The spread of modern humans in Europe John F. Hoffecker1 Institute of Arctic and Alpine Research, University of Colorado, 1560 30th Street, Campus Box 450, Boulder, CO 80309-0450 Edited by Richard G. Klein, Stanford University, Stanford, CA, and approved May 15, 2009 (received for review March 28, 2009) The earliest credible evidence of Homo sapiens in Europe is an made a significant genetic and/or cultural contribution to the archaeological proxy in the form of several artifact assemblages modern human population of Europe. (Bohunician) found in South-Central and possibly Eastern Europe, The interpretation of the genetics of living human popula- dating to <48,000 calibrated radiocarbon years before present (cal tions, supplemented with the analysis of fossil DNA extracted BP). They are similar to assemblages probably made by modern from Neanderthal and early modern human specimens, favors humans in the Levant (Emiran) at an earlier date and apparently the replacement model. The limited number of mtDNA lineages represent a population movement into the Balkans during a warm among living non-African populations is consistent with a model climate interval [Greenland Interstadial 12 (GI 12)]. A second of rapid dispersal, initially eastward out of Africa and subse- population movement may be represented by a diverse set of quently northward into the Eurasian interior (5). Results to date artifact assemblages (sometimes termed Proto-Aurignacian) found from ongoing reconstruction of the Neanderthal genome indi- in the Balkans, parts of Southwest Europe, and probably in Eastern cate a distinctive pattern that cannot be found among living Europe, and dating to several brief interstadials (GI 11–GI 9) that humans and suggests minimal genic exchange between the two preceded the beginning of cold Heinrich Event 4 (HE4) (Ϸ40,000 cal taxa (6). Advocates of the assimilation model argue, however, BP). They are similar to contemporaneous assemblages made by that the existing molecular evidence does not preclude Nean- modern humans in the Levant (Ahmarian). The earliest known derthal contributions to the early modern human European human skeletal remains in Europe that may be unequivocally genome (7). assigned to H. sapiens (Peçstera cu Oase, Romania) date to this time There are factors other than the anatomical and behavioral period (Ϸ42,000 cal BP) but are not associated with artifacts. After traits of the Neanderthals and modern humans that probably the Campanian Ignimbrite volcanic eruption (40,000 cal BP) and the played a role in the transition. One of these is the changing beginning of HE4, artifact assemblages assigned to the classic climates of the MIS 3 interval and their impact on European Aurignacian, an industry associated with modern human skeletal biota. The most widely used stratigraphic framework for MIS 3 remains that seems to have developed in Europe, spread through- Europe is the climate proxy record of the North Atlantic and out the continent. Greenland. According to this record, the period between 60,000 and 30,000 cal BP was characterized by a sequence of generally archaeology ͉ Neanderthals ͉ Homo sapiens ͉ Western Eurasia brief, but often relatively pronounced, oscillations in climate. Oxygen-isotope data from the Greenland Ice Sheet Project 2 (GISP2) ice core indicate no less than 13 warm intervals [or he spread of modern humans in Europe is a controversial Greenland Interstadials (GI)] and 14 cold intervals [or Green- Ttopic in paleoanthropology. There is consensus that at the land Stadials (GS)] during this period (8). The most severe cold beginning of the interstadial period corresponding to Marine intervals correspond to Heinrich Events (HEs), and there are 3 Isotope Stage 3 (MIS 3) at Ϸ60,000 years ago Europe was such events during MIS 3 (HE5–HE3). exclusively occupied by Homo neanderthalensis,whoproduced Amorespecificclimate-relatedfactoristheCampanian stone artifacts classified by archaeologists as Middle Paleolithic, Ignimbrite (CI) volcanic eruption, dated at Ϸ40,000 cal BP, and that by the end of MIS 3 [Ϸ30,000 calibrated radiocarbon which apparently had devastating effects on plant and animal life years before present (cal BP)], the continent was occupied by across large areas of Southern and Eastern Europe and is linked anatomically modern humans (Homo sapiens), who produced a to a cold interval. The CI eruption is identified in GISP2 in the variety of artifacts assigned to the Upper Paleolithic. There is form of a sulfate peak above an interstadial (GI 9) and below considerable disagreement, however, about how this transition HE4 (9). occurred. Some paleoanthropologists have argued that the transition Problems with the Human Fossil and Archaeological Record represents a relatively straightforward replacement of one con- There are several reasons paleoanthropologists have found it generic hominin taxon by another. According to this view, difficult to reconstruct events related to the spread of modern Neanderthals made no significant genetic or cultural contribu- humans in Europe. One is a scarcity of human fossils dating to tion to the human population that inhabited Europe at 30,000 cal the period of the transition, a problem exacerbated in recent BP. The lack of interaction between the two taxa is assumed to years by the redating of a number of human fossils formerly reflect genetic distance and/or profound biobehavioral differ- assigned to this interval to a younger age (7). In some cases, ences (1, 2). The latter may be important to explaining how a human fossil remains are present, but they represent small replacement could have occurred: how a colonizing species from portions of the skeleton (e.g., isolated teeth) difficult to assign outside Europe could successfully compete with an established to a specific taxon (10). local species. Superior cognitive and communicative abilities Because of the gaps and ambiguities of the human fossil record (‘‘behavioral modernity’’) could have conferred a competitive for this period, the transition from Neanderthals to modern advantage on modern humans despite their external origin. humans in Europe has been reconstructed primarily on the basis An alternative model postulates substantial genic exchange of archaeological remains. The latter also contain ambiguities, and cultural influence between Neanderthals and modern hu- mans. Advocates of the ‘‘assimilation model’’ emphasize human fossils that appear to exhibit a combination of Neanderthal and Author contributions: J.F.H. wrote the paper. modern human anatomical traits and archaeological assem- The author declares no conflict of interest. blages that contain a mixture of types both in Middle and Upper This article is a PNAS Direct Submission. Paleolithic industries (3, 4). They conclude that Neanderthals 1E-mail: [email protected]. 16040–16045 ͉ PNAS ͉ September 22, 2009 ͉ vol. 106 ͉ no. 38 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0903446106 however, and many artifact assemblages dating to this period (21), which is most clearly manifest in syntactical language. cannot be firmly attributed to one taxon or the other. These Language and other uses of symbols are, however, part of a SPECIAL FEATURE include assemblages that are not associated with diagnostic broader capacity to create complex, hierarchically organized human fossils and contain a combination of artifact types structures (sometimes labeled recursion) in a variety of media traditionally assigned to Middle and Upper Paleolithic. They are both symbolic and nonsymbolic (22). The latter include tech- often interpreted as manifestations of cultural influence be- nology, which exhibits a pattern of accelerating innovation and tween Neanderthals and modern humans (11), but there are expanding complexity during the Upper Paleolithic (23). The use other reasons typical Middle and Upper Paleolithic artifact of symbols also may have conferred some unique organizational forms might be found together in the same occupation (12). abilities on modern humans (24), and the creation of novel Although stone blade technology is traditionally associated with technologies and organizational structures may have played a Upper Paleolithic industries, it became apparent many years ago significant role in the dispersal of modern humans and their that Middle Paleolithic industries in various parts of Eurasia seemingly rapid colonization of a variety of habitats and climate yield evidence of blade production. Blade manufacture is well zones. documented in the Middle Paleolithic of Europe and the Near Another factor is the presence of competitor species. Both East (13, 14). Neanderthals and hyenas represent likely competitors for mod- If Neanderthals produced at least some of the stone artifact ern humans in Europe, especially with respect to large mammal forms found in Upper Paleolithic assemblages, anatomically prey. With this in mind, it should be noted that comparative modern humans continued to manufacture and use many typical analysis of stable isotope values for Neanderthal and hyena bone Middle Paleolithic forms long after the transition. Production of from a cave in France (late MIS 3) suggests that emphasis on side-scrapers, points, small bifaces, and other such forms con- superherbivores (mammoth and rhinoceros) by the former reduced tinued into the Upper Paleolithic and post-Paleolithic industries. resource competition with hyenas (25). As for modern humans, In North America, such artifacts are common in Paleoindian there is evidence for exploitation of smaller