REVIEW SUMMARY◥

PALEOANTHROPOLOGY

On the origin of modern humans:Asian perspectivesChristopher J. Bae,* Katerina Douka,* Michael D. Petraglia*

BACKGROUND: The earliest fossils of Homosapiens are located inAfrica anddated to the lateMiddle Pleistocene. At somepoint later,modernhumansdispersed intoAsia and reached the far-away locales of Europe,Australia, and eventuallytheAmericas.Given thatNeandertals,Denisovans,mid-PleistoceneHomo, andH. floresiensiswerepresent in Asia before the appearance ofmod-ernhumans, the timingandnature of the spreadof modern humans across Eurasia continue tobe subjects of intense debate. For instance, didmodern humans replace the indigenous popu-lationswhenmoving intonewregions?Alterna-tively, did population contact and interbreedingoccur regularly? In terms of behavior, did tech-nological innovations and symbolism facilitatedispersals of modern humans? For example, itis often assumed that onlymodernhumanswerecapable of using watercraft and navigating todistant locations such as Australia and theJapanese archipelago—destinations that wouldnot have been visible to the naked eye from the

departure points, even during glacial stageswhen sea levels would have beenmuch lower.Moreover, what role did major climatic fluc-tuations and environmental events (e.g., theToba volcanic super-eruption) play in the dis-persal of modern humans across Asia? Did ex-tirpations of groups occur regularly, and didextinctions of populations takeplace?Questionssuch as these are paramount in understandinghominin evolution and Late Pleistocene Asianpaleoanthropology.

ADVANCES:An increasing number of multi-disciplinary field and laboratory projects focusedon archaeological sites and fossil localities fromdifferent areas of Asia are producing impor-tant findings, allowing researchers to addresskey evolutionary questions that have long per-plexed the field. For instance, technologicaladvances have increased our ability to success-fully collect ancient DNA from hominin fossils,providing proof that interbreeding occurred

on a somewhat regular basis. New finds ofH. sapiens fossils, with increasingly secure datingassociations, are emerging in different areasof Asia, some seemingly from the first half ofthe Late Pleistocene. Cultural variability dis-cerned from archaeological studies indicatesthat modern human behaviors did not simply

spread across Asia in atime-transgressive pat-tern. This regional varia-tion, which is particularlydistinct in Southeast Asia,could be related at leastin part to environmental

and ecological variation (e.g., Palearctic versusOriental biogeographic zones).

OUTLOOK:Recent findings fromarchaeology,hominin paleontology, geochronology, and ge-netics indicate that the strict “out of Africa”model, which posits that therewas only a singledispersal into Eurasia at ~60,000 years ago, isin need of revision. In particular, a multiple-dispersal model, perhaps beginning at theadvent of the Late Pleistocene, needs to be ex-amined more closely. An increasingly robustrecord from Late Pleistocene Asian paleoan-thropology is helping to build and establishnew views about the origin and dispersal ofmodern humans.▪

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The list of author affiliations can be found in the full article online.*Corresponding author. Email: cjbae@hawaii.edu (C.J.B.);douka@shh.mpg.de (K.D.); petraglia@shh.mpg.de (M.D.P.)Cite this article as C. J. Bae et al., Science 358, eaai9067(2017). DOI: 10.1126/science.aai9067

Map of sites with agesand postulated earlyand later pathwaysassociated with modernhumans dispersingacross Asia during theLate Pleistocene.Regions of assumedgenetic admixture arealso shown. ka, thousandyears ago.

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REVIEW◥

PALEOANTHROPOLOGY

On the origin of modern humans:Asian perspectivesChristopher J. Bae,1* Katerina Douka,2,3* Michael D. Petraglia2,4*

The traditional “out of Africa” model, which posits a dispersal of modern Homo sapiensacross Eurasia as a single wave at ~60,000 years ago and the subsequent replacement ofall indigenous populations, is in need of revision. Recent discoveries from archaeology,hominin paleontology, geochronology, genetics, and paleoenvironmental studies havecontributed to a better understanding of the Late Pleistocene record in Asia. Importantfindings highlighted here include growing evidence for multiple dispersals predating60,000 years ago in regions such as southern and eastern Asia. Modern humans moving intoAsia met Neandertals, Denisovans, mid-Pleistocene Homo, and possibly H. floresiensis, withsomedegreeof interbreedingoccurring.These early humandispersals,which left at least somegenetic traces in modern populations, indicate that later replacements were not wholesale.

The origin of modern humans has long per-plexed us. As the well-known paleoanthro-pologist William Howells remarked morethan four decades ago [(1), p. 477], “Thatpart of human history covering the emer-

gence of modern man and his regional differ-entiation continues to be surprisingly obscure.Locations of some elements of agreement or con-troversy…have long been clear, but the dimensionsof the whole problem are far from obvious. Thetrees are familiar, but the forest is not.”Perhaps the primary reason for this is that

there has beennouniversal consensus on the traitsthat make us human. Arguments for a large cra-nial capacity defining our species went by thewayside with the realization that Neandertals,whose cranial capacity is slightly larger than ourson average, were not actually Cossack soldiersor pathological anomalies, but rather were ofa much greater geological age than previouslythought and in fact were penecontemporaneouswith the earliest modern humans (2, 3). Further,we once assumed that “culture” clearly distin-guished us from all other life forms. However,when Jane Goodall (4) returned from her fieldstudies in the 1960swith the discovery that chim-panzees made and used tools, it raised questionsabout whether we could continue to use a broadvariable such as culture to define humans. Thefew generally agreed-upon autapomorphies spe-cific to modern humans include such phenotypictraits as the presence of amental eminence and aglobular braincase. However, given the absence

of the latter trait among the recently reportedearly modern human fossils from Jebel Irhoud,Morocco (5, 6 ), it may be possible that it devel-oped much more recently, only within the past130,000 years.Some of the earliest morphologically modern

humans are reported from the sites OmoKibish,dating to ~195 thousand years ago (ka) (7), andHerto, dating to ~160 ka (8), both located in theHorn of Africa (Fig. 1A). These fossils have beenused for the past several decades to support anEast African origin formodern humans, corrobo-rating similar findings fromgenetic studies (9–11).Yet the recent discovery of modern human fossilsfrom Jebel Irhoud dating to ~310 ka (5, 12) raisesimportant questions about the singular role ofEast Africa in the genesis of modern humanmor-phology. Further, questions exist about whetherso-called modern human behaviors appearedaround the same time as modern human mor-phology, with most studies supporting a slowerbehavioral transition that occurred over the spanof several hundred thousand years in Africa (13).Despite the general acceptance that Homo

sapiens arose in Africa, the initial arrival andsurvival of modern humans in different areas ofthe world continue to be strongly debated. Overthe past several decades, Asia has been receiv-ing increasing attention in these discussions,particularly because it is considered the conduitthrough which H. sapiens arrived in distant lo-cales such as Western Europe, Australia, andeventually the Americas. Importantly, the Asiancontinent, bounded roughly by the Pacific, Indian,and Arctic Oceans on three sides and Europe tothe west, includes a wide range of latitudinal,longitudinal, and even altitudinal variation,whichhas major implications for human evolution (14).Because the questions of what, where, how, andespecially why with regard to our becoming “hu-man” continue to be of great interest, we evaluatethe debate on modern human origins and, spe-

cifically, how the Asian record contributes to ad-dressing such questions.

The big questions

Findings fromarchaeology, homininpaleontology,geochronology, genetics, and paleoclimatologyhave all been contributing to a better understand-ing of the Late Pleistocene human evolutionaryrecord in Asia. Here we discuss some of the bigquestions that paleoanthropologists are investi-gating across Asia: Can modern human dispersalout of Africa be considered a single event occurringonly after 60 ka, or is the picture more compli-cated? By which route(s) did modern humans dis-perse across Asia? What was the nature of theinteractionsbetweenmodernhumansandhominingroups already present in Asia? What role didgeographic and/or paleoenvironmental variationsplay in modern human dispersals?

Can the modern human dispersal beconsidered a single event occurring onlyafter 60 ka?

Variations of the “out of Africa” (OoA)modelmaybe broadly categorized as follows: (i) a single dis-persal occurring during marine isotope stage(MIS) 5; (ii) multiple dispersals beginning dur-ing MIS 5; (iii) a single dispersal occurring dur-ingMIS 3; and (iv)multiple dispersals beginningduring MIS 3. We detail each of these broadly de-finedmodels below, but we begin with the single-dispersal MIS 3 iteration because it has receivedthe greatest attention, followed by the multiple-dispersal MIS 5 model.

Single dispersal during MIS 3

The traditional OoAmodel proposes that a singlemajor dispersal event of modern humans out ofAfrica and into Eurasia occurred some time after60 to 50 ka (15). In this model, earlier dispersalsby anatomically modern humans into the Levant(e.g., Qafzeh and Skhul) were minor in scale and,for all intents and purposes, evolutionary deadends. This OoAmodel was largely supported byearly genetic studies and to various extents byarchaeology, geochronology, and hominin pale-ontology (16–21). The 60-ka dispersal continues tobe based primarily on genetic studies of present-day human population variation across the world.Given the degree of variability in the genetic clock(because of varying mutation rates and other un-certainties), it may be possible that this eventoccurred earlier or later than the 60-ka marker(18, 22). More recent whole-genome studies (23–25)suggest that a single major dispersal event oc-curred during which “all contemporary non-Africans branched off from a single ancestralpopulation” [(26), p. 179] some time during theLate Pleistocene (27 ). Archaeologists have alsoset the boundary between 60 and 50 ka on thebasis of the timing of the behavioral and tech-nological transition from theMiddle to theUpperPaleolithic (20, 21, 28).

Multiple dispersals during MIS 5

Another dispersal scenario that is receivingincreasing attention is the possibility that multiple

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1Department of Anthropology, University of Hawai‘i at Manoa,2424 Maile Way, 346 Saunders Hall, Honolulu, HI 96822, USA.2Max Planck Institute for the Science of Human History, KahlaischeStrasse 10, D-07743 Jena, Germany. 3Research Laboratory forArchaeology and the History of Art, School of Archaeology,University of Oxford, 1-2 South Parks Road, OX1 3TG Oxford,UK. 4Human Origins Program, National Museum of NaturalHistory, Smithsonian Institution, Washington, DC 20560, USA.*Corresponding author. Email: cjbae@hawaii.edu (C.J.B.);douka@shh.mpg.de (K.D.); petraglia@shh.mpg.de (M.D.P.)

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dispersals began by the beginning of the LatePleistocene (14, 29–31). Given the increasing num-ber of paleontological and archaeological reportsof hominins from sites in different areas of Asiathat supposedly predate 60 ka, it would appearthat earlier dispersals out of Africamade it to theLevant (Qafzeh and Skhul) and probably alsoto South, East, and Southeast Asia (Fig. 1A andTable 1) (32–42). At least some traces of theseearlier dispersals would be expected to be pres-ent in the modern record. A recent genetic studyseems to support the fossil and archaeologicalrecords in that ~2% of the genome of modernPapua New Guineans derives from an ancestrythat predates the postulated 60-ka expansion bymodern humans out of Africa (43).

Single dispersal during MIS 5 and multipledispersals during MIS 3

These twomodels receive the least support fromthe various scientific records. The model of a sin-gle dispersal during MIS 5 only works if modernhumans suddenly appeared all across Asia in largenumbers and remained so continuously through-out the Late Pleistocene. Although a growing num-ber of sites have been dated to MIS 5 and 4, anda number of these are considered to be associatedwith modern humans, the data do not seem toreflect a major dispersal event at this early date(compare Fig. 1, A and B). No genetic studies ofwhich we are aware support such a model. Themodel of multiple dispersals during MIS 3 onlyworks if there is no evidence formodern humansbefore MIS 3 (compare with Fig. 1A).

By which route(s) did modern humansdisperse across Asia?

Themost widely discussed OoA routes have EastAfrica as the departure point into Asia. Research-

ers have hypothesized two distinct paths: Thefirst involves crossing over from northern Egyptto the Sinai Peninsula, whereas the second in-volves crossing the Bab al Mandab Strait toYemen in the southernmost part of the ArabianPeninsula (30,44–46) (Fig. 1A). TheBabalMandabStrait is usually about 20 km wide, and duringglacial periods, it may have only been about 5to 15 km wide. Given the short distances in-volved, the other continent would have been vis-ible from the points of both departure and arrival(47), as is the case today. Yet this route requires awater crossing that would have made rafting anecessity. The Sinai Peninsula, on the other hand,is the only land corridor that has persisted sincethepermanent closingof theTethys Seawayduringthe Miocene. This land route remains the stron-gest, and, for some, the most parsimonious can-didate for the key dispersal pathway beyondAfrica (48, 49).There is little consensus as to the route(s)

taken once outside of Africa. Two major direc-tional dispersal models have been proposed:northern and southern. The northern dispersalmodel posits that humans moved north of theSinai and through the Negev region to reach theeastern Mediterranean Levant (48). Evidence tosupport this includes the early modern humansites of Skhul and Qafzeh in Israel that date to be-tween 120 and 90 ka and proposed technologicalsimilarities between artifact assemblages in north-eastern Africa and the Levant (44, 48, 50, 51).After this period, there is no evidence for thepresence of modern humans in the Levant untilabout 55 ka or later, based on the recent findingsfrom Manot Cave (52). Because of this paucity ofevidence, the early presence of modern humansin the Levant is considered by many to be a faileddispersal event.

The basic tenet of the southern dispersal hy-pothesis is an eastward expansion from theHornof Africa via the Strait of Bab al Mandab, acrossthe southern part of the Arabian Peninsula, alongthe Yemen-Oman littorals to the PersianGulf, andthen along the coast of the Indian subcontinent(18). Upon arrival at the Sunda Shelf, and after ashort hiatus, humans dispersed to Sahul, eventu-ally reachingAustralasia soon after 60 ka (53). Thesouthern coastal dispersal route out of Africa andaround the IndianOcean continues to receive sub-stantial attention, in part because a number ofgenetic studies seem to support it [e.g., (18, 19, 25)].However, formodernhumans to have been able totraverse the southern coastal route, regular accessto fresh water and utilization of marine resourceswould have been necessary (54, 55). Unfortunately,clear evidence for a coastal dispersal around theIndian Ocean is not present for regions outsideSunda, and instead, dispersal from the Sinaiacross terrestrial regions of Arabia and southernAsia is surmised as the main route of populationmovements (29–31). It is possible that althoughcoastlines provided favorable habitats, at leastoccasionally, reliance on such resources shouldbe seen as only one component of the whole hu-man subsistence package (31).

FADs and TAQs

An important point in developing a more con-crete understanding of the timing and directionof human movements outside Africa is that thefirst appearance datum (FAD) ofmodern humanscan serve as terminus ante quem (TAQ) for whenthese dispersals began. In this regard, with theemphasis on the supposed “end points,” the keyarrival areas are Europe, Australasia, the Japanesearchipelago, and eventually the New World.Europe has long been at the forefront of these

Bae et al., Science 358, eaai9067 (2017) 8 December 2017 2 of 7

Fig. 1. Map of sites and postulated migratory pathways associatedwith modern humans dispersing across Asia during the LatePleistocene. Archaic human distributions are also shown. (A) Initialdispersal(s) of Homo sapiens, based on sites predating 60 ka. (B) Subsequent

migration pathways of H. sapiens, based on evidence from the most importantsites dated to between 60 and 30 ka.Yellow stripes and translucentorange represent tentative ranges for Neandertals and early Homo sapiens,respectively.

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discussions because it is a heavily studied regionand an area that was occupied by Neandertalsfor several hundred thousand years, with onlyabout a 5000- to 3000-year overlap withmodernhumans after initial colonization by the lattergroup (56). Althoughmigration corridors betweenEurope and the Levant may have been presentduring MIS 5 (57), evidence for an unequivocalFAD by modern humans before 44 ka is absent.The earliest example of fully modern humananatomy in Europe is the mandibular fragmentfrom Kent’s Cavern in England and the Cavalloteeth from southern Italy (58, 59), dating to be-tween 41 and 44 ka (Fig. 1B). However, given thegeographic location of both sites, and assumingthat dispersals into Europe originated from theLevant or elsewhere in northernAsia and traveledwestward, this opens the possibility that earlierevidence formodern humans in central or easternEurope may be present.It has long been argued that modern humans

were the only hominin taxon capable of peoplingAustralasia, particularly because it would haveinvolved the ability to build sturdy watercraftand navigate the open seas (60). The peopling ofAustralasia took on greater importance once itwas realized that it likely occurred some timebetween 60 and 40 ka (61, 62). The recent re-analysis of theMadjedbebe (Malakunanja II) sitein northern Australia pushes the initial peoplingof the region back to at least 59 ka and possibly65 ka (63), although no fossils have been re-covered from the site.With early modern humanfossils being reported in mainland Southeast Asia(36, 39, 40), Indonesia (42), and the Philippines(38) (Fig. 1A) that predate the findings fromMadjedbebe (65 ka) andNewGuinea [49 ka (64)],this is perhaps not all that surprising.

A major colonization event that has not re-ceived as much attention is the peopling of theJapanese archipelago; it has been suggested thatthis could have occurred during MIS 6, when aland connection was likely present, or some timeduring MIS 3, when no land connection existed(28, 65–67). Given that only a few sites in Japanpredate 40 ka, and that there are questions aboutthe context and/or artifactual nature of the ma-terials at those localities, the earliest presenceof modern humans in Japan is considered to beabout 40 ka (67). Assuming that this date is cor-rect, the initial colonization would have had toinvolve some type of watercraft and a high degreeof seafaring skill (28, 34, 65, 66).The timing and route bywhich humans arrived

in the Americas have been the subjects of a longand often heated debate (68, 69). Most data ap-pear to support colonization through Beringia ei-ther via the ice corridor or the coastal route sometime during or right after the last glacial maxi-mum (~20 to 15 ka) (68). However, to reachNorthAmerica, human foragers had to have first arrivedin Siberia. The earliest peopling of Siberia northof 50°N appears to have only occurred some timebetween 50 and 45 ka, as indicated by the humanfemur from Ust’-Ishim in western Siberia (70),and the earliest peopling north of 60°N occurredperhaps only as recently as 32 ka (68, 71). Nean-dertals and Denisovans were clearly in southernSiberia during the first half of the Late Pleisto-cene, but more northward dispersals were likelyby modern humans (Fig. 1B).

How did modern humans interact withhominin groups already present in Asia?

When humans arrive in a new territory, one ofseveral thingsmay happen, generally ranging from

admixture and the sharing of culture to competi-tion between and possibly the extinction of one ofthe populations (45). Data from genetics and ar-chaeology have directly contributed to increasingour understanding of what may have happenedwhen Late Pleistocene humans moved into newregions of Asia.

Introgression

Over the past decade, technological advances inthe field of ancient DNA analysis have allowedscientists to obtain uncontaminated genome-wide data from Pleistocene hominin fossils. Thishas shown that a fair degree of introgression oc-curredbetweenNeandertals andmodernhumans(27, 72–74). In fact, estimates of Neanderthal DNApresent in non-Africanmodern humans generallyrange between 1 and 4% (72). One estimate fromtheRomanian Pestera çuOase 1 fossil is as high as9%, suggesting that this particularmodern humanwith a minimum age of 40,000 years may havehad aNeandertal ancestor as recently as four to sixgenerations back (75). The recent genetic iden-tification of penecontemporaneous Denisovansin southern Siberia further complicates the LatePleistocene human evolutionary picture in Asia(76–79). Reich and colleagues (80) estimated thatabout 5% of modern-day Melanesian DNA origi-nates from this ancestral Denisovan population,althoughmore recent estimates are between 1 and3% (27, 81). Further, Prüfer and colleagues (73)found that Neandertals, whowere also present atDenisova Cave, interbred with Denisovans; simi-larly, gene flow occurred between Denisovansand a yet-to-be identified hominin population. Inthe latter case, Prüfer and colleagues (73) pos-tulated that the gene flow could be from an an-cestral population, such as H. erectus. Thus, a

Bae et al., Science 358, eaai9067 (2017) 8 December 2017 3 of 7

Table 1. Background data for all Asian Late Pleistocene sites associated with early modern humans that appear in Fig. 1A. Triple plus signs indicate

high confidence (hominin fossils and archaeology found in clear association with solid dates); double plus signs, medium confidence (hominin fossils and/or

archaeology found in association or questionable association with dates); single plus sign, weak confidence (hominin fossils and/or archaeology found inquestionable association with dates).

Site number in Fig. 1A Site Present-day country Proposed age range

(thousand years)

Hominin fossils Archaeology Confidence Reference

9 Skhul, Qafzeh Israel 120 to 90 Yes (H. sapiens) Yes +++ (50, 51).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

10 Jebel Qattar Saudi Arabia 75 None reported Yes ++ (110).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

11 Mundafan Saudi Arabia 100 to 80 None reported Yes ++ (31).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

12 Aybut Al Auwal Oman 105 None reported Yes ++ (111).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

13 Jebel Faya C United Arab Emirates 125 None reported Yes ++ (112).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

14 Katoati, 16R Dune India 96, 80 None reported Yes ++ (95).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

15 Jwalapuram India 85 to 75 None reported Yes ++ (33).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

16 Huanglong China 100 to 80 Yes (H. sapiens) Yes ++ (35).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

17 Luna China 120 to 70 Yes (H. sapiens) Yes ++ (40).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

18 Liujiang China 130 to 70 Yes (H. sapiens) None reported + (32).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

19 Fuyan China 120 to 80 Yes (H. sapiens) None reported ++ (37, 41).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

20 Zhiren China 100 Yes (H. sapiens) None reported ++ (36).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

21 Tam Pa Ling Laos 63 to 46 Yes (H. sapiens) None reported ++ (39).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

22 Callao Philippines 67 Yes (H. sapiens?) Yes ++ (38).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

23 Lida Ajer Sumatra 73 to 63 Yes (H. sapiens) Yes ++ (42).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

24 Madjedbebe Australia 65 None reported Yes ++ (63).. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... ..

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growingnumberof studies indicatemultiple admix-ture events betweenmodernhumans,Neandertals,Denisovans, and a nonidentified population—events assumed tohave occurred inAsia (11, 73,82).Substantial overlap in time ranges in these sameareas also lends support to likely interactions be-tween these different populations (Fig. 2).Genetic studies have shown that the admix-

ture between non-African modern humans andNeandertals could have occurred as recently as40 to 86 ka (70, 75). The younger date wouldtend to support the 60-ka OoA model, whereasthe older admixture date could be interpretedas one of the early dispersals thought to haveoccurred during MIS 5. Malaspinas and colleagues(23) presented an even more complex admix-ture model and suggested a series of events thatoccurred between 72 and 42 ka, which includeda “ghost” lineage. To further complicate thematter,Posth and colleagues (74) recently suggested thatthe beginning of H. sapiens–Neandertal intro-gression could date to as far back as ~270 ka.Although indications of introgression now

commonly appear in the genetic literature, weshould attempt to determine whether it is pos-sible to identify how genetic interchange appearsphenotypically. A range of studies of hybrids amongclosely related nonhuman primates identified ex-amples of dysgenesis (“hybrid weakness”) and/orheterosis (“hybrid vigor”) when evaluating a di-versity of size and shape variables (83). A numberof fossils have been proposed as possible hybridsin the Late Pleistocene human fossil record (84),including from Pestera çu Oase in Romania (85)and Zhirendong in China (36). Martinón-Torres

and colleagues (86) even recently suggested thatH. floresiensis may be a hybrid. The key tophenotypically identifying a hybrid may be toobserve, with some regularity, unusual traits (e.g.,supernumerary teeth) that are not present inthe proposed parent population but suddenlyappear in the supposed offspring.

Cultural diffusion

In a straightforward scenario, modern humanswould have moved out of Africa and into Asiacarrying with them a set of standard “modern”behaviors (e.g., the use of blades, microblades,art, and symbolism). This is commonly referredto as the “human revolution” model, thoughtto reflect the Middle to Late Paleolithic transi-tion (21, 28, 55). Numerous studies, however,have questioned whether a behavioral revolu-tion actually took place and whether a model,originally developed for the western Europeanrecord, is suitable to other regions of the OldWorld [e.g., (13, 34, 87–90)]. Further, the humanbehavioral and skeletal records do not line upneatly: Modern human behaviors often appearin areas where modern human fossils do not. Be-haviors traditionally considered to be represent-ative of modern humans now have been reportedin association with Neandertals, Denisovans, andpossibly other hominin taxa (91–93).Blade technology, long considered one of the

core components of the Upper Paleolithic inAsia, appeared in western Asia after 50 ka andarrived in South and North Asia sometime after-ward. Microblades appeared during early MIS 3in South Asia and late MIS 3 in North Asia, be-

coming more prominent after 35 and 25 ka, re-spectively (31, 33, 34, 94, 95). Interestingly, earlyblade andmicroblade technologies have yet to beidentified in Southeast Asia, including southernChina. Because Southeast Asia represents a dif-ferent biogeographic zone (Oriental) than theother regions (Palearctic), this suggests that dif-ferent ecological demands required the develop-ment of a different behavioral toolkit to survive(14, 34, 96–98). Early evidence of rock art (99)and deep-sea pelagic fishing (100) in SoutheastAsia are clear signs of other forms of modernhuman adaptation.It has long been thought that modern human

foraging groupsmoving over the northern routethrough Asia carried with them a modern be-havioral package (28, 34, 101), sometimes equatedwith the Initial Upper Paleolithic technocomplex.Interestingly, however, the recent identifica-tions of Denisovans andNeandertals inDenisovaCave—a site that has traditionally been knownfor the presence of a diverse Upper Paleolithicindustry (e.g., blades, bone tools, and bone or-naments) (102)—has complicated this dispersalmodel, particularly given the apparent absenceof H. sapiens fossils at the site (Box 1). A set ofperforated teeth and ostrich eggshell and bonependantswere excavated from layer 11 ofDenisovaCave, the same layer that is assigned to Nean-dertals (sublayer 11.4) and Denisovans (sublayer11.2) (73). This may add to the growing evidencethat, at least on a small scale, Neandertals andperhaps other hominins were capable of sym-bolic behavior (91, 92). Alternatively, we maybe witnessing a series of local extinction and/or

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Fig. 2. Age ranges for the presence of different hominin taxa (mod-ern humans, Neandertals, Denisovans, and H. floresiensis) in allmajor regions of Asia. The dotted line represents the proposed 60-ka

exodus out of Africa supported by various studies. If the 60-ka model iscorrect, modern humans should not appear in Asia earlier than that.NGRIP, North Greenland Ice Core Project.

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replacement events at Denisova Cave that in-volved all three hominin populations, withmodernhumans solely responsible for the Upper Paleo-lithic industries. Another site with evidence of veryearly symbolic behavior (~45 ka) is Kara Bom,which is located, likeDenisovaCave, in theRussianAltai Mountains (102).

What role did geographic and/orpaleoenvironmental variations play?

Modern humans dispersing out of Africa andinto Asia were able to adjust to a diversity ofnew environments and often would have faceda variety of geographic barriers (e.g., moun-tain ranges, major riverways, deserts, and seas)(30, 31, 34, 45, 46). Biological adaptations wouldhave facilitated dispersals during the Late Pleis-tocene tohigh-altitude regions such as theQinghai-Tibetan Plateau by <30ka (103) and far northernSiberia by 32 ka (68, 71). Nevertheless, culturalinnovations would have been of even greater im-portance than biological adaptations, simply be-cause the latter may take generations to appearin a population, whereas the former can appearand spread quickly in a single generation. Theearly development of footwear, as indirectly evi-denced at the 40-kaTianyuanCave site innorthernChina (104), is a case in point; this cultural traitwould have immediately facilitated humandisper-sals into colder environments (both latitudinallyand altitudinally).Major natural events such as the Toba volcanic

super-eruption at 74 ka in Sumatra, Indonesia,are surmised to have contributed to global cool-ing, substantial landscape resculpting, and thedie-off of floras and faunas, leading to mam-malian bottlenecks and extinctions (105, 106).Ambrose (107) proposed that the Toba super-eruption led to the extinction of archaic humansand a population crash in modern H. sapiens.

However, on-the-ground research indicated thatterrestrial environments were reshaped moresubtly in India (108) and Africa (109) and thatMiddle Paleolithic populations in the Indian sub-continent survived the super-eruption (33, 108).The present-day submergence of coastlines

containing traces of hominin occupationwill hin-der reconstruction of dispersal routes, partic-ularly during major glacial periods when sealevels were ~100m below their current levels (54).A good example of this is the eastern Chinaseaboard: During glacial periods, the coastal plainwould have extended outward 400 to 600 kmandconnected areas such as the Shandong Peninsulain eastern China with the Korean Peninsula, fa-cilitating movement of a variety of animals, in-cluding humans, across the dry Yellow Sea (94).In the Korea-China case, there is good reason toassume that a number of archaeological sites andPleistocene faunas are present in this submergedformer coastal plain. It is not clear that the sameargument can be made for all coastal regions inAsia. For instance, proponents of the southerncoastal dispersal model argue that the reason thatthere is a paucity of evidence of coastal occupationis that the sites are now submerged (17, 55). How-ever, the coastline along the IndianOcean rimandthe western side of the Sunda Shelf has areas ofrelatively steep drop-off, so that it is unlikely thatmany coastal siteswouldbenowsubmerged;more-over, archaeological surveys in these steep coastalshelves and in some uplifted shoreline areas havefailed to find Late Pleistocene coastal sites (31).

So what happened then?

Growing evidence indicates thatmodern humandispersals out of Africa into Asia occurred by 60 kaand afterward (Fig. 1B). Such dispersal eventsacross Eurasia are supported by a diversity ofstudies from genetics and archaeology (11, 20, 28).

However, increasing findings indicate that multipledispersals out of Africa by early modern humansbegan during MIS 5, resulting in their earlier ar-rival in distant localities in the Levant, South Asia,Southeast Asia, and China (33, 35–37, 39–42, 50)(Fig. 1A).The initial dispersals out of Africa duringMIS

5 were likely by small groups of foragers, andthese appear to have moved along both a south-ern and a northern route. The initial dispersalby modern humans northward reached at leastQafzeh and Skhul. The southern routemay havefollowed the coast around the Indian Ocean(18–20), but archaeological evidence dominatesfor inland dispersal corridors, where a diversityof habitats occur and where reliable freshwaterrivers, lakes, and animal resources were present(29–31). Sites dating to early MIS 5 to MIS 4 thatappear in places such as India, southern China,Laos, Sumatra, and the Philippines are all locateda fair distance from any paleocoasts. At least someof these early dispersals left low-level genetic tracesin modern human populations (43).A later, major OoA event most likely occurred

some time around 60 ka and thereafter. Thislater dispersal by larger and more demograph-ically successful human populations maskedgenetic traces of the earlier dispersals (73). Thesedispersals across Asia occurred in both north-erly and southerly directions (28). In the movenorth,modern human foragers skirted the Qinghai-Tibetan Plateau to its south to eventually reachSiberia (70). At around the same time or soon after,populations reached Europe. These northward-traveling human populations carried an advancedtoolkit comprising microliths, blades, compositetools, and symbolic objects (beads and colorants),which eventually facilitated their dispersal andsuccessful establishment in higher latitudes andaltitudes. These foraging groups carrying a spe-cializedmicroblade toolkit eventuallymade theirway to the Americas through Beringia (69). Thesouthern route includes possiblemovement path-ways through the Indian subcontinent, mainlandSoutheast Asia, and eventually as far north ascentral China and southward into the SoutheastAsian islands and on to Australasia. Questionsremain as to why modern human foragers arriv-ing in Southeast Asia discarded blade andmicro-blade stone tool industries, although evidenceindicates that communities had ground stonetechnologies, which represented adaptations tonew environments (63). Further, there are ques-tions concerning what happened when differentforaging groups, originating in areas to the northand south, met in central China (34, 89).

Moving forward: Future directions ofLate Pleistocene Asianpaleoanthropology

A rigid definition of the OoAmodel positing thatmodern humans dispersed from Africa only after60 ka and simply replaced all indigenous popula-tions (e.g., mid-Pleistocene Homo, Neandertals,Denisovans, and H. floresiensis) with no inter-breeding can no longer be considered valid.Whatis needed now is to develop more detailed

Bae et al., Science 358, eaai9067 (2017) 8 December 2017 5 of 7

Box 1. Who were the Denisovans?On the basis of DNA sequencing of a juvenile finger bone found almost a decade ago, a

previously unknown Late Pleistocene hominin population was identified from Denisova Cave inthe Altai Mountains in southern Siberia, now referred to as the Denisovans (76, 77). Thehominin fossil assemblage from Denisova Cave includes this distal manual phalanx from layer11.2 (Denisova 3) and an upper left M3 or M2 tooth from layer 11.1 (Denisova 4), found inassociation with various archaeological materials typical of both the late Middle Paleolithic (e.g.,Levallois flakes) and the Upper Paleolithic (e.g., microblades and ornaments made from groundstone) (113). In addition, an upper molar (Denisova 8) was found at the interface of layers 11.4and 12 in 2010, tentatively also identified as an M3 or M2 (78), and a lower left molar (Denisova 2)was recently added to the small number of fossils from the site (79). The archaeological sequencebegins at about 250 ka; Denisova 8 has been tentatively dated to >50 ka, whereas Denisova 3 and4 have been dated to between 50 and 30 ka (76–78), although it is likely that these dates will berevised after further geochronological study.

Despite the fact that genetic analyses indicated that the Denisovans were statisticallysignificantly different from both modern humans and Neandertals, comparative morphologicalstudies of the phalanx and molars were inconclusive (11, 77, 78). Thus, these remains werereferred to simply as Denisovans and not assigned a new species name. Since these initial studies,however, suggestions have arisen that Denisovans may be present in the fossils of Chinese mid-Pleistocene Homo (or even Penghu 1 from Taiwan) (14, 86, 114). Initial comparative studies haveshown that the Denisovan dentition displays similarities with those of the Chinese Xujiayao homininfossils and Teshik-Tash and Oase 2 fossils from western Asia (115, 116). To further complicatematters, at least three Neandertal fossils were also identified at the site (Denisova 5, 9, and 11)(73, 117).

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models that include the growing evidence forearly dispersals, contractions, extirpations, andextinctions of human groups and lineages, whilerecognizing that not all pre–60 ka dispersalswere evolutionary dead ends. Further, there arestill large swathes of territory in Asia that remainlargely unexplored, and previously identified sitesandmaterials are in need of renewed study. Fortu-nately, the increasing number of multidisciplinaryresearch programs launched in Asia over the pastfew decades has resulted not only in the reportingof many important sites and findings, but also theaccumulation of information that fills in gaps inthe evolutionary record, thereby facilitatingbroaderinterregional comparisons.As attested to by the great interest generated

by the Central Asiatic Expeditions in the early20th century, Asia was once considered to bethe cradle of mankind (14). Although importantfinds from Europe and Africa over the course ofthe past century have diverted attention, Asia is acontinent that has much to offer to research onmodern human origins, thereby shapingwhat wethink we know about our evolution and history.

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ACKNOWLEDGMENTS

We thank the participants of the Wenner-Gren Symposium “HumanColonization of Asia in the Late Pleistocene” for stimulating andlively discussions in Sintra, Portugal. We acknowledge thesupport over the years from the Wenner-Gren Foundation forAnthropological Research, the National Geographic Society, theU.S. National Science Foundation, the Academy of Korean Studies,the College of Social Sciences and School of Pacific and AsianStudies at the University of Hawaiʻi at Manoa (C.J.B.), the MaxPlanck Institute for the Science of Human History (K.D. and M.D.P,)and the European Research Council [ERC-2012-AdG-324139PALAEOCHRON and ERC-2016-STG-715069 FINDER (K.D.) andERC-2011-AdG-295719 PALAEODESERTS (M.D.P.)]. We thankL. Aiello and the anonymous reviewers for their comments andrecommendations.

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On the origin of modern humans: Asian perspectivesChristopher J. Bae, Katerina Douka and Michael D. Petraglia

DOI: 10.1126/science.aai9067 (6368), eaai9067.358Science 

, this issue p. eaai9067Scienceaffected modern human dispersals and interactions with indigenous populations.routes across the Asian continent. They also review behavioral and environmental variability and how these may have paleoclimatology. They evaluate single versus multiple dispersal models and southern versus the northern dispersalAsian human evolutionary record from archaeology, hominin paleontology, geochronology, genetics, and

review the current state of the Late Pleistoceneet al.patterns of early modern humans as they spread out of Africa. Bae In recent years, there has been increasing focus on the paleoanthropology of Asia, particularly the migration

The peopling of Asia

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