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On the origin of modern humans: Asian perspectives

Article in Science · December 2017 DOI: 10.1126/science.aai9067

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◥ on a somewhat regular basis. New finds of REVIEW SUMMARY H. sapiens fossils, with increasingly secure dating associations, are emerging in different areas of Asia, some seemingly from the first half of PALEOANTHROPOLOGY the Late . Cultural variability dis- cerned from archaeological studies indicates On the origin of modern humans: that modern human behaviors did not simply ◥ spread across Asia in a ON OUR WEBSITE time-transgressive pat- Asian perspectives Read the full article tern. This regional varia- at http://dx.doi. tion, which is particularly Christopher J. Bae,* Katerina Douka,* Michael D. Petraglia* org/10.1126/ distinct in Southeast Asia, science.aai9067 could be related at least ...... in part to environmental BACKGROUND: The earliest fossils of Homo departure points, even during glacial stages and ecological variation (e.g., Palearctic versus sapiens are located in Africa and dated to the late when sea levels would have been much lower. Oriental biogeographic zones). Middle Pleistocene. At some point later, modern Moreover, what role did major climatic fluc- humans dispersed into Asia and reached the far- tuations and environmental events (e.g., the OUTLOOK: Recent findings from , away locales of Europe, , and eventually Toba volcanic super-eruption) play in the dis- hominin paleontology, geochronology, and ge- the Americas. Given that Neandertals, Denisovans, persal of modern humans across Asia? Did ex- netics indicate that the strict “out of Africa” Downloaded from mid-Pleistocene Homo,andH. floresiensis were tirpations of groups occur regularly, and did model, which posits that there was only a single present in Asia before the appearance of mod- extinctions of populations take place? Questions dispersal into Eurasia at ~60,000 years ago, is ern humans, the timing and nature of the spread such as these are paramount in understanding in need of revision. In particular, a multiple- of modern humans across Eurasia continue to hominin evolution and Late Pleistocene Asian dispersal model, perhaps beginning at the be subjects of intense debate. For instance, did paleoanthropology. advent of the Late Pleistocene, needs to be ex-

modern humans replace the indigenous popu- amined more closely. An increasingly robust http://science.sciencemag.org/ lations when moving into new regions? Alterna- ADVANCES: An increasing number of multi- record from Late Pleistocene Asian paleoan- tively, did population contact and interbreeding disciplinary field and laboratory projects focused thropology is helping to build and establish occur regularly? In terms of behavior, did tech- on archaeological sites and fossil localities from new views about the origin and dispersal of nological innovations and symbolism facilitate different areas of Asia are producing impor- modern humans.▪ dispersals of modern humans? For example, it tant findings, allowing researchers to address is often assumed that only modern humans were key evolutionary questions that have long per- capable of using watercraft and navigating to plexed the field. For instance, technological The list of author affiliations can be found in the full article online. distant locations such as Australia and the advances have increased our ability to success- *Corresponding author. Email: cjbae@.edu (C.J.B.); — [email protected] (K.D.); [email protected] (M.D.P.) Japanese archipelago destinations that would fully collect ancient DNA from hominin fossils, Cite this article as C. J. Bae et al., Science 358, eaai9067 not have been visible to the naked eye from the providing proof that interbreeding occurred (2017). DOI: 10.1126/science.aai9067

on December 7, 2017

Map of sites with ages and postulated early and later pathways associated with modern humans dispersing across Asia during the Late Pleistocene. Regions of assumed genetic admixture are also shown. ka, thousand years ago.

Bae et al., Science 358, 1269 (2017) 8 December 2017 1of1 RESEARCH

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

The big questions PALEOANTHROPOLOGY Findings from archaeology, hominin paleontology, geochronology, genetics, and paleoclimatology have all been contributing to a better understand- On the origin of modern humans: ing of the Late Pleistocene human evolutionary record in Asia. Here we discuss some of the big questions that paleoanthropologists are investi- Asian perspectives gating across Asia: Can modern human dispersal

1 2,3 2,4 out of Africa be considered a single event occurring Christopher J. Bae, * Katerina Douka, * Michael D. Petraglia * only after 60 ka, or is the picture more compli- cated? By which route(s) did modern humans dis- “ ” Homo sapiens The traditional out of Africa model, which posits a dispersal of modern perse across Asia? What was the nature of the across Eurasia as a single wave at ~60,000 years ago and the subsequent replacement of interactions between modern humans and hominin all indigenous populations, is in need of revision. Recent discoveries from archaeology, groups already present in Asia? What role did hominin paleontology, geochronology, genetics, and paleoenvironmental studies have geographic and/or paleoenvironmental variations contributed to a better understanding of the Late Pleistocene record in Asia. Important play in modern human dispersals? findings highlighted here include growing evidence for multiple dispersals predating

60,000 years ago in regions such as southern and eastern Asia. Modern humans moving into Can the modern human dispersal be Downloaded from Asia met Neandertals, Denisovans, mid-Pleistocene Homo, and possibly H. floresiensis,with considered a single event occurring only some degree of interbreeding occurring.These early human dispersals, which left at least some after 60 ka? genetic traces in modern populations, indicate that later replacements were not wholesale. Variations of the “out of Africa” (OoA) model may be broadly categorized as follows: (i) a single dis- he origin of modern humans has long per- of the latter trait among the recently reported persal occurring during marine isotope stage plexed us. As the well-known paleoanthro- early modern human fossils from , (MIS) 5; (ii) multiple dispersals beginning dur- http://science.sciencemag.org/ pologist William Howells remarked more (5, 6), it may be possible that it devel- ing MIS 5; (iii) a single dispersal occurring dur- T than four decades ago [(1), p. 477], “That oped much more recently, only within the past ing MIS 3; and (iv) multiple dispersals beginning part of human history covering the emer- 130,000 years. during MIS 3. We detail each of these broadly de- gence of modern man and his regional differ- Some of the earliest morphologically modern fined models below, but we begin with the single- entiation continues to be surprisingly obscure. humans are reported from the sites Omo Kibish, dispersal MIS 3 iteration because it has received Locations of some elements of agreement or con- dating to ~195 thousand years ago (ka) (7), and the greatest attention, followed by the multiple- troversy…have long been clear, but the dimensions Herto, dating to ~160 ka (8), both located in the dispersal MIS 5 model. of the whole problem are far from obvious. The Horn of Africa (Fig. 1A). These fossils have been trees are familiar, but the forest is not.” used for the past several decades to support an Single dispersal during MIS 3 Perhaps the primary reason for this is that East African origin for modern humans, corrobo- The traditional OoA model proposes that a single 9–11 there has been no universal consensus on the traits rating similar findings from genetic studies ( ). major dispersal event of modern humans out of on December 7, 2017 that make us human. Arguments for a large cra- Yet the recent discovery of modern human fossils Africa and into Eurasia occurred some time after nial capacity defining our species went by the from Jebel Irhoud dating to ~310 ka (5, 12)raises 60 to 50 ka (15). In this model, earlier dispersals wayside with the realization that Neandertals, important questions about the singular role of by anatomically modern humans into the Levant whose cranial capacity is slightly larger than ours East Africa in the genesis of modern human mor- (e.g., Qafzeh and Skhul) were minor in scale and, on average, were not actually Cossack soldiers phology. Further, questions exist about whether for all intents and purposes, evolutionary dead or pathological anomalies, but rather were of so-called modern human behaviors appeared ends. This OoA model was largely supported by a much greater geological age than previously around the same time as modern human mor- early genetic studies and to various extents by thought and in fact were penecontemporaneous phology, with most studies supporting a slower archaeology, geochronology, and hominin pale- with the earliest modern humans (2, 3). Further, behavioral transition that occurred over the span ontology (16–21). The 60-ka dispersal continues to we once assumed that “culture” clearly distin- of several hundred thousand years in Africa (13). be based primarily on genetic studies of present- guished us from all other life forms. However, Despite the general acceptance that Homo day human population variation across the world. when Jane Goodall (4) returned from her field sapiens arose in Africa, the initial arrival and Given the degree of variability in the genetic clock studies in the 1960s with the discovery that chim- survival of modern humans in different areas of (because of varying mutation rates and other un- panzeesmadeandusedtools,itraisedquestions the world continue to be strongly debated. Over certainties), it may be possible that this event about whether we could continue to use a broad the past several decades, Asia has been receiv- occurred earlier or later than the 60-ka marker variable such as culture to define humans. The ing increasing attention in these discussions, (18, 22). More recent whole-genome studies (23–25) few generally agreed-upon autapomorphies spe- particularly because it is considered the conduit suggest that a single major dispersal event oc- cific to modern humans include such phenotypic through which H. sapiens arrived in distant lo- curred during which “all contemporary non- traits as the presence of a mental eminence and a cales such as Western Europe, Australia, and Africans branched off from a single ancestral globular braincase. However, given the absence eventually the Americas. Importantly, the Asian population” [(26), p. 179] some time during the continent, bounded roughly by the Pacific, Indian, Late Pleistocene (27). Archaeologists have also 1Department of Anthropology, University of Hawai‘i at Manoa, andArcticOceansonthreesidesandEuropeto set the boundary between 60 and 50 ka on the 2424 Maile Way, 346 Saunders Hall, Honolulu, HI 96822, USA. the west, includes a wide range of latitudinal, basis of the timing of the behavioral and tech- 2Max Planck Institute for the Science of Human History, Kahlaische Strasse 10, D-07743 Jena, . 3Research Laboratory for longitudinal, and even altitudinal variation, which nological transition from the Middle to the Upper Archaeology and the History of Art, School of Archaeology, has major implications for human evolution (14). Paleolithic (20, 21, 28). University of Oxford, 1-2 South Parks Road, OX1 3TG Oxford, Because the questions of what, where, how, and 4 UK. Human Origins Program, National Museum of Natural especially why with regard to our becoming “hu- Multiple dispersals during MIS 5 History, Smithsonian Institution, Washington, DC 20560, USA. ” *Corresponding author. Email: [email protected] (C.J.B.); man continue to be of great interest, we evaluate Another dispersal scenario that is receiving [email protected] (K.D.); [email protected] (M.D.P.) the debate on modern human origins and, spe- increasing attention is the possibility that multiple

Bae et al., Science 358, eaai9067 (2017) 8 December 2017 1of7 RESEARCH | REVIEW dispersals began by the beginning of the Late ers have hypothesized two distinct paths: The The basic tenet of the southern dispersal hy- Pleistocene (14, 29–31). Given the increasing num- first involves crossing over from northern pothesis is an eastward expansion from the Horn ber of paleontological and archaeological reports to the Sinai Peninsula, whereas the second in- of Africa via the Strait of Bab al Mandab, across of hominins from sites in different areas of Asia volves crossing the Bab al Mandab Strait to the southern part of the Arabian Peninsula, along that supposedly predate 60 ka, it would appear Yemen in the southernmost part of the Arabian the Yemen-Oman littorals to the Persian Gulf, and that earlier dispersals out of Africa made it to the Peninsula (30, 44–46) (Fig. 1A). The Bab al Mandab then along the coast of the Indian subcontinent Levant (Qafzeh and Skhul) and probably also Strait is usually about 20 km wide, and during (18). Upon arrival at the Sunda Shelf, and after a to South, East, and Southeast Asia (Fig. 1A and glacial periods, it may have only been about 5 short hiatus, humans dispersed to Sahul, eventu- Table 1) (32–42).Atleastsometracesofthese to 15 km wide. Given the short distances in- ally reaching Australasia soon after 60 ka (53). The earlier dispersals would be expected to be pres- volved, the other continent would have been vis- southern coastal dispersal route out of Africa and ent in the modern record. A recent genetic study ible from the points of both departure and arrival around the Indian Ocean continues to receive sub- seems to support the fossil and archaeological (47),asisthecasetoday.Yetthisrouterequiresa stantial attention, in part because a number of records in that ~2% of the genome of modern water crossing that would have made rafting a genetic studies seem to support it [e.g., (18, 19, 25)]. Papua New Guineans derives from an ancestry necessity. The Sinai Peninsula, on the other hand, However, for modern humans to have been able to that predates the postulated 60-ka expansion by is the only land corridor that has persisted since traverse the southern coastal route, regular access modern humans out of Africa (43). the permanent closing of the Tethys Seaway during to fresh water and utilization of marine resources the Miocene. This land route remains the stron- would have been necessary (54, 55). Unfortunately, Single dispersal during MIS 5 and multiple gest,and,forsome,themostparsimoniouscan- clear evidence for a coastal dispersal around the dispersals during MIS 3 didate for the key dispersal pathway beyond Indian Ocean is not present for regions outside These two models receive the least support from Africa (48, 49). Sunda, and instead, dispersal from the Sinai the various scientific records. The model of a sin- There is little consensus as to the route(s) across terrestrial regions of Arabia and southern Downloaded from gle dispersal during MIS 5 only works if modern taken once outside of Africa. Two major direc- Asia is surmised as the main route of population humans suddenly appeared all across Asia in large tional dispersal models have been proposed: movements (29–31). It is possible that although numbers and remained so continuously through- northern and southern. The northern dispersal coastlines provided favorable habitats, at least out the Late Pleistocene. Although a growing num- model posits that humans moved north of the occasionally, reliance on such resources should ber of sites have been dated to MIS 5 and 4, and Sinai and through the Negev region to reach the be seen as only one component of the whole hu- a number of these are considered to be associated eastern Mediterranean Levant (48). Evidence to man subsistence package (31). http://science.sciencemag.org/ with modern humans, the data do not seem to support this includes the early modern human reflect a major dispersal event at this early date sites of Skhul and Qafzeh in that date to be- FADs and TAQs (compare Fig. 1, A and B). No genetic studies of tween 120 and 90 ka and proposed technological An important point in developing a more con- which we are aware support such a model. The similarities between artifact assemblages in north- crete understanding of the timing and direction model of multiple dispersals during MIS 3 only eastern Africa and the Levant (44, 48, 50, 51). of human movements outside Africa is that the works if there is no evidence for modern humans After this period, there is no evidence for the first appearance datum (FAD) of modern humans before MIS 3 (compare with Fig. 1A). presence of modern humans in the Levant until can serve as terminus ante quem (TAQ) for when about55kaorlater,basedontherecentfindings these dispersals began. In this regard, with the By which route(s) did modern humans from (52). Because of this paucity of emphasis on the supposed “end points,” the key disperse across Asia? evidence, the early presence of modern humans arrival areas are Europe, Australasia, the Japanese

The most widely discussed OoA routes have East intheLevantisconsideredbymanytobeafailed archipelago, and eventually the New World. on December 7, 2017 Africa as the departure point into Asia. Research- dispersal event. Europe has long been at the forefront of these

Fig. 1. Map of sites and postulated migratory pathways associated migration pathways of H. sapiens, based on evidence from the most important with modern humans dispersing across Asia during the Late sites dated to between 60 and 30 ka. Yellow stripes and translucent Pleistocene. Archaic human distributions are also shown. (A)Initial orange represent tentative ranges for Neandertals and early Homo sapiens, dispersal(s) of Homo sapiens, based on sites predating 60 ka. (B)Subsequent respectively.

Bae et al., Science 358, eaai9067 (2017) 8 December 2017 2of7 RESEARCH | REVIEW discussions because it is a heavily studied region A major colonization event that has not re- admixtureandthesharingofculturetocompeti- and an area that was occupied by Neandertals ceived as much attention is the peopling of the tion between and possibly the extinction of one of for several hundred thousand years, with only Japanese archipelago; it has been suggested that the populations (45). Data from genetics and ar- about a 5000- to 3000-year overlap with modern this could have occurred during MIS 6, when a chaeology have directly contributed to increasing humans after initial colonization by the latter land connection was likely present, or some time our understanding of what may have happened group (56). Although migration corridors between during MIS 3, when no land connection existed when Late Pleistocene humans moved into new Europe and the Levant may have been present (28, 65–67). Given that only a few sites in regions of Asia. during MIS 5 (57), evidence for an unequivocal predate 40 ka, and that there are questions about FAD by modern humans before 44 ka is absent. the context and/or artifactual nature of the ma- Introgression The earliest example of fully modern human terials at those localities, the earliest presence Over the past decade, technological advances in anatomy in Europe is the mandibular fragment of modern humans in Japan is considered to be the field of ancient DNA analysis have allowed from Kent’s Cavern in England and the Cavallo about 40 ka (67). Assuming that this date is cor- scientists to obtain uncontaminated genome- teeth from southern (58, 59), dating to be- rect, the initial colonization would have had to wide data from Pleistocene hominin fossils. This tween 41 and 44 ka (Fig. 1B). However, given the involvesometypeofwatercraftandahighdegree has shown that a fair degree of introgression oc- geographic location of both sites, and assuming of seafaring skill (28, 34, 65, 66). curred between Neandertals and modern humans that dispersals into Europe originated from the Thetimingandroutebywhichhumansarrived (27, 72–74). In fact, estimates of Neanderthal DNA Levant or elsewhere in northern Asia and traveled intheAmericashavebeenthesubjectsofalong present in non-African modern humans generally westward, this opens the possibility that earlier and often heated debate (68, 69). Most data ap- range between 1 and 4% (72). One estimate from evidence for modern humans in central or eastern pear to support colonization through Beringia ei- the Romanian Pestera çu Oase 1 fossil is as high as Europe may be present. ther via the ice corridor or the coastal route some 9%, suggesting that this particular modern human

It has long been argued that modern humans time during or right after the last glacial maxi- with a minimum age of 40,000 years may have Downloaded from were the only hominin taxon capable of peopling mum (~20 to 15 ka) (68). However, to reach North had a Neandertal ancestor as recently as four to six Australasia, particularly because it would have America, human foragers had to have first arrived generations back (75). The recent genetic iden- involved the ability to build sturdy watercraft in Siberia. The earliest peopling of Siberia north tification of penecontemporaneous Denisovans and navigate the open seas (60). The peopling of of 50°N appears to have only occurred some time in southern Siberia further complicates the Late Australasia took on greater importance once it between 50 and 45 ka, as indicated by the human Pleistocene human evolutionary picture in Asia was realized that it likely occurred some time femur from Ust’-Ishim in western Siberia (70), (76–79). Reich and colleagues (80) estimated that http://science.sciencemag.org/ between 60 and 40 ka (61, 62). The recent re- and the earliest peopling north of 60°N occurred about 5% of modern-day Melanesian DNA origi- analysis of the (Malakunanja II) site perhapsonlyasrecentlyas32ka(68, 71). Nean- nates from this ancestral Denisovan population, in northern Australia pushes the initial peopling dertals and Denisovans were clearly in southern although more recent estimates are between 1 and of the region back to at least 59 ka and possibly Siberia during the first half of the Late Pleisto- 3% (27, 81). Further, Prüfer and colleagues (73) 65 ka (63), although no fossils have been re- cene, but more northward dispersals were likely found that Neandertals, who were also present at covered from the site. With early modern human by modern humans (Fig. 1B). , interbred with Denisovans; simi- fossils being reported in mainland Southeast Asia larly, gene flow occurred between Denisovans (36, 39, 40), (42), and the How did modern humans interact with and a yet-to-be identified hominin population. In (38) (Fig. 1A) that predate the findings from hominin groups already present in Asia? the latter case, Prüfer and colleagues (73)pos- Madjedbebe (65 ka) and New Guinea [49 ka (64)], When humans arrive in a new territory, one of tulated that the gene flow could be from an an- H. erectus this is perhaps not all that surprising. several things may happen, generally ranging from cestral population, such as . Thus, a on December 7, 2017

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 in questionable association with dates).

Site number in Fig. 1A Site Present-day country Proposed age range Hominin fossils Archaeology Confidence Reference (thousand years) H. sapiens 50 51 9...... Skhul, Qafzeh Israel 120 to 90 Yes ( ) Yes +++ ( , ) 110 ...... 10 Jebel Qattar Saudi Arabia 75 None reported Yes ++ ( ) 31 ...... 11 Mundafan Saudi Arabia 100 to 80 None reported Yes ++ ( ) 111 ...... 12 Aybut Al Auwal Oman 105 None reported Yes ++ ( ) 112 ...... 13 Jebel Faya C United Arab Emirates 125 None reported Yes ++ ( ) 95 ...... 14 Katoati, 16R Dune 96, 80 None reported Yes ++ ( ) 33 ...... 15 Jwalapuram India 85 to 75 None reported Yes ++ ( ) H. sapiens 35 ...... 16 Huanglong 100 to 80 Yes ( ) Yes ++ ( ) H. sapiens 40 ...... 17 Luna China 120 to 70 Yes ( ) Yes ++ ( ) H. sapiens 32 ...... 18 Liujiang China 130 to 70 Yes ( ) None reported + ( ) H. sapiens 37 41 ...... 19 Fuyan China 120 to 80 Yes ( ) None reported ++ ( , ) H. sapiens 36 ...... 20 Zhiren China 100 Yes ( ) None reported ++ ( ) H. sapiens 39 ...... 21 Tam Pa Ling 63 to 46 Yes ( ) None reported ++ ( ) H. sapiens 38 ...... 22 Callao Philippines 67 Yes ( ?) Yes ++ ( ) H. sapiens 42 ...... 23 Lida Ajer Sumatra 73 to 63 Yes ( ) Yes ++ ( ) 63 ...... 24 Madjedbebe Australia 65 None reported Yes ++ ( )

Bae et al., Science 358, eaai9067 (2017) 8 December 2017 3of7 RESEARCH | REVIEW growing number of studies indicate multiple admix- and colleagues (86) even recently suggested that coming more prominent after 35 and 25 ka, re- ture events between modern humans, Neandertals, H. floresiensis may be a hybrid. The key to spectively (31, 33, 34, 94, 95). Interestingly, early Denisovans, and a nonidentified population— phenotypically identifying a hybrid may be to blade and microblade technologies have yet to be events assumed to have occurred in Asia (11, 73, 82). observe, with some regularity, unusual traits (e.g., identified in Southeast Asia, including southern Substantial overlap in time ranges in these same supernumerary teeth) that are not present in China. Because Southeast Asia represents a dif- areas also lends support to likely interactions be- the proposed parent population but suddenly ferent biogeographic zone (Oriental) than the tween these different populations (Fig. 2). appear in the supposed offspring. other regions (Palearctic), this suggests that dif- Genetic studies have shown that the admix- ferent ecological demands required the develop- ture between non-African modern humans and Cultural diffusion ment of a different behavioral toolkit to survive Neandertals could have occurred as recently as In a straightforward scenario, modern humans (14, 34, 96–98). Early evidence of rock art (99) 40 to 86 ka (70, 75). The younger date would would have moved out of Africa and into Asia and deep-sea pelagic fishing (100) in Southeast tend to support the 60-ka OoA model, whereas carrying with them a set of standard “modern” Asia are clear signs of other forms of modern the older admixture date could be interpreted behaviors (e.g., the use of blades, microblades, human adaptation. as one of the early dispersals thought to have art, and symbolism). This is commonly referred It has long been thought that modern human occurred during MIS 5. Malaspinas and colleagues to as the “human revolution” model, thought foraging groups moving over the northern route (23) presented an even more complex admix- to reflect the Middle to Late Paleolithic transi- through Asia carried with them a modern be- ture model and suggested a series of events that tion (21, 28, 55). Numerous studies, however, havioral package (28, 34, 101), sometimes equated occurred between 72 and 42 ka, which included have questioned whether a behavioral revolu- with the Initial Upper Paleolithic technocomplex. a “ghost” lineage. To further complicate the matter, tion actually took place and whether a model, Interestingly, however, the recent identifica- Posth and colleagues (74) recently suggested that originally developed for the western European tionsofDenisovansandNeandertalsinDenisova the beginning of H. sapiens–Neandertal intro- record, is suitable to other regions of the Old Cave—a site that has traditionally been known Downloaded from gression could date to as far back as ~270 ka. World [e.g., (13, 34, 87–90)].Further,thehuman for the presence of a diverse Upper Paleolithic Although indications of introgression now behavioral and skeletal records do not line up industry (e.g., blades, bone tools, and bone or- commonly appear in the genetic literature, we neatly: Modern human behaviors often appear naments) (102)—has complicated this dispersal should attempt to determine whether it is pos- in areas where modern human fossils do not. Be- model, particularly given the apparent absence sible to identify how genetic interchange appears haviors traditionally considered to be represent- of H. sapiens fossils at the site (Box 1). A set of phenotypically. A range of studies of hybrids among ative of modern humans now have been reported perforated teeth and ostrich eggshell and bone http://science.sciencemag.org/ closely related nonhuman primates identified ex- in association with Neandertals, Denisovans, and pendants were excavated from layer 11 of Denisova amples of dysgenesis (“hybrid weakness”)and/or possibly other hominin taxa (91–93). Cave, the same layer that is assigned to Nean- heterosis (“hybrid vigor”) when evaluating a di- Blade technology, long considered one of the dertals (sublayer 11.4) and Denisovans (sublayer versity of size and shape variables (83). A number core components of the Upper Paleolithic in 11.2) (73). This may add to the growing evidence offossilshavebeenproposedaspossiblehybrids Asia, appeared in western Asia after 50 ka and that, at least on a small scale, Neandertals and in the Late Pleistocene human fossil record (84), arrived in South and North Asia sometime after- perhaps other hominins were capable of sym- including from Pestera çu Oase in (85) ward. Microblades appeared during early MIS 3 bolic behavior (91, 92). Alternatively, we may and Zhirendong in China (36). Martinón-Torres in South Asia and late MIS 3 in North Asia, be- be witnessing a series of local extinction and/or

Central Asia on December 7, 2017 Annual precipiation West Asia North Asia Central Asia East Asia South Asia Southeast Asia [mm] MIS

330 290 250

1 10 ka 10 ka Mal’ta 2 25 Kulbulak 25 Pokrovka Upper Cave Üçağızlı Yamashita-Cho 3 Teshik Tash Batadomba Niah Cave Ust’-Ishim Tianyuan Kebara 50 Okladnikov Fa Hien Tabon 50 Manot

Shanidar Tam Pa Ling 4 Callao Amud Obi Rakhmat Chagyrskaya 75 75

Liang Bua Huanglong Qafzeh Zhiren 5 Denisova 100 Luna 100 Fuyan Skhūl Tabun Denisova 125 125

-32 -36 -40 -44 700 500 300 NGRIP East Asian monsoon Neandertals Modern humans Denisovans H. floresiensis δ18O [‰] Annual precipiation [mm]

Fig. 2. Age ranges for the presence of different hominin taxa (mod- exodus out of Africa supported by various studies. If the 60-ka model is ern humans, Neandertals, Denisovans, and H. floresiensis) in all correct, modern humans should not appear in Asia earlier than that. major regions of Asia. The dotted line represents the proposed 60-ka NGRIP, North Greenland Ice Core Project.

Bae et al., Science 358, eaai9067 (2017) 8 December 2017 4of7 RESEARCH | REVIEW

However, increasing findings indicate that multiple Box 1. Who were the Denisovans? dispersals out of Africa by early modern humans On the basis of DNA sequencing of a juvenile finger bone found almost a decade ago, a began during MIS 5, resulting in their earlier ar- previously unknown Late Pleistocene hominin population was identified from Denisova Cave in rival in distant localities in the Levant, South Asia, the Altai Mountains in southern Siberia, now referred to as the Denisovans (76, 77). The Southeast Asia, and China (33, 35–37, 39–42, 50) hominin fossil assemblage from Denisova Cave includes this distal manual phalanx from layer (Fig. 1A). 11.2 (Denisova 3) and an upper left M3 or M2 tooth from layer 11.1 (Denisova 4), found in The initial dispersals out of Africa during MIS association with various archaeological materials typical of both the late Middle Paleolithic (e.g., 5 were likely by small groups of foragers, and Levallois flakes) and the Upper Paleolithic (e.g., microblades and ornaments made from ground these appear to have moved along both a south- stone) (113). In addition, an upper molar (Denisova 8) was found at the interface of layers 11.4 ern and a northern route. The initial dispersal and12in2010,tentativelyalsoidentifiedasanM3orM2(78), and a lower left molar (Denisova 2) by modern humans northward reached at least was recently added to the small number of fossils from the site (79). The archaeological sequence Qafzeh and Skhul. The southern route may have begins at about 250 ka; Denisova 8 has been tentatively dated to >50 ka, whereas Denisova 3 and followedthecoastaroundtheIndianOcean 4 have been dated to between 50 and 30 ka (76–78), although it is likely that these dates will be (18–20), but archaeologicalevidencedominates revised after further geochronological study. for inland dispersal corridors, where a diversity Despite the fact that genetic analyses indicated that the Denisovans were statistically of habitats occur and where reliable freshwater significantly different from both modern humans and Neandertals, comparative morphological rivers, lakes, and animal resources were present studies of the phalanx and molars were inconclusive (11, 77, 78). Thus, these remains were (29–31).SitesdatingtoearlyMIS5toMIS4that referred to simply as Denisovans and not assigned a new species name. Since these initial studies, appear in places such as India, southern China, however, suggestions have arisen that Denisovans may be present in the fossils of Chinese mid- Laos,Sumatra,andthePhilippinesarealllocated

Pleistocene Homo (orevenPenghu1fromTaiwan)(14, 86, 114). Initial comparative studies have a fair distance from any paleocoasts. At least some Downloaded from shown that the Denisovan dentition displays similarities with those of the Chinese Xujiayao hominin of these early dispersals left low-level genetic traces fossils and Teshik-Tash and Oase 2 fossils from western Asia (115, 116). To further complicate in modern human populations (43). matters, at least three Neandertal fossils were also identified at the site (Denisova 5, 9, and 11) A later, major OoA event most likely occurred (73, 117). some time around 60 ka and thereafter. This later dispersal by larger and more demograph- ically successful human populations masked http://science.sciencemag.org/ replacement events at Denisova Cave that in- However, on-the-ground research indicated that genetic traces of the earlier dispersals (73). These volved all three hominin populations, with modern terrestrial environments were reshaped more dispersals across Asia occurred in both north- humans solely responsible for the Upper Paleo- subtly in India (108) and Africa (109) and that erly and southerly directions (28). In the move lithic industries. Another site with evidence of very Middle Paleolithic populations in the Indian sub- north, modern human foragers skirted the Qinghai- early symbolic behavior (~45 ka) is Kara Bom, continent survived the super-eruption (33, 108). Tibetan Plateau to its south to eventually reach which is located, like Denisova Cave, in the Russian The present-day submergence of coastlines Siberia (70).Ataroundthesametimeorsoonafter, Altai Mountains (102). containing traces of hominin occupation will hin- populations reached Europe. These northward- der reconstruction of dispersal routes, partic- traveling human populations carried an advanced What role did geographic and/or ularly during major glacial periods when sea toolkit comprising microliths, blades, composite paleoenvironmental variations play? levels were ~100 m below their current levels (54). tools, and symbolic objects (beads and colorants),

Modern humans dispersing out of Africa and A good example of this is the eastern China which eventually facilitated their dispersal and on December 7, 2017 into Asia were able to adjust to a diversity of seaboard: During glacial periods, the coastal plain successful establishment in higher latitudes and new environments and often would have faced would have extended outward 400 to 600 km and altitudes. These foraging groups carrying a spe- a variety of geographic barriers (e.g., moun- connected areas such as the Shandong Peninsula cialized microblade toolkit eventually made their tain ranges, major riverways, deserts, and seas) in eastern China with the Korean Peninsula, fa- way to the Americas through Beringia (69). The (30, 31, 34, 45, 46). Biological adaptations would cilitating movement of a variety of animals, in- southern route includes possible movement path- have facilitated dispersals during the Late Pleis- cluding humans, across the dry Yellow Sea (94). ways through the Indian subcontinent, mainland tocene to high-altitude regions such as the Qinghai- In the Korea-China case, there is good reason to Southeast Asia, and eventually as far north as Tibetan Plateau by <30 ka (103) and far northern assume that a number of archaeological sites and central China and southward into the Southeast Siberia by 32 ka (68, 71). Nevertheless, cultural Pleistocene faunas are present in this submerged Asian islands and on to Australasia. Questions innovations would have been of even greater im- former coastal plain. It is not clear that the same remain as to why modern human foragers arriv- portance than biological adaptations, simply be- argument can be made for all coastal regions in ing in Southeast Asia discarded blade and micro- cause the latter may take generations to appear Asia. For instance, proponents of the southern blade industries, although evidence in a population, whereas the former can appear coastaldispersalmodelarguethatthereasonthat indicates that communities had ground stone and spread quickly in a single generation. The thereisapaucityofevidenceofcoastaloccupation technologies, which represented adaptations to early development of footwear, as indirectly evi- is that the sites are now submerged (17, 55). How- new environments (63). Further, there are ques- denced at the 40-ka site in northern ever, the coastline along the Indian Ocean rim and tions concerning what happened when different China (104), is a case in point; this cultural trait the western side of the Sunda Shelf has areas of foraging groups, originating in areas to the north would have immediately facilitated human disper- relatively steep drop-off, so that it is unlikely that and south, met in central China (34, 89). sals into colder environments (both latitudinally many coastal sites would be now submerged; more- and altitudinally). over, archaeological surveys in these steep coastal Moving forward: Future directions of Major natural events such as the Toba volcanic shelves and in some uplifted shoreline areas have Late Pleistocene Asian super-eruption at 74 ka in Sumatra, Indonesia, failed to find Late Pleistocene coastal sites (31). paleoanthropology are surmised to have contributed to global cool- A rigid definition of the OoA model positing that ing, substantial landscape resculpting, and the So what happened then? modern humans dispersed from Africa only after die-offofflorasandfaunas,leadingtomam- Growing evidence indicates that modern human 60 ka and simply replaced all indigenous popula- malian bottlenecks and extinctions (105, 106). dispersals out of Africa into Asia occurred by 60 ka tions (e.g., mid-Pleistocene Homo,Neandertals, Ambrose (107) proposed that the Toba super- and afterward (Fig. 1B). Such dispersal events Denisovans, and H. floresiensis)withnointer- eruption led to the extinction of archaic humans across Eurasia are supported by a diversity of breeding can no longer be considered valid. What and a population crash in modern H. sapiens. studies from genetics and archaeology (11, 20, 28). is needed now is to develop more detailed

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Bae et al., Science 358, eaai9067 (2017) 8 December 2017 7of7 On the origin of modern humans: Asian perspectives Christopher J. Bae, Katerina Douka and Michael D. Petraglia

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

The peopling of Asia In recent years, there has been increasing focus on the paleoanthropology of Asia, particularly the migration patterns of early modern humans as they spread out of Africa. Bae et al. review the current state of the Late Pleistocene Asian human evolutionary record from archaeology, hominin paleontology, geochronology, genetics, and paleoclimatology. They evaluate single versus multiple dispersal models and southern versus the northern dispersal Downloaded from routes across the Asian continent. They also review behavioral and environmental variability and how these may have affected modern human dispersals and interactions with indigenous populations. Science, this issue p. eaai9067 http://science.sciencemag.org/

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ANTHROPOLOGY Copyright © 2018 The Authors, some rights reserved; Current evidence allows multiple models for the exclusive licensee American Association peopling of the Americas for the Advancement Ben A. Potter1*, James F. Baichtal2, Alwynne B. Beaudoin3, Lars Fehren-Schmitz4, of Science. No claim to 5 5 1 6 7 original U.S. Government C. Vance Haynes , Vance T. Holliday , Charles E. Holmes , John W. Ives , Robert L. Kelly , Works. Distributed 8 9 10 11,12,13 1,14 Bastien Llamas , Ripan S. Malhi , D. Shane Miller , David Reich , Joshua D. Reuther , under a Creative 15 7 Stephan Schiffels , Todd A. Surovell Commons Attribution NonCommercial Some recent academic and popular literature implies that the problem of the colonization of the Americas has License 4.0 (CC BY-NC). been largely resolved in favor of one specific model: a Pacific coastal migration, dependent on high marine pro- ductivity, from the Bering Strait to South America, thousands of years before Clovis, the earliest widespread cul- tural manifestation south of the glacial ice. Speculations on maritime adaptations and typological links (stemmed points) across thousands of kilometers have also been advanced. A review of the current genetic, archeological, and paleoecological evidence indicates that ancestral Native American population expansion occurred after 16,000 years ago, consistent with the archeological record, particularly with the earliest securely dated sites after ~15,000 years ago. These data are largely consistent with either an inland (ice-free corridor) or Pacific coastal Downloaded from routes (or both), but neither can be rejected at present. Systematic archeological and paleoecological investiga- tions, informed by geomorphology, are required to test each hypothesis.

INTRODUCTION

More nuanced consideration of the proposed alternatives can also http://advances.sciencemag.org/ Investigation of the peopling of the Americas has generated decades be found (10–12). Here, we evaluate the claims made in (1) and of scholarly studies, increasingly illuminated by paleoecological and elsewhere with respect to the current genetic, archeological, and particularly paleogenetic research. There are currently several models paleoecological data and identify model constraints. We also sug- of the peopling process differing with respect to timing, routes, and gest avenues of further research to refine models of the peopling of affiliation with modern (and ancient) populations in Asia and the the Americas. Due to multiple dating techniques presented in this Americas (Fig. 1). One perspective that has become prominent in paper, we use years ago for calibrated radiocarbon dates, OSL and the last decade is of an early entry (~25,000 to 15,000 years ago) into cosmogenic dates, and genetic age estimates. All of these are rough- the Americas via a Pacific coastal migration. This perspective fur- ly comparable. ther implies ecological adaptations (for example, the kelp highway hypothesis) and, more recently, typological relationships (stemmed points) (1–5). We believe that this perspective, although commonly GENETIC AND ARCHEOLOGICAL CONGRUENCE on May 2, 2019 disseminated in the popular press (6–8), is a prematurely narrow Genetic studies provide independent information on the timing and interpretation of current evidence, which yields far less certainty. nature of Native American ancestral divergence from northeast Asian Some proponents (1) also assert that there is near-complete agree- populations, genetic isolation, and expansion into the Americas. ment among archeologists on these issues, but the most recent relevant The most recent comprehensive ancient mitogenomic analysis (13) survey (9) shows that archeologists remain divided, with substan- indicates that Native American ancestors diverged from Siberian tial numbers thinking migrants used both interior and coastal routes, populations between 24,900 and 18,400 years ago with population as well as strong skepticism for several proposed pre-Clovis sites. expansion associated with female lineage diversification sometime between ~16,000 to 13,000 years ago. These results are consistent with a large-scale genomic study based on mostly modern Native 1Department of Anthropology, University of Fairbanks, Fairbanks, AK 99775, American and Siberian data (14). We should be careful to insist on USA. 2Tongass National Forest, U.S. Forest Service, Thorne Bay, AK 99919, USA. confidence intervals rather than relying on mean or median esti- 3Royal Alberta Museum, Edmonton, Alberta T5J 0G2, . 4UCSC Paleogenomics Lab, Department of Anthropology, University of California at Santa Cruz, Santa mates, because the former more accurately reflect the precision of Cruz, CA 95064, USA. 5School of Anthropology and Department of Geosciences, the data. This approach also results in consistency with a wider range University of Arizona, Tucson, AZ 85721, USA. 6Institute of Prairie Archaeology, Uni- of colonization models rather than narrowly limiting the options. 7 versity of Alberta, Edmonton, Alberta T6G 2R3, Canada. Department of Anthropology, Models of diversification should encompass migration from the University of Wyoming, Laramie, WY 82071, USA. 8Australian Centre for Ancient DNA, Environment Institute, School of Biological Sciences, University of Adelaide, geographic location of the ancestral Native American population, Adelaide, South Australia, Australia. 9Department of Anthropology and Carl R. Woese which is currently unknown, but probably includes expansion into 10 Institute for Genomic Biology, University of Illinois, Urbana, IL 61801, USA. Department northeastern Siberia and Beringia. As a possible working hypothe- of Anthropology and Middle Eastern Cultures, Mississippi State University, Starkville, MS 39759, USA. 11Department of Genetics, Harvard Medical School, Bost­ on, MA 02115, USA. sis, if Native American ancestors were situated in southern Siberia 12Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA. 20,000 years ago, then the post–16,000-year expansion must include 13Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, migration into northeast Asia. MA 02142, USA. 14Archaeology Department, University of Alaska Museum of the 15 Genetic analyses dependent on data from modern populations do North, Fairbanks, AK 99775, USA. Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena 07745, Germany. not bear directly on the geographic locations of the divergence events *Corresponding author. Email: [email protected] (13). For instance, the data used to generate the Beringian Incubation

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Archeological sites, >13 ka

Archeological sites, 13–10 ka

Geological/biological samples, 15.7 – 13.3 ka, indicating ice-free and/or vegetated conditions Glacial ice limits (55) 13.4 ka 14.0 ka 15.0 ka

Glacial ice at 14.8 ka Archeological sites, (48) post 8 ka Downloaded from

Fig. 1. Northwest North America with archeological sites older than 10,000 calibrated years before the present (Supplementary Materials) and proposed colo- nization routes: IFC and NPC. Glacial ice extent (white) from (48), and archeological site and geological sample locations summarized in (12, 78). Laurentide Ice Sheet limits (dotted lines) from (55). ka, thousand years; IFC, ice-free corridor; NPC, North Pacific coast. http://advances.sciencemag.org/ Model only require that Native American ancestors were geographi- The locations of ancestral Native Americans between ~20,000 and cally isolated from wherever the East Asian/Siberian ancestors in- 15,000 years ago remain unknown, but two scenarios have been habited during the time of isolation (15). The genetic data do not proposed (19). Scenario 1 posits that the split of Ancient Beringians require that this isolation occurred in central or eastern Beringia— and other Native Americans occurred in northeast Asia/Siberia, it could range across a vast area, from Cis-Baikal to Hokkaido. So while scenario 2 posits that this split occurred in eastern Beringia far, complete nuclear genomes from ancient samples produced in (Alaska). Current archeological and paleoecological data support recent years (16–18) are not able either to substantially narrow the scenario 1. There is no secure evidence of ~20,000-year-old American divergence estimate or to clarify spatial routes of the initial peopling. sites, while there is abundant evidence of human occupation in A recent analysis of the 11,500-year-old Upward Sun River 1 ge- northeast Asia (for example, southern Siberia, Amur basin, Primor’ye, nome (19) suggests that Native Americans descend from a single and Japanese archipelago) (fig. S1) (23). The LGM is regionally population that separated from East Asians by 26,100 to 23,900 characterized by very cold and arid conditions with evidence for on May 2, 2019 years ago, with two deep branches: an Ancient Beringian popula- depopulation of north Asia and no evidence throughout Eurasia for tion that split off ~22,000 to 18,000 years ago and a second branch northward expansions of humans (24, 25). Previous genetic models that split into northern and southern lineages ~17,500 to 14,600 of Native American demography indicate a bottleneck during this years ago (19). Earlier gene flow between ancestral Native Americans period, with expansion only after 16,000 to 13,000 years ago (13, 26). and Ancient North Eurasians (ANEs) (represented by Mal’ta and We observe a clear pattern of human expansion from Siberia to Afontova individuals) between ~25,000 and 20,000 years ago strongly Beringia around 16,000 to 14,000 years (12) and the first unequivocal suggests geographic proximity of these groups, somewhere in and widespread occupations south of glacial ice in the Americas after southern Siberia, where all ANE individuals have been located (see 13,500 years ago, associated with Clovis and Fishtail complex tech- fig. S1 for localities and regions mentioned in the text). The record nologies (27–29). We note that both point types are continent-wide­ of human remains in northeast Asia is very sparse, but they have in North and South America, respectively. They are the only point been recovered at Yana RHS, dating to ~27,000 years ago (20). Un- types with such broad distributions and are consistent with coloniz- fortunately, no ancient DNA analysis has yet been published, but ing processes (30–32), although they might also represent commu- Yana’s location at the extreme western edge of Beringia will make it nication of ideas among low-density early populations. difficult to draw firm conclusions about populations present in the We have firmer geographic constraints on these populations af- rest of western, central, and eastern Beringia, for example, for 1500 ter about 12,600 years ago. Ancient Beringians, associated with the to 2000 km to the southern Beringian coasts or 2500 km to Alaska. Denali complex/Paleoarctic tradition, were in Alaska and adjacent The lack of an unequivocal human presence in the entire region areas between 12,500 and 6000 years ago (19). Although the northern during the Last Glacial Maximum (LGM) between the Yana occu- lineage (including Na-Dene, Algonquian, Salish, Tsimshian, and pation (during a warm period) and the clear expansion of Diuktai Haida) appears constrained to northern North America (33), the Culture (Late Upper Paleolithic) populations moving from south to southern lineage directly links with Clovis (Anzick) (16–18). How- north after 16,000 years ago suggests a temporary expansion of ever, we have no direct genetic evidence arising from populations Middle Upper Paleolithic populations followed by later contraction associated with pre-Clovis sites linking them with later Native during the LGM followed by expansion after the onset of deglaciation Americans. Thus, we should be careful to distinguish potential failed (21, 22). migrations versus the direct ancestors of Clovis and later Paleoindians.

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We also note that pre-Clovis sites continue to vary in site integrity, (Stratum IX) (39). Hunter Island (40) contains materials that may that is, clear associations of secure dates and unambiguous cultural date to ~13,500 years ago or to the Younger Dryas (both radiocarbon materials. There appear to be relatively few technological or adap- dates come from the same layer and do not overlap). Similarly, tive connections among the proposed pre-Clovis sites, or with (lat- Kildit Narrows contains scattered materials from a charcoal-rich er) unequivocal Paleoindian complexes, represented by hundreds of layer with three nonoverlapping associated dates of ~13,600, 12,800, sites and thousands of artifacts across the Americas (34, 35). How- and 10,700 years ago (40). In the latter two cases, the association of ever, analyses by (36) have shown that currently dated Clovis sites the cultural materials and dates is unclear. represent a sample that came from a population of sites that date to Throughout most (~2000 km) of the hypothetical NPC route, a time span covering 1070 to 835 years. This suggests that it is pos- from Yakutat Bay to the Aleutians, the earliest human occupations sible that some pre-Clovis sites after ~15,000 years ago may repre- post-date 8000 years ago (more than 6000 years after the earliest sent Clovis ancestors or are Clovis sites that lack diagnostic artifact interior Beringian occupations), long after shorelines stabilized, types. and using technology derived from earlier interior traditions (Fig. 1) (41, 42). Furthermore, the Siberian Diuktai Culture (~18,000 to 12,000 years ago) is terrestrial, while there is no evidence for POTENTIAL MIGRATION ROUTES coastal or maritime economies along the northwest Pacific coast We review here issues with both North Pacific coast (NPC) and ice- from the Kuriles, Kamchatka, Chukotka, or the Okhotsk Sea coast free corridor (IFC) routes of colonization of mid-continental North until the middle Holocene (43). East Beringian obsidian distribu- America (Fig. 1). We note that an NPC route could originate along tion patterns show long-distance east-west movement of obsidian Downloaded from southern Beringia or from interior Beringia. The IFC route has sev- from interior sources between 14,000 and 13,000 years ago, while eral potential branches funneling in from the north. These include coastal sources were only used 4900 to 2300 years after the earliest a route west of the Mackenzie River between the northern sections interior use, and no coastal obsidian has been found substantially of the Laurentide and Cordilleran Ice Sheets, or through the Liard inland (12). If Paleoindian ancestors moved along the southern and Peace River areas, which also deglaciated early (37). coastal edge of Beringia, we would expect earlier sites in adjacent

A coastal colonization route remains a viable hypothesis; however, Pacific drainages (for example, Copper and Susitna rivers) and later http://advances.sciencemag.org/ several issues relating to the proposed coastal migration have been occupations in the deep interior (for example, Tanana and Yukon typically ignored (12). Contrary to commonly asserted claims, the rivers). Extant data show the earliest occupations along the Tanana entire late Pleistocene coast was not submerged due to rising sea River (~14,200 years ago), later expansion of related technologies levels. A comprehensive meta-analysis (38) reviewing paleoecoastal into the Pacific drainages (~12,000 years ago), and much later ex- geomorphology from Puget Sound to the Alaska Peninsula indicated pansion to the coast (~8000 years ago). All these patterns are incon- that more than half of the northwest Pacific coastal regions retained sistent with an initial coastal migration along the southern edge of preserved pre-Clovis–aged shorelines (Fig. 2). Surveys in these re- Beringia before 16,000 years ago (12). gions have so far failed to discover sites securely dated to older than More research is required to assess resource bases along the NPC ~12,600 years ago (1600 years later than the earliest unequivocal route. Some coastal refugia have been identified in the southern sites in interior Beringia), contradicting common assertions of an part of the coastal route [for example, (44, 45)], whereas the record early coastal migration (12). A few potential earlier sites that have is sparse to the north, including the Alexander Archipelago, southern on May 2, 2019 been reported recently, including Triquet Island, remain unreported coastal Alaska, the Alaska Peninsula, and the Aleutians [see review in peer-reviewed sources. Calvert Island cultural materials includ- in (12)]. Anadromous fish could have been a stable resource for hu- ing human footprints are associated with bracketing ages of be- mans, but the earliest evidence of salmon fishing is in interior Alaska tween 13,300 and 12,700 years ago (Stratum X) and 12,650 years ago (46, 47). Other complications to a coastal route include the potential

14-0 14.5-0 17-0 12-0 6-0 10-0 17-0 15-13 + 5-0 14.1-0 11.0-0 14.5-0 15-0 13.5-0 10.1-0 15-0 15-11.5 + 5-0 15.5-13.0 + 6-0 10.5-0 14 + 4-0 17-0 16-14 + 8-0 16-12 + 4-0 Pre-Clovis coasts below modern sea level (submerged) 4-0 Pre-Clovis coasts above modern sea level

7-0

Fig. 2. Sea-level curves by region and periods above modern sea level (in thousands of calibrated years before the present) (that is, pre-Clovis occupations would be potentially accessible if they are extant), adapted from data in (38, 79).

Potter et al., Sci. Adv. 2018; 4 : eaat5473 8 August 2018 3 of 8 SCIENCE ADVANCES | REVIEW presence of sea ice (pack and drift), recurrent volcanism, and potential biological materials] and leaving its geological framework in a fluid reduction in kelp richness and abundance in periglacial environ- state of understanding. Timing of the LGM and subsequent degla- ments (12). The ecological viability of large stretches of the coastal cial sequences vary considerably in northern and southern corridor route has not been fully evaluated yet, and more work needs to be regions (54). Currently evolving geoarcheological and paleo­ done before we can identify the time periods when this region could ecological studies of interior routes indicate that IFC deglaciation support human populations from the Aleutian area to Puget Sound. initiated by 19,000 years ago. A series of 76 10Be surface exposure Alternatively, another potential entry to the NPC from southwestern cosmogenic nuclide ages reveal that intermediate and high eleva- Yukon is constrained by the deglaciation of the White Pass, estimated tion sites in the Peace River Corridor bottleneck were ice-free be- between 13,500 and 13,000 years ago (48), likely too late to serve as tween 15,000 and 14,000 years ago, while 22 luminescence dates on a route for Paleoindian ancestors. eolian sand indicate that a broad subaerially exposed landscape was The enigmatic record at Bluefish Cave raises the possibility of present by at least ~15,000 years ago (and possibly earlier) and that population pulses into eastern Beringia as early as 24,000 years ago glacial lakes had already substantially drained (Fig. 3) (37, 55–57). (49). We note that if there was successful settlement in the LGM, we Figure 1 illustrates the locations of these key late Pleistocene should see more abundant evidence of sites in the succeeding mil- (and pre-Clovis) geological and paleoecological samples. At least lennia, which we do not. In contrast, a substantial continuous re- two routes into the Peace River Corridor have been proposed: one cord begins ~14,200 years ago at Swan Point CZ4b with multiple along the east side of the Mackenzie Mountains (solid red line hearth features and overlapping dates on hearth charcoal and asso- in Fig. 1), and the other to the west of the Mackenzie Mountains ciated fauna, which represents an East Beringian branch of the geo- through the Yukon Plateau and Pelly River valley to the Liard River Downloaded from graphically extensive Siberian Diuktai Culture (50). East Beringian (dotted red line in Fig. 1) (58). tradition populations around 15,000 to 14,000 years ago would be Moreover, 14C dates on taiga vole indicate vegetated conditions adapted to expanding habitat in the northern funnels of the IFC. in some areas of the bottleneck by at least 14,870 years ago (59), and The southern funnel of the IFC had a detectable human presence by a poplar fragment from Boone Lake in the uplands of northwestern 13,300 years ago (Fig. 1), where a camel and horses were butchered Alberta (60) indicates the presence of trees by at least 13,500 years ago.

in an earliest Clovis or pre-Clovis time range in Alberta’s St. Mary These data suggest a vegetated Corridor well before minimum age http://advances.sciencemag.org/ Reservoir (51–53). estimates of ecological viability derived from the presence of bison Any evaluation of the IFC must rest on a secure geological foun- and horse at 13,100 years ago (61, 62) and plant macrofossils and dation, involving a vast region affected by intense glacial and parag- environmental DNA at Charlie Lake at 12,600 years ago (63) (Fig. 3). lacial dynamics that challenge geologists and paleoecologists. The Beyond the IFC region, other researchers have identified alternative IFC region has received episodic attention over the last several inland routes through unglaciated Cordilleran areas (64–66), where decades. There is currently, however, an almost unprecedented resources such as sheep may have persisted through the LGM (67). level of earth science interest in the central portion of the IFC, Collectively, these data indicate that the Corridor and adjacent in- applying methods previously unavailable [from mapping using terior areas could have emerged as a potential route for ancestral light detection and ranging (LIDAR) data to the increased use of Native Americans as early as 15,000 to 14,000 years ago, and that luminescence and cosmogenic nuclide dating techniques on non- movements in either direction along the entire length of the Corridor on May 2, 2019

Other events

Dating method OSL IRSL 14C

Biological “viability” minima according to (63) Bison dispersal minima (61) Earliest Clovis

Swan Point Paisley Cave Demic Page-Ladson expansion Monte Verde

Fig. 3. Chronology of the central IFC. OSL and IRSL dates indicate minima ages of deglaciation and pro-glacial lake drainage (55), and calibrated 14C dates indicate minima dates for fauna and vegetation (12, 35, 61, 63, 80–82). Demic expansion estimates of Native American ancestors from (13). All dates are shown with 1 SD.

Potter et al., Sci. Adv. 2018; 4 : eaat5473 8 August 2018 4 of 8 SCIENCE ADVANCES | REVIEW were feasible well before Clovis times (12, 68). Both pathways, inte- pathways. Current genetic data provide a relatively wide window of rior and coastal, allow viable hypotheses that need not be mutually constraints for location of the genetic isolation of Native American exclusive and should be further tested. ancestors, and later expansion from Siberia into the Americas (and possibly northeast Asia) around 16,000 to 13,500 years ago. As geneti- cists and archeologists and indigenous communities work together STEMMED POINTS AS CULTURAL DIAGNOSTICS in a respectful and mutually beneficial manner, the opportunities to Several authors (1, 3) have suggested that a variety of stemmed analyze additional human remains to infer population history in the points in different contexts represent a coastal expansion before Americas grow. In parallel, systematic paleogenetic analyses of se- 16,000 years ago. This hypothesis is at a nascent stage, rather than curely dated sediments (77) could potentially directly reveal human [as expressed in (1)] the strongest hypothesis on offer. Stemming is presence. a widespread form of haft design innovated numerous times across Current archeological data fit with terrestrial or coastal migrations multiple continents and is thus not an appropriate derived character (or both) that probably occurred well after the LGM, most probably on which to base a hypothesis of cultural affiliation. No detailed tech- after 16,000 years ago and before the widespread Paleoindian occu- nological analysis has established empirical validity to connect these pations around 13,500 years ago. This configuration of the empirical disparate assemblages. Proponents have noted (7) that stemmed points, evidence explains the absence of consensus among archeologists and crescents, and shell middens date between 12,200 and 11,400 years ago other scientists regarding both routes and timing of the peopling of before the present (cal yr B.P.), about 1000 to 2000 years after wide- the Americas, and should prompt us to continue systematic, geomor- spread Beringian and Clovis sites. Terrestrially oriented subsistence phologically targeted investigations along both pathways. Downloaded from practices are evident across North America several centuries before the appearance of evidence for coastal adaptations. All the well-dated SUPPLEMENTARY MATERIALS early coastal sites from North America are younger than the earliest Supplementary material for this article is available at http://advances.sciencemag.org/cgi/ Clovis sites. Two early near-coastal sites in South America, Monte content/full/4/8/eaat5473/DC1 Verde and Huaca Prieta (69, 70), have few technological connections Table S1. Late Pleistocene and Early Holocene components illustrated in Fig. 1. Fig. S1. Locations mentioned in the text.

with later Paleoindian groups, including the Western Stemmed tra- http://advances.sciencemag.org/ References (83–141) dition of western North America. Contrary to previous assertions (1, 3), Ushki Lake and Paisley REFERENCES AND NOTES Cave stemmed points are dissimilar to Jomon tanged points in key 1. T. J. Braje, T. D. Dillehay, J. M. Erlandson, R. G. Klein, T. C. Rick, Finding the first Americans. ways; despite the map symbols, these points come from interior Science 358, 592–594 (2017). sites reflecting terrestrial adaptations. The Channel Islands sites are 2. J. M. Erlandson, In Paleoamerican Odyssey, K. E. Graf, C. V. Ketron, M. R. Waters, Eds. (Texas not associated with dated stemmed points (and stemmed points in A&M Univ. Press, 2013), pp. 127–131. Mobility and Ancient Society in Asia and the Americas California are not well dated). Triquet Island, apparently dating to 3. J. M. Erlandson, T. J. Braje, in , M. Frachetti, R. Spengler III, Eds. 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Potter et al., Sci. Adv. 2018; 4 : eaat5473 8 August 2018 8 of 8 Current evidence allows multiple models for the peopling of the Americas Ben A. Potter, James F. Baichtal, Alwynne B. Beaudoin, Lars Fehren-Schmitz, C. Vance Haynes, Vance T. Holliday, Charles E. Holmes, John W. Ives, Robert L. Kelly, Bastien Llamas, Ripan S. Malhi, D. Shane Miller, David Reich, Joshua D. Reuther, Stephan Schiffels and Todd A. Surovell

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