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The Makers of the Protoaurignacian and Implications for Neandertal Extinction S

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The Makers of the Protoaurignacian and Implications for Neandertal Extinction S RESEARCH | REPORTS 7. M. A. Bonaguidi et al., Cell 145,1142–1155 (2011). 19. J. E. Bestman, J. Lee-Osbourne, H. T. Cline, J. Comp. Neurol. Agreement no. 340793; and to J.S.B. from the Fundação para a 8. M. M. Reimer et al., J. Neurosci. 28, 8510–8516 (2008). 520, 401–433 (2012). Ciência e Tecnologia, Portugal (FCT); to F.T. from European 9. M. Carlén et al., Nat. Neurosci. 12, 259–267 (2009). 20. K. Edelmann et al., J. Comp. Neurol. 521, 3099–3115 (2013). Research Council grant LatentCauses and a BioSysNet grant by 10. K. Meletis et al., PLOS Biol. 6, e182 (2008). the Bavarian ministry of education and research. Supplementary 11. M. März, R. Schmidt, S. Rastegar, U. Strähle, Dev. Dyn. 240, ACKNOWLEDGMENTS materials contain additional data. 2221–2231 (2011). We thank P. Raymonds for sharing the Tg(gfap:GFP)mi2001 – 12. B. Adolf et al., Dev. Biol. 295, 278 293 (2006). fish line. We also thank T. Özturk, A. Steiner-Mazzardi, and SUPPLEMENTARY MATERIALS 13. B. Ayari, K. H. El Hachimi, C. Yanicostas, A. Landoulsi, S. Hübinger for excellent technical help; A. Lepier for the viral www.sciencemag.org/content/348/6236/789/suppl/DC1 N. Soussi-Yanicostas, J. Neurotrauma 27, 959–972 (2010). vector production; S. Hake for the help with intracellular FACS; Materials and Methods 14. N. Kishimoto, K. Shimizu, K. Sawamoto, Dis. Model. Mech. 5, and P. Alexandre, V. Borrell, P. Chapouton, L. Dimou, and Figs. S1 to S17 200–209 (2012). L. Godinho for critical reading of the manuscript. We acknowledge Tables S1 and S2 15. M. März et al., Glia 58, 870–888 (2010). funding to J.N. from the German Research foundation (DFG) by References (21–26) 16. R. L. Bernardos, P. A. Raymond, Gene Expr. Patterns 6, the Sonderforschungsbereich (SFB) 870 and Schwerpunktprogramm Movies S1 to S4 1007–1013 (2006). “Integrative analysis of olfaction”; to M.G. from the DFG by the 17. P. Chapouton et al., J. Neurosci. 30, 7961–7974 (2010). SFB 870, the Leibniz Prize, the Helmholtz Alliance ICEMED, and 12 November 2014; accepted 15 April 2015 18. I. Rothenaigner et al., Development 138, 1459–1469 (2011). the European Research Council grant ChroNeuroRepair: Grant 10.1126/science.aaa2729 ARCHAEOLOGY crucial to current interpretations regarding the timing of arrival of AMHs and their interaction with Neandertals (5–9). The Protoaurignacian appeared around 42,000 The makers of the Protoaurignacian cal yr B.P. (8, 10) in southwest and south-central Europe (fig. S1). In addition to the presence of and implications for personal ornaments, such as perforated shells and worked bones, the Protoaurignacian is char- Neandertal extinction acterized by a dominance of bladelets with typ- ical retouched standardized implements such as 1,2 3 2 4 5 2,6 S. Benazzi, * V. Slon, S. Talamo, F. Negrino, M. Peresani, S. E. Bailey, Font-Yves points and Dufour bladelets produced S. Sawyer,3 D. Panetta,7 G. Vicino,8 E. Starnini,9,10 M. A. Mannino,2 P. A. Salvadori,7 from unipolar cores (5). This techno-complex has M. Meyer,3 S. Pääbo,3 J.-J. Hublin2 been tentatively linked to the Ahmarian industry of the Levant (6, 9). Because the Ahmarian has The Protoaurignacian culture is pivotal to the debate about the timing of the arrival of been attributed to modern humans (11), it has modern humans in western Europe and the demise of Neandertals. However, which on March 30, 2016 been suggested that the Protoaurignacian reflects group is responsible for this culture remains uncertain. We investigated dental remains a westward population movement of AMHs from associated with the Protoaurignacian. The lower deciduous incisor from Riparo Bombrini the Near East (1, 7). However, because only three is modern human, based on its morphology. The upper deciduous incisor from Grotta nondiagnostic human remains are associated with di Fumane contains ancient mitochondrial DNA of a modern human type. These teeth this culture, it is still uncertain who the makers of are the oldest human remains in an Aurignacian-related archaeological context, the Protoaurignacian were (9, 12). The fossil re- confirming that by 41,000 calendar years before the present, modern humans bearing mains associated with the Protoaurignacian that Protoaurignacian culture spread into southern Europe. Because the last Neandertals are available for study consist of the undiagnostic date to 41,030 to 39,260 calendar years before the present, we suggest that the skeletal fragments of a fetus retrieved from Le Downloaded from Protoaurignacian triggered the demise of Neandertals in this area. Piage rock shelter (France) (13), for which the he timing and pattern of the biological and modern humans (AMHs) (4), and a variety of stratigraphic integrity of the Châtelperronian/ cultural shifts that occurred in Western “transitional” and early Upper Paleolithic cultures Aurignacian sequence has been questioned (5), Europe around 45,000 to 35,000 calendar emerged. Among them, the Protoaurignacian is and two deciduous incisors from two northern T years before the present (cal yr B.P.) fuel continuing debates among paleoanthropol- ogists and prehistorians (1–3). During this pe- riod, Neandertals were replaced by anatomically 1Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121 Ravenna, Italy. 2Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany. 3Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany. 4Dipartimento di Antichità, Filosofia, Storia e Geografia, Università di Genova, Via Balbi 2, 16126 Genova, Italy. 5Sezione di Scienze Preistoriche e Antropologiche, Dipartimento di Studi Umanistici, Corso Ercole I d’Este 32, Università di Ferrara, 44100 Ferrara, Italy. 6Center for the Study of Human Origins, Department of Anthropology, New York University, 25 Waverly Place, New York, NY 10003, USA. 7CNR Institute of Clinical Physiology, National Research Council, Via G. Moruzzi 1, 56124 Pisa, Italy. 8Museo Archeologico del Finale, Chiostri di Santa Caterina, 17024 Finale Ligure Borgo, Italy. 9Scuola di Scienze Umanistiche, Dipartimento di Studi Storici, Università di Torino, via S. Fig. 1. Three-dimensional digital models of the Protoaurignacian human remains. The Bombrini Ottavio 20, 10124 Torino, Italy. 10Museo Preistorico Nazionale dei Balzi Rossi, Via Balzi Rossi 9, 18039 Ventimiglia, Italy. tooth is a lower left lateral deciduous incisor (Ldi2), whereas Fumane 2 is an upper right lateral deciduous *Corresponding author. E-mail: [email protected] incisor (Rdi2). B, buccal; D, distal; L, lingual; M, mesial; O, occlusal. Scale bar, 1 cm. SCIENCE sciencemag.org 15 MAY 2015 • VOL 348 ISSUE 6236 793 RESEARCH | REPORTS Italian sites: Riparo Bombrini (western Ligurian libraries from this specimen, which yielded a total of modern humans (Fig. 2) and basally in hap- Alps, Italy) and Grotta di Fumane (western Lessini of 335,628 unique mtDNA fragments (table S4). logroup R (table S6), as also observed for the Mountains, Italy). The lower left lateral deciduous The frequencies of cytosine (C) to thymine (T) ~45,000-year-old AMH specimen from Ust’-Ishim incisor (Ldi2; Fig. 1) found in 1976 in Riparo Bombrini substitutions at the ends of these fragments (34 [in western Siberia (26)], a major group of related (14, 15)(figs.S2toS5)andtheupperrightlateral to 37%, fig. S9), which reflect the deamination of mtDNAs in Eurasia (27)intowhichmostpre- deciduous incisor (Rdi2, Fig. 1) labeled Fumane 2, cytosine residues typical of ancient DNA (21, 22), agricultural mtDNAs in Europe fall (28). which was retrieved in 1992 from the Protoau- are consistent with results from other specimens As expected for an ancient specimen (23, 25), rignacian deposit of Grotta di Fumane (15, 16) of similar age (23–26). Among the fragments the Fumane 2 mtDNA has accumulated fewer (figs. S6 and S7), have to date not been conclu- carrying terminal C-to-T substitutions, we esti- nucleotide substitutions than present-day mtDNA sively attributed to modern humans or Neandertals. mated the residual present-day DNA contamina- (Fig. 2). Using 10 directly dated ancient modern The crown diameters of deciduous incisors are tion to be 3.8% (15). humans (25, 26) as multiple calibration points, we undiagnostic for Neandertals and modern humans, Using these fragments, we reconstructed a estimated the age of the Fumane 2 terminal node as is also the case for other tooth classes (2). mitochondrial genome of 157-fold coverage (fig. to be 44,599 (95% highest posterior density: 19,755 However, on the basis of the buccolingual crown S10). This mtDNA sequence was aligned to the to 72,070) yr B.P. diameter, the Bombrini specimen is close to the mtDNAs of 54 present-day humans, 10 ancient We thus conclude that the Fumane 2 individ- mean of Upper Paleolithic modern humans, where- modern humans, 10 Neandertals, 2 Denisovans, ual carried a mitochondrial genome of a modern as Fumane 2 is closer to the Neandertal mean a hominin from Sima de los Huesos (Spain), and human type. This shows that this individual was (table S1). Other than that, the worn deciduous achimpanzee(Pan troglodytes).TheFumane2 a modern human or had at least some ancestors lower incisors do not provide any morphologically mitochondrial genome falls within the variation who were modern humans. diagnostic information. To establish the identity of the makers of the Protoaurignacian, we analyzed the three-dimensional Table 1. 3D enamel thickness. Bombrini (Ldi2) is standardized to Z scores (for RET index) of the enamel thickness components of the Bombrini Neandertal and recent modern human (RMH) di2 sample in different wear stages. Standard deviations are Ldi2 using a digital approach (17), and we were indicated in parentheses. AET, average enamel thickness index; RET, relative enamel thickness index. able to investigate DNA from the Fumane 2 spec- imen (15).
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