

analyses.

ConcludingRemarks:MovingForwards

Availablemorphological, archaeological,genetic,andpaleoenvironmental dataindicatethat

thesubdivisionofMiddleandLatePleistoceneAfricanhumanpopulationsdrovethe

mosaic-likeemergenceandevolutionofderivedH.sapiensmorphology.Reproductivelysemi-isolated

populationsadapted tolocal ecologiesalongside drift.Suchpopulationisolationwas likely

facilitatedby small population sizes. Thus, as with other fauna, gene flow should not be

assumedtohavebeenconstantthroughtime,orto haveoccurredatthesameratewithin

andbetweendifferentregions.AcrossthelargetimescalesoftheMiddleandLatePleistocene,

withtheir strong climatic fluctuations, the number of intermediate populations connecting

differentregionsisalsolikelytohavefluctuatedconsiderably.

Severalmajorunansweredquestionsflowfromthisreorientationofrecenthumanorigins(see

OutstandingQuestions).Didkeydiagnosticmorphologicalcharacteristicsemergeinoneregion

andbecome elaboratedwithsubsequentdispersals?Ordidthetransitionfrom‘archaic’to

‘modern’–whetherindicatedbymorphologyormaterialculture–occurgradually,andina

mosaic-likefashionacrossthecontinent?Ifthiswasthecase,didAfricanarchaichybridization

alsoplayarole?Howdoestheexistingevidenceforstructureaffectourunderstandingofthe

historyofpopulationsizechangesanddispersals?Similarly,wehavenofirm grasponthe

OutstandingQuestions Intheconventionalview,H.sapiens emergedinoneregionand/or popula-tionofAfrica.Instead,newdata sug-gestthatavarietyoftransitionalhuman groups,withamosaicofprimitiveand derivedfeatures,mayhavelivedover an extensivearea fromMorocco to South Africa between >300ka and 12ka.

Threeoutstandingquestionsemerge fromthisview.First,withintheAfrican ‘multiregional’ paradigm,which spe-ciesbestfitsastheancestor(s)ofH. sapiens?Manyaspectsofthedelicate H.sapiens facialshapemaynotbe derivedbutinsteadbeprimitive reten-tionsfromanancestorwitha general-izedfacialshape.Itthereforeseems possiblethatH.sapiensdidnotevolve fromtheAfricanformsofH. heidelber-gensis(as represented,e.g.,by the BodoskullfromEthiopia,andBroken Hill fromZambia), butfroma more primitive H. antecessor or H. erec-tus-like ancestor, beginning at 0.5Ma[1,2].However,hybridization duringtheinceptionofthisprocessis alsoapossibility.Resolvingthe speci-ationofH.sapiensandthecharacterof ancestral populations represents a crucialfirststepinunderstandingthe emergenceofthemorphological fea-turesthatdiagnoseourspeciesduring thelaterMiddlePleistocene.

Second,howmanypopulations, envi-ronments,andgeographicalareasof AfricaplayedaroleintheoriginsofH. sapiens?Didadjoiningareasof west-ern Asiaalsoplay a part?It seems possible thatearly humansfollowed thesameecologicalpartitioningand subspeciationpatternsthatareseen among continentally distributed Afri-can mammals, many of which emerged at the same time as the genusHomo.TheSaharamayhave playedaparticularlyimportantrolein this respect. Other areas, such as regionsofforest,mayalsohave sup-ported populations who remained semi-isolatedfromthoseingrasslands andsavannahs.Addressingthe chal-lengesofresearchindesertsand rain-forestswillbedifficult,butislikelytobe rewarding.

Finally,weresomeofouranatomical traitsinheritedfromtransitionalAfrican

concordancethatmightexistbetweenmorphologicalandculturalstructuring.Regionalcultural

signaturesareapparent,raisingthepossibilitythatspatiallydistinctformsofmaterialculture

reflectsimilarpatternsofpopulationisolationandaggregation.Fillingintheseknowledgegaps

requiresustoreconsiderpaleoanthropologicalspeciesconceptswhicharechallengedbythe

viewofdeeppopulationstructurewithsporadicgeneflow/admixture.

Ultimately,reconstructingthedemographichistoryofhumanpopulationsinitsfullcomplexityis

beyondthepowerofpopulationgenomicsalone,necessitatinganinterdisciplinaryapproach.In

thepastthishasbeenachievedbygeneticistsworkingwitharchaeologistsand

paleoanthro-pologiststo define anarrowset ofsimplifiedhypotheseswhosegeneticoutcomescan be

comparedtoidentifythemodelsthatbestexplainthedata.Whilesuchanapproachhasmet

withconsiderablesuccess,amorecompletepicturewillrequireintegratingdifferentdatatypes

(genetic,fossil,material culture,paleoclimate andpaleoecological data) usingthe sameor

analogousmodelsofpopulationstructure,sizechange,anddispersal.Thisrepresentsamajor

challengeforancestraldemographicinferenceoverthecomingyears.

Fullycharacterizingthenatureofthisapparent‘Africanmultiregionalism’alsorequiresrejecting

numerouslongstanding,ifimplicit,assumptions,andformulatingnewquestions.Forexample,

thechronologicallagbetweengeneticestimatesofpopulationdivergencetimesand

morpho-logicalchangesinthefossilrecordisnotwellunderstood,andshouldnotbeassumedtobe

short– particularlybecause inferencesfrom geneticdataare profoundly influenced bythe

modelsorfamiliesofmodelsused.Forinstance,theestimatesofpopulationsplittimesthatare

sometimespublishedmaybecomelessappropriateorrelevantinourunderstandingofhuman

evolutionifmodelsofspatialstructurearetobeused.

Similarly,whileaglobularbraincase doesseemto representasynapomorphyofextantH.

sapiens,canitbeeffectivelycharacterizedforapplicationtothefossilrecord?Weemphasize

thatH.sapiensisalineagewithdeepandlikelydiverseAfricanrootsthatchallengeouruseof

termssuchas‘archaicH.sapiens’and‘anatomicallymodernhumans’. Unlesstheycanbe

operationalized with more clearly defined traits, such categories will have declining value.

DiagnosticsofH.sapiensmustreflecttrajectoriesofevolutionratherthanstaticviewsofour

species–whichhaschanged,andcontinuestochange,atvariousscales.

Thenextdecade ofresearch willbe crucialto resolving theseemergingresearch themes.

ContemporaryhumangenomesarenowavailablefromacrosstheAfricancontinent,together

withan increasingnumberofancientgenomes.Ourunderstandingofpaleoecologyisalso

improvingthankstobiogeographicreconstructionspremisedonthegenomesofAfricanfauna.

Paleoclimatereconstructionsare increasingly precise,withrapidlygrowing proxydata and

bettermodelscoveringkeyperiods.Finally,theexpansionofpaleoanthropological

investiga-tionsintoneglectedareasofAfricawillundoubtedlyrevealnewdatathatwillsignificantlyrefine

theparametersofrecenthumanevolution.

Acknowledgments

E.M.L.S.andH.S.G.wishtothanktheBritishAcademyofHumanitiesandSocialSciencesforfundingthisresearch.E.M.L. S.thankstheWellcomeTrust,theGaltonInstituteandJesusCollegeOxfordforfundingtheworkshop‘HumanEvolutionin StructuredPopulations’attheUniversityofOxfordthatprovidedtheplatformforthisOpinionpiece.M.G.T.wassupported byWellcomeTrustSeniorInvestigatorAwardGrant100719/Z/12/Z.A.M.wassupportedbytheEuropeanResearch CouncilConsolidatorgrant647787–LocalAdaptation.C.S.thankstheCallevaFoundationandtheHumanOrigins ResearchFund.G.P.R.andC.A.T.thanktheAmericanSchoolofPrehistoricResearch(HarvardUniversity).J.S.T.was supportedbytheEuropeanResearchCouncilConsolidatorgrantno.617627.F.D.thankstheResearchCouncilof

forms before they became extinct? TherangeofdatesforH.nalediand H. heidelbergensisconfirmsthe late survivalofatleasttwoarchaicspecies inAfrica.Thesizeandenvironmental diversity of Africa, particularly the poorlyinvestigatedforested regions, mayhavepermittedthelatesurvival ofmorearchaicspeciesaswellasof earlyformsofH.sapiens.These dis-coverieshavefuelledspeculationsthat H. sapiensmay have interbredwith archaicspeciesinAfricaitself. Distin-guishing admixturebetweenspecies fromthe reintegration of diverseH. sapiens lineagesrepresentsa major challenge,withsignificant taxonomic implications.

NorwayanditsCentresofExcellencefundingscheme,theSFFCentreforEarlySapiensBehaviour(projectnumber 262618),andtheLaScArBxresearchprogramme(ANR-10-LABX-52).R.W.D.isgratefultotheLeverhulmeTrustforgrant EM-2016-050.R.D.thankstheWellcomeTrustforfundingundergrantsWT207492andWT206194.L.C.wasfundedby theLIABEEG-B(LaboratoireInternationalAssocié -Bioinformatics,Ecology,Evolution,Genomics,andBehaviour) (CNRS),theLaboratoired’Excellence(LabEx)projectTULIP(ANR-10-LABX-41;ANR-11-IDEX-0002-02),an Investisse-mentd’Avenirgrant(CEBA;ANR-10-LABX-25-01)andtheInstitutoGulbenkiandeCiência.Forthecomputedtomography datainFigure1,wethankthecuratorsoftheoriginalfossilsinMoroccoandIsrael,andJ-J.Hublin.Finally,wethank MichelleO’ReillyattheMaxPlanckInstitutefortheScienceofHumanHistoryforthedesignofFigureIinBox1and Figures3and4.

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