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Quaternary International

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Before the massive modern dispersal into : A 55,000--old partial cranium from Manot ,

∗ Gerhard W. Webera, , Israel Hershkovitzb,c, Philipp Gunzd, Simon Neubauerd, Avner Ayalone, Bruce Latimerf, Miryam Bar-Matthewse, Gal Yasure, Omry Barzilaig, Hila Mayb,c a Department of & Core Facility for Micro-Computed Tomography, University of Vienna, Althanstr. 14, A-1090, Vienna, b Department of and Anthropology, Sackler Faculty of , , PO Box 39040, 6997801, Tel Aviv, Israel c Dan David Center for Human & Research, Shmunis Family Anthropology Institute, Sackler Fac. of Med., Tel Aviv University, PO Box 39040, 6997801, Tel Aviv, Israel d Department of , Max-Planck-Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103, , e Geological Survey of Israel, Yisha'ayahu Leibowitz St. 32, , Israel f Departments of Anatomy and Orthodontics, Case Western Reserve University, 44106, Cleveland, OH, USA g Israel Antiquities Authority, PO Box 586, 91004, Jerusalem, Israel

ARTICLE INFO ABSTRACT

Keywords: Genetic and archaeological models predict that African modern successfully colonized Eurasia between Early modern humans 60,000 and 40,000 (ka), replacing all other forms of hominins. While there is good evidence for the first arrival in Eurasia around 50-45ka, the record is extremely scarce with regard to earlier re- Out-of- presentatives. A partial calvaria discovered at (Western Galilee, Israel) dated to > 55 ka by ur- Modern anium–thorium dating was recently described. Since then, other findings indicated an early dispersal of modern Hybridization humans out-of-Africa between 194 and 177ka (Misliya-1) or possibly even earlier at 210ka (Apidima 1), and a Neurocranial shape quite long existence of sapiens in Africa (, ~300ka). While the faces of these early Homo sapiens appear quite modern, the shape of the braincase seems to lack behind, reaching the modern state only around after 35ka. Here, new data and approaches were applied to the Manot 1 calvaria. The ecto- and en- docranial shape analyses based on micro-computed tomography data and a landmark-semilandmark approach using multiple reconstructions of the incomplete calvaria confirm that Manot 1 is unequivocally modern human. Its endocranial shape is markedly different from the earliest known Homo sapiens and close to the Levantine Qafzeh/Skhul assemblage (120-90ka) as as modern humans, but still shows some deviations from both groups. The absence of other Homo sapiens in the between the Qafzeh/Skhul and Manot popula- tions is not supportive for the hypothesis of a continuous occupation or the local evolution of modern humans. It suggests that Manot 1 represents a population migrating out-of-Africa and reaching the during warmer and wetter climatic conditions over the Northern Sahara and the Mediterranean. Manot 1 shows that both modern humans and Neanderthals (e.g. Kebara, Amud) contemporaneously inhabited the Levant during the Middle to Upper interface. The endocranial shape of Manot 1 might indicate that this population had not yet fully reached the brainshape of modern humans evident after 35ka.

1. Introduction et al., 2011; Sutikna et al., 2016; Mondal et al., 2016; Douka et al., 2019, Détroit et al., 2019). The final expansion of modern humans across the entire Modern human fossils from the beginning of this transitional period between 60 and 40 thousand years ago (ka) was one of the major events are very rare but are key to understanding the relationships and pro- in human evolution. It heralded the decline of all other hominin groups cesses that ultimately resulted in modern Homo sapiens. Manot 1 is a that existed, most notably the Neanderthals, but probably also other partial cranium (Fig. 1) from this crucial period (Hershkovitz et al., archaic forms that still roamed Asia (Yokoyama et al., 2008; Indriati 2015). Manot Cave is situated in Israel in the eastern Mediterranean

∗ Corresponding author. Dept. of Anthropology, University of Vienna, Althanstr. 14, A-1090, Vienna, Austria. E-mail address: [email protected] (G.W. Weber). URL: http://www.anthropology.at/people/gweber (G.W. Weber). https://doi.org/10.1016/j.quaint.2019.10.009 Received 4 February 2019; Received in revised form 19 July 2019; Accepted 11 October 2019 1040-6182/ © 2019 Elsevier Ltd and INQUA. All rights reserved.

Please cite this article as: Gerhard W. Weber, et al., Quaternary International, https://doi.org/10.1016/j.quaint.2019.10.009 G.W. Weber, et al. Quaternary International xxx (xxxx) xxx–xxx

Fig. 1. The original specimen Manot 1 in left and top view. Note the brownish crust that was used for U–Th dating.

Fig. 2. Map of West Asian sites and map of the cave indicating the excavation areas A-L and the discovery area of Manot 1 (red circle). The photo shows the exact spot where the calvaria was found on the flowstone ledge in a small side chamber near Area G. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) zone, along with many other important Israeli sites such as Hayonim, (Fig. 1) could be sampled and U–Th dating could be applied. The dating Amud, Skhul, Qafzeh, Tabun or Kebara, and not far from in of 11 samples from the calcitic crust yielded ages between 68.4ka ± 6.8 , and Dederiyeh in (Fig. 2 left). The cave is an active to 39.2ka ± 5.6. The average of all 11 samples was 54.7ka ± 5.5 (2σ karstic cave with abundant . It consists of an 80 m long error). (Hershkovitz et al., 2015). Manot 1 is thus either related to an main hall sloping down and two lower chambers connecting from the IUP phase, as suggested in Area C based on the very few flint artefacts north and the south (Fig. 2 middle). Part of the cave surface is covered uncovered in Units 7–8, or Manot 1 is associated with a late by flowstones. The Manot calotte was found behind a partial wall of occupation of the cave. Mousterian artefacts were recovered in Areas C resting on a flowstone ledge in a small side chamber (right and D (Hershkovitz et al., 2015; Marder et al., 2017). to area G, Fig. 2, red circles) extending from the NE wall. There were no The overall shape and the qualitative traits of the calvaria demon- associated loose sediments or cultural artefacts. strated that Manot 1 was unequivocally a modern human (Hershkovitz Seven areas (A-G) were opened during the excavations 2010–2014 et al., 2015). However, in this initial publication, the shape of the en- (Fig. 2 middle). The other areas (H-L) were processed in later seasons docranium was not analyzed using statistical shape analysis. In addi- 2015–2018. The archaeological record demonstrates that the cave was tion, several findings after 2015 raised interesting questions and per- intensively occupied during the Early (EUP; attested spectives related to the early and late evolution of anatomically modern by intact sequences of layers in Area E and preserved sedimentological humans. layers in Area C; Marder et al., 2013). The sequence is stratified going One of the discoveries that increased our knowledge about the back in (top to bottom) from Levantine (38-34ka) to African beginning of our Homo sapiens since the initial pre- (46-38ka) and possibly Initial Upper Paleolithic (> 50ka) sentation of Manot 1 (Hershkovitz et al., 2015) was that Homo sapiens, (Hershkovitz et al., 2015). The (MP) is documented or at least hominins very close to our own lineage (Hublin et al., 2017), by scattered finds in Areas A, C and D (Barzilai et al., 2012, 2016; had established themselves as early as Marine Isotope Stage (MIS)-8/9 Marder et al., 2018). In Area E, near the entrance, there are the remains in North (Jebel Irhoud ~300ka; Richter et al., 2017). These of the last occupation with Levantine Aurignacian before the cave en- findings further substantiated the idea (Bräuer et al., 1997) that Homo collapsed and sealed the cave. sapiens originated and dispersed in Africa far earlier than was suggested The radiocarbon dates from samples are in good agreement by the East African MIS-6 fossils from Omo (195ka; McDougall et al., with Uranium–Thorium (U–Th) dates from the in situ flowstones and 2005) and Herto (160ka; White et al., 2003). For example, Florisbad 1 confirm the occupation of the cave during the MP (Hershkovitz et al., from (Dreyer, 1935; ~259ka, Grün et al., 1996) and Eliye 2015). The calcitic crusts on the inside and outside of the calvaria Springs ES-11693 from (Bräuer and Leakey, 1986) may represent

2 G.W. Weber, et al. Quaternary International xxx (xxxx) xxx–xxx an archaic part of the Homo sapiens (Stringer, 2016), dating back around 45ka (Fu et al., 2014), in Tam Pa Ling () 51-46ka (Demeter more than 200ka. Another new discovery, the Levantine maxilla Mis- et al., 2012), at Willandra Lakes () 46-39ka (Allen and liya-1 (Hershkovitz et al., 2018), indicated mi- O'Connell, 2014), and also in Niah () > 46ka (Barker et al., gration out-of-Africa and suggested that Homo sapiens had reached West 2007) and, demonstrated by figurative , at Lubang Jeriji Saléh Asia during early MIS-6, specifically between 194 and 177ka, a time (Borneo) > 40ka (Aubert et al., 2018). The highest Paleolithic ar- roughly contemporaneous with the Omo and Herto people inhabiting chaeological site in Nwya Devu proves that humans were also capable . A recently re-analyzed specimen from (Apidima 1) of inhabiting the Tibetan Plateau at an altitude of 4600 meters above might suggest the arrival of modern humans in even earlier sea level between 40-30ka (Zhang et al., 2018). The presence of modern during MIS-7 (Harvati et al., 2019), but this result is challenged by humans in Europe is substantiated, for instance at the Grotta del Ca- another study (de Lumley, 2019). The fossils from Jebel Irhoud, Mis- vallo in Southern between 45 and 43ka (Benazzi et al., 2011), at liya, and possibly Apidima, thus showed that our species was existing in Kent's Cavern in 44–41.5ka (Higham et al., 2011), along the Africa, and also left Africa, much earlier than we previously antici- Danube in Willendorf/Austria 43.5ka (Nigst et al., 2014), or in Peştera pated. The dental and maxillary anatomy of Misliya 1 is very modern, cu Oase in 42-37ka (Trinkaus et al., 2003). Claims for modern as well as the faces and dental characters of the Jebel Irhoud specimens. human activities > 50ka were made in (formerly Mala- In contrast, the preserved braincases at Jebel Irhoud are not globular, kunanja II) in Australia (Clarkson et al., 2017) but these seem im- generally one of the major characteristics indicating human probable in the face of other fossil, archaeological and genetic results (Neubauer et al., 2018). (O'Connell et al., 2018). During MIS-5 (130-71ka) northeast Africa and the Levant experi- Fitting roughly the fossil and archaeological records, genomics enced climatic amelioration related to changes in temperature and supports the dates of diversification of Eurasian populations after they precipitation that made otherwise arid regions passable for hominins had left Africa. For autosomal , the split time between eastern and (Vaks et al., 2007; Bar-Matthews et al., 2017). While there was already western Eurasians is estimated around 47ka (Terhorst et al., 2017), or a limited potential for dispersal during MIS-7/6, a paleohydrological divergence beginning around 60-50ka is obtained under a model as- corridor formed several during MIS-5 (Breeze et al., 2016). As a suming gradual separation (Schiffels and Durbin, 2014). The Y-chro- consequence, the movement of people between Africa and Eurasia, mosome gives a similar date for the diversification of non-African leading through the Levant, became more feasible. For several decades, lineages of 55–50ka (Poznik et al., 2016), and this is further confirmed the populations from Qafzeh (Vandermeersch, 1981; Valladas et al., by mitochondrial data with a calculated non-African diversification 1987) and Skhul (Stringer et al., 1989; Mercier et al., 1993) in Israel between 55 and 45ka (Posth et al., 2016). represented the earliest evidence of modern humans outside Africa Although not all the fossil and archaeological evidence and dates between 120 and 90ka. They could possibly exemplify an African po- are undisputed, we can recognize occasional modern human dispersals pulation that used a paleohydrological corridor to reach Eurasia. Since into Eurasia from early MIS-6, and probably even MIS-7, onwards, the discovery of Misliya, however, another hypothesis is that Qafzeh/ culminating in a more ubiquitous modern human movement into Skhul might be remnants of this local modern population (Weber et al., Eurasia between 50 and 40ka, and the disappearance of Neanderthals at 2018a), which opens a further possibility, that of a long-term inter- the end of this period (Higham et al., 2014). What needs to be con- mingling with non-modern hominins in the region. The pronounced sidered is that mitochondrial DNA (mtDNA) L3, which is diversity, for instance at Qafzeh, currently remains inexplicable and has ancestral to all non-Africans, originated in Africa around 70-60ka engaged anthropologists for decades. Vandermeersch (1981) high- (Soares et al., 2012, but see Discussion below). This observation sug- lighted the Homo sapiens ( stricto)affinities of the Qafzeh remains, gests that most of the earlier modern humans mentioned above are not but he noted robust and primitive features as well. Trinkaus (2005) our immediate ancestors. In addition, the last flow from Nean- described an overall derived modern human pattern of the Qafzeh/ derthals into Europeans most likely occurred 65-47ka (Sankararaman Skhul sample along with a minority of retained archaic features. et al., 2012). Schwartz and Tattersall (2003) interpreted two morphs at Qafzeh The idea that Homo sapiens evolved within a single population in (Qafzeh 3, 5, 6, 7, 8 vs. Qafzeh 1, 2, 9, 11), emphasizing different su- Africa and dispersed into Eurasia in a single event seems outdated in the praorbital and symphyseal morphologies. These differences could be a light of the evidence at . The derived modern human morphology sign of or of different populations. Despite the large was likely rather driven by a subdivision of Middle and Late diversity, the endocranial shape of the braincases was found to be more African populations which were semi-isolated and adapted to local globular in the Qafzeh/Skhul sample than in the oldest crania attrib- ecologies (Scerri et al., 2018). A constant gene-flow throughout time uted to Homo sapiens from Jebel Irhoud and Omo, but yet not the same was not necessarily established. The connectivity of these structured as present-day humans (Neubauer et al., 2018). populations, each showing different characteristics of anatomical The climatic conditions during MIS-5 and also later may have al- modernity, might have changed over time. In addition, they likely lowed Homo sapiens to disperse from Africa to Eurasia in several waves diffused into Eurasia in multiple waves at different times and routes, and using several routes (e.g. the Levant as well as the Bab al-Mandab and might have interbred in the new territories, both with modern strait) (Bae et al., 2017). The findings from Daoxian (Liu et al., 2015) human precursors from earlier waves as well as with archaic popula- support the presence of modern humans in between 120 and tions (Sankararaman et al., 2016; Yang and Fu, 2018). 80ka. Unfortunately, only dental remains but no crania are described For the shape of the braincase, however, we can recognize a pro- for the site. The reconstruction of paleoenvironmental dynamics of an gression towards globularization over time. Those modern humans in in the Thar desert () identified human occu- Europe and Africa after 35ka are indistinguishable from present-day pation during phases of enhanced humidity between 96 and 60ka humans (Neubauer et al., 2018). Between the times of Qafzeh/Skhul (Blinkhorn et al., 2017). A 85ka modern human phalanx (Al-Wusta-1) (120-90ka) and, for instance, Upper Paleolithic specimens such as from the Arabian Peninsula indicated that dispersals out-of-Africa were Mladeč 1 (35ka) or Cro-Magnon (31ka), such a transition must have not limited to the Levant (Groucutt et al., 2018). Fossil human teeth happened. The hominin calvaria from the Manot Cave provides the first from Lida Ajer (Sumatra) were recently re-investigated. According to fossil evidence falling in this crucial transitional period. With its dating these new analyses (Westaway et al., 2017), modern humans were of > 55ka (Hershkovitz et al., 2015) it is also young enough to possibly present in between 73 and 63ka. originate from the African haplogroup L3 stem population of Eurasians. The density of evidence for modern human occupation in Eurasia The Levant is not only one major corridor for increases further during MIS-3 (60-27ka; van Meerbeeck et al., 2011). out-of-Africa but it is also the geographical convergence between the Modern humans are documented in Ust’-Ishim in western three Africa, Asia, and Europe. The Levant was also occupied

3 G.W. Weber, et al. Quaternary International xxx (xxxx) xxx–xxx by Neanderthals (e.g., Kebara, Amud) during the critical period re- After sliding, the semilandmarks were converted to shape variables garded here. by computing another Procrustes superimposition. We then analyzed As we showed (Hershkovitz et al., 2015) Manot 1 is unequivocally these Procrustes shape variables using principal component analysis modern human with regard to the external shape of the braincase, if (PCA). In contrast to the initial publication (Hershkovitz et al., 2015), compared to closely related humans and other more archaic groups of our missing-data protocol yields now multiple reconstructions of the Homo. Since modern human populations very successfully colonized Manot 1 calvaria, and of the as well. We projected these Eurasia between 50 and 40ka, which might also be related to the re- reconstruction distributions into the principal component space of the shaping and re-organization of the , our hypothesis here is that extant and fossil specimens. The GM computations were performed in Manot 1 would already show an internal cranial shape close to Upper Mathematica 10.1 (Wolfram Research). The estimates of Manot 1 en- Paleolithic and present-day humans. We test this hypothesis and the docranial volume (ECV) were based on the multiple endocranial re- affiliation of Manot 1 to modern humans re-investigating the ecto- and constructions of the cranium and followed the procedures published in endocranial shape with refined and additional data and methods using Spoor et al. (2015) and Neubauer et al. (2018). a large Pleistocene Homo sample, and put Manot 1 into context with the latest insights into modern human evolution. 3. Results

2. Material and Methods The Manot 1 calvaria is fairly well preserved (Figs. 1 and 4) and comprises the uppermost part of the frontal (but is missing gla- For the Manot 1 calvaria, we used micro-computed tomography bella and the superciliary region), two nearly complete parietal , (μCT) data of higher resolution than the medical CT scan used for the and the broken inferior to the external occipital protu- initial publication (Hershkovitz et al., 2015). Manot 1 was scanned at berance. It is small, gracile, and features thin bones. The state of the the Core Facility for Micro-Computed Tomography at the University of obliteration of the sutures suggests an adult age (Hershkovitz et al., Vienna with a custom built VISCOM X8060 (Germany) μCT scanner: 2015). Fig. 4 shows that the parietal bosses are pronounced, the 130 kV, 360 μA, 1400 msec, diamond high performance transmission broadest area of the cranium is high on the braincase, and both side target, 0.75 mm copper filter, spatial resolution 47 μm. X-ray images walls are parallel and vertically oriented which are all traits char- were taken from 1440 different angles. Using filtered back-projection in acteristic of modern humans. There are other traits that are not typical VISCOM XVR-CT 1.07 software, these data were reconstructed as 3D for modern humans, for instance, a coronal keel (i.e. an elevated cor- volumes with a color depth of 16,384 grey values. onal suture), the flattening on top of the braincase or the The comparative sample for the ectocranial data is given in Table 1. which is frequently found in European Neanderthals (Fig. 4). Early UP It comprises 10 Neanderthals, 11 archaic Homo, 17 Upper Paleolithic modern humans also show an occipital bun in high frequency (e.g. humans, 7 early Homo sapiens, and 150 recent modern humans from Mladeč; Weber et al., 2006) as do some African Middle-to-Late Pleis- diverse geographical regions of the world. Fossil specimens that were tocene samples (Harvati et al., 2010). Manot 1 features a spherical either broken or distorted on one side were completed by -ima- suprainiac fossa (Fig. 4) which involves only the external table. The ging the better preserved side along a midsagittal plane. This symmetry spherical shape is different from Neanderthals wherein the fossa is plane was estimated using a least squares plane computed from the transversely elongated. It is also dissimilar from the Levantine early midsagittal landmarks and curve-semilandmarks (see also Gunz et al., Homo sapiens from Qafzeh and Skhul (Smith et al., 2005), but resembles 2009a for additional details). For the endocranial comparative sample some North-African Epipaleolithic from Afalou/ and the see Neubauer et al., (2018). UP from Aduma in (Haile-Selassie et al., 2004). The We use three-dimensional geometric morphometrics (GM) based on landmark Inion in Manot 1 lies below the Endoinion which is the op- anatomical landmarks as well as curve and surface semilandmarks posite of the condition seen in Neanderthals. In modern humans, the (Bookstein, 1997; Gunz and Mitteroecker, 2013) to estimate missing two landmarks usually coincide (Dean et al., 1998). A comparison of data, and compare the external and endocranial morphology of Manot 1 the most important qualitative traits of Manot 1 with the UP European to recent and fossil humans. For the external shape analysis, we used specimen Mladeč 1, recent modern humans and Neanderthals was the measurement protocol described in Gunz et al. (2009b). The anchor summarized in Hershkovitz et al., (2015) Extended Data Table 2. Both points measured at the anatomical landmarks bregma, lambda and Manot 1 and Mladeč 1 show a mosaic of modern and inion, as well as points on either side of the coronal suture, the mid- features. sagittal profile, and the nuchal curve guided the initial placement of the Our principal component analysis (PCA) of the external shape of the surface semilandmarks in the incomplete Manot 1 calvaria. These an- calvaria reveals a separation between and chor points, as well as a mesh of surface semilandmarks, were then Neanderthals, and fossil and recent Homo sapiens (Fig. 5; PC 1 accounts digitized on a complete modern human reference cranium. A thin-plate for 40%, PC 2 for 22%, and PC 3 for 7% of total shape variance). All spline interpolation computed from the anchor points was used to warp reconstructions of Manot 1 (magenta convex hull) fall within the Homo the mesh of surface semilandmarks from the reference specimen to sapiens distribution, and plot close to Upper Paleolithic fossils and some Manot 1; these warped semilandmarks were then projected onto Manot early Homo sapiens. 1 by selecting the closest point on the exterior cranial surface. For the A comparative analysis of the endocranial shape (Fig. 6) shows endocranial shape analysis (Fig. 3) we used the comparative data and distinct clusters of archaic Homo, Neanderthals, and recent Homo sa- protocol described in Neubauer et al. (2018). piens in shape space. Fossils attributed to Homo sapiens exhibit a clear In both GM analyses, semilandmarks were allowed to slide along the trend of endocranial shape change over time: the earliest Homo sapiens respective curves and the neurocranial surface so as to minimise the in our sample (Jebel Irhoud 1 and 2, Omo-Kibish 2) cluster with Homo thin-plate spline bending energy between each specimen and the erectus s.l. and Neanderthals. L.H. 18, Skhul 5, and Qafzeh 6 and 9 sample mean shape. The latter was computed as the average shape cluster on the fringes of extant Homo sapiens variation, and Upper Pa- following a Procrustes superimposition (Rohlf and Slice, 1990) of all leolithic Homo sapiens overlap almost completely with the recent landmarks and semilandmarks, which standardizes information about modern human sample. Multiple endocranial reconstructions of Manot position, orientation, and scale. Those landmarks and semilandmarks 1 (magenta convex hull) plot close together, considering the relatively that were missing on the Manot 1 calvaria and endocranium were es- large number of missing landmarks and semilandmarks that had to be timated using a thin-plate spline interpolation algorithm following estimated (as illustrated in Fig. 3). Different reconstructions of Manot 1 Gunz et al. (2009b), based on multiple reference specimens (using all plot close to the recent modern human shape variation (Fig. 6, grey). extant and fossil specimens, except s.l.). Notably, all reconstructions of Manot 1 fall close to both Qafzeh/Skhul

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Table 1 Sample description. All specimens were assigned a priori to one of the five groups. Group arrangement is heuristic but in fact results from scientific publications of other authors.

4. Discussion

The Manot 1 calvaria is fairly well preserved but is unfortunately missing the whole frontal brow region, the temporal bone, and the cranial base. For the geometric morphometric approach in the current study, these parts were estimated based on multiple reference speci- mens (see Material and Methods) which is an interesting alternative to test the stability of results. In the initial publication (Hershkovitz et al., 2015), in contrast, the set of landmarks of all specimens were cut down Fig. 3. Landmarks and semi-landmarks used to quantify endocranial shape to the available landmark set of Manot 1. With the new approach we shown on a virtual representation of Manot 1 (a) and multiple reconstructions obtained multiple reconstructions of Manot 1 which are shown in Fig. 5 of missing endocranial landmarks and semilandmarks (b). (ectocranial) and Fig. 6 (endocranial). In addition, we advanced the approach exploiting a high-resolution micro-computed tomography (Fig. 6 dark green) and Upper Paleolithic Homo sapiens (Fig. 6 ), scan of Manot 1. however do not overlap with both. The results of the new ectocranial metric analyses are in perfect Based on the multiple endocranial reconstructions of Manot we used agreement with our former conclusions (Hershkovitz et al., 2015). The multivariate regression to estimate the specimen's endocranial volume Manot 1 calvaria is clearly a modern human, resembling closely some (ECV) following Spoor et al. (2015) and Neubauer et al. (2018). ECV Upper Paleolithic fossils and some early Homo sapiens. This finding is estimates for Manot 1, based on 109 modern and fossil H. sapiens re- underlined by the analysis of qualitative characters (Fig. 4), for in- ference specimens for reconstruction, range from 1028 to 1114 ml, with stance, common traits of Manot 1 and Upper Paleolithic specimens a median of 1067 ml, a mean of 1068 ml, and a standard deviation of (Hershkovitz et al., 2015). Although we used here a whole range of 18 ml. different possible reconstructions for the calvaria, their shape variation remains rather limited (Fig. 5, magenta convex hull) and the cloud of reconstructions is always with the distribution of modern humans.

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initial publication (Hershkovitz et al., 2015), reveals an advanced state of brain globularization, different from the first representatives of Homo sapiens such as Jebel Irhoud and Omo and at the fringe of the modern human range of variation. While a gradient towards more globular brain shape from early to Upper Paleolithic Homo sapiens and recent modern humans was described (Neubauer et al., 2018), Manot 1 is indeed similar to the Levantine Qafzeh/Skhul assemblage (120-90ka) and some Upper Paleolithic (e.g. Mladeč 1) and recent modern human individuals. Manot's endocranial shape is, however, also different to the shape of the local, slightly older individuals. This difference does not mainly concern the general state of globularization (which is largely along PC1 in the plots of Fig. 6) but other shape differences, including more parallel side walls in Manot. Our hypothesis that Manot 1 would show an endocranial shape close to Upper Paleolithic and present-day humans can be confirmed, however, with the restriction that its shape is close to, but not included, in the distribution of this sample. We will come back to this point below in the discussion. The reconstructions of the endocranial volume in this contribution are based on a complex metric approach (see Material and Methods). With an average for the multiple possible reconstructions of 1068 ml ± 18 (SD) it yielded a result that is slightly lower than the average previous estimate (Holloway et al., 2004) based on lengths, widths, and circumferences of the (mean 1155 ml), but de- a somewhat larger volume than the approach using physical sculpturing (1010 ml) (Hershkovitz et al., 2015). Nonetheless, all ap- proaches of endocranial volume estimation confirm the small size of Manot 1 in the lowest range of modern human cranial capacities. Fig. 4. Most important qualitative traits indicated on the virtual representation of the Manot 1 calvaria in left and occipital view. There remain two interesting questions around the Manot calvaria: First, how does Manot 1 relate to earlier modern human populations in the Levant and to later populations in Eurasia; and second, is Manot 1 fi fi Manot 1 can thus be con rmed as the rst known fossil evidence of possibly a between modern humans and Neanderthals? modern humans inhabiting the Levantine corridor in the time frame Answering these questions would clearly benefit from ancient DNA fi between 70 and 50ka. It lls the chronological hiatus in the fossil re- analyses. However, the preservation conditions at Manot Cave did not cord right before the massive dispersal of modern humans into Eurasia. allow extracting any exploitable DNA samples from the abundant Manot 1 also documents the close geographical and temporal proximity faunal remains at the cave using current methods (Slon Viviane, pers. of Neanderthals (Amud 60-50ka, Valladas et al., 1999; Kebara 60ka, comm. Jan. 2019). Pending advanced developments in ancient DNA Valladas et al., 1987) and modern humans in the late Levantine Middle methodology, further conclusions about Manot 1 can currently only be Paleolithic. drawn from the morphological data. The endocranial metric analysis, which was not available for the Several lines of evidence indicate that Homo sapiens dispersed out-

Fig. 5. The first three Principal Components in shape space for ectocranial data; grey, recent modern hu- mans of diverse geographical origins; red, Neanderthals; blue, Upper Palaeolithic modern hu- mans; green, early Homo sapiens; orange, archaic hominins; magenta, multiple reconstructions of Manot 1. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

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Fig. 6. The first three Principal Components in shape space for endocranial data in two different views; colours as in Fig. 5. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) of-Africa (Skoglund and Mathieson, 2018: 382). With the sequence of record. These fossils could theoretically represent a long and local fossils from Misliya-1 to the Qafzeh/Skhul assemblage and to Manot 1 it evolutionary line, but they could also originate from multiple in- is presently clear that Homo sapiens left Africa earlier than previously dependent migration events (see Introduction). While Misliya-1 appears thought and inhabited the Levant, at least sporadically, between quite modern in all its anatomical units (maxillary bone, premolars, ~185ka and ~55ka. Yet, there are large chronological gaps in the molars; Hershkovitz et al., 2018), the much later Qafzeh/Skhul

7 G.W. Weber, et al. Quaternary International xxx (xxxx) xxx–xxx assemblage differs in the manifestation of archaic traits. As mentioned, modern Europeans. This scenario is in agreement with the genetic there could have been two different morphs present during MIS-5 findings that Neanderthal traits were already introduced into modern (Schwartz and Tattersall, 2003). Metric analysis of Levantine post- European human before they actually reached Europe canine teeth confirmed the high intra-group variation (Weber et al., (Sankararaman et al., 2012). Additional genetic input from Nean- 2018b). Our GM analysis here shows that there is a large shape varia- derthals in Europe might also have contributed, as the assimilation tion among Qafzeh 9, Qafzeh 6 and Skhul V ectocranially, and to a model (Smith et al., 2005) would predict. lesser extent endocranially. Manot 1 is closest to Qafzeh 9, but differs The presence of a mosaic morphology in Manot 1 and some UP from all of them. It is not possible to determine the exact relationship European specimens might be interpreted as an indication of ad- between these specimens with such limited fossil samples. However, the mixture. As Fig. 4 shows, Manot 1 features some traits that are found in complete absence of other modern humans between the Qafzeh/Skhul Neanderthals, aside the more numerous modern traits. The same is true populations (120-90ka) and Manot 1 (> 55ka) weakens any idea re- for Mladeč 1(Hershkovitz et al., 2015 Extended Data Table 2). It is garding the continuous occupation and local evolution in the Levant. worth noting that different traits can have different diagnostic values. Alternatively, Manot 1 could originate from a migration of Africans For instance, vertical cranial side walls and a broadest skull region high into West Asia that came later than those MIS-5 people who inhabited on the parietals are reliable indicators of a modern neurocranial shape. the Qafzeh/Skhul several tens of millennia before. Manot 1 oc- In contrast, the occipital bun appears occasionally in modern humans, cupies the appropriate and geography for when and where as does the suprainiac fossa. Since the overall shape of the calvaria is in we would expect to find a population migrating into Eurasia between any case very modern and distinct from Neanderthals (see Figs. 5 and 60 and 40ka. It falls comfortably into the time interval of the estimated 6), the indications for hybridization of Manot 1 are inconclusive. diversification of non-African lineages regarding autosomal, Y-chro- Moreover, the identification of hybrids based solely on cranial mor- mosomal, and mitochondrial DNA (see Introduction). It also post-dates phology has to be viewed very cautiously. Mladeč 5 and 6 in our ec- the emergence of mtDNA haplogroup L3 in Africa between 70 and 60ka tocranial shape analysis (Fig. 5; unfortunately, no endocranial analysis (79-59ka 95% confidence interval; Soares et al., 2012) which is an- is possible since the original skulls were destroyed in WW II and the cestral to all non-African . The branches M and N likely casts do not allow placing endocranial landmarks) would actually be diversified later from L3 en-route (Soares et al., 2012). This picture was better candidates for hybrids but there remains the question of sexual challenged recently by another study proposing an out-of-Africa mi- dimorphism (both are classified as males, whereas Mladeč 1 may re- gration of a pre-L3 lineage into Asia around 125ka, and a return of the present a female, like Manot 1). L3 lineages from Eurasia to Africa ~70ka (Cabrera et al., 2018). Other new interesting findings from the Manot Cave were recently Despite this complication, Manot 1 could still represent a member of an described. Six teeth (three deciduous and three permanent) were found L3 group that gave rise to Eurasian UP populations. at the cave, and four of them could be metrically analyzed (Sarig et al., Could Manot 1 be one of our direct ancestors? The data of 2019). These younger teeth come from other cave areas (C, E, and J) the modern human from Peştera cu Oase (Romania, 42-37ka) than Manot 1 (area G) and confirm the presence of modern humans in shows that even an early European UP individual might not have the later Ahmarian (46-42ka) and Levantine Aurignacian (38-34ka) contributed substantially to later humans in Europe (Fu et al., 2015). period. The material demonstrates a mosaic of modern and Neanderthal Skoglund and Mathieson (2018) speculate in their review that many dental traits, but to a varying degree. Another contribution dealing with ancient populations > 45ka may indeed have simply gone extinct. bones from Manot Cave demonstrates that they belong to a modern Nevertheless, modern Papuans show genomes that in fact derive pri- human, yet also showing few Neanderthal features (Borgel et al., 2019). marily from the main expansion of modern humans out-of-Africa, but These results are compatible with the hypothesis that different Homo carry at least 2% of an earlier, otherwise extinct dispersal (Pagani et al., populations, possibly exhibiting varying degrees of Neanderthal ad- 2016), which could possibly relate back to an early MIS-5 migration of mixture, occupied Manot Cave during the Early Upper Paleolithic modern humans. This suggests that the likelihood of Manot 1 being period. Since Neanderthals were present in the area between 60 and among our direct ancestors might be small but not zero. In any case, it is 50ka (e.g. Amud, Kebara), a hybridization cannot be excluded for the only fossil evidence in West Asia from the crucial time of the Manot 1 but our data cannot prove this. The critical endocranial shape massive expansion movements of modern humans into Eurasia. differences with regard to globularization between modern and more All living non-African humans carry 1–4% Neanderthal genes archaic Homo are mainly found on PC1 (Fig. 6), while Manot 1 shows (Green et al., 2010). Using the breakdown of Neanderthal segments in indeed a modern state but deviates slightly from Qafzeh/Skhul, Upper the genome, the period when this gene flow took place was estimated Paleolithic and recent humans mainly along PC2 and PC3. Instead of between 60 and 50ka (Sankararaman et al., 2012; Fu et al., 2014; hybridization this could mean that Manot 1 had not yet fully reached Moorjani et al., 2016). The fact that Neanderthal ancestry is shared the brainshape of modern humans < 35ka, indicating that this process among all non-Africans suggests that at least the first pulse of admixture of globularization was ongoing after 55ka. happened within a short time in a restricted area before these ancestors spread out into Eurasia. An obvious region for this event is West Asia 5. Conclusions (Sankararaman et al., 2012). Since decades, anthropologists consider it highly likely that hybrids could be present in this geographical transi- New ecto- and endocranial data both confirm that Manot 1 re- tion zone (Simmons, 1999). presents the first evidence of modern humans inhabiting the Levantine This scenario does not mean admixture was restricted to a single corridor > 55ka, prior to the massive dispersal of modern humans into event. The different levels of Neanderthal ancestry in East Asians and Eurasia 50-40ka and after the estimated emergence time of mtDNA Europeans can be best explained by additional pulses of admixture haplogroup L3 which is ancestral to all non-Africans. (Villanea and Schraiber, 2019). The genome of the Peştera cu Oase Manot 1 is similar in respect to qualitative traits and ectocranial hominin (42-37ka) also documents an admixture with Neanderthals shape to Upper Paleolithic and recent crania. It is different from most only four to six generations back, and thus additional episodes of in- early Homo sapiens. terbreeding (Fu et al., 2015). Manot 1 has reached an endocranial shape close to Upper Manot 1 is currently the best fossil evidence that modern humans Paleolithic and present-day humans but is deviating to a certain extent and Neanderthals lived in close temporal and spatial proximity in the from these populations and not included in their distribution which Levant. It is during this period when a potential pulse of admixture may might indicate that the evolution of modern globulariza- have occurred. Manot 1 could potentially represent a hybrid between tion was not yet completed. Neanderthals and modern humans and also be ancestral to the first Both modern humans and Neanderthals (e.g. Kebara, Amud)

8 G.W. Weber, et al. Quaternary International xxx (xxxx) xxx–xxx contemporaneously inhabited the Levant during the Middle to Upper in lowland tropical Southeast Asia: the antiquity and behavior of anatomically Paleolithic interface. Genetic studies suggest that interbreeding oc- modern humans at Niah Cave (Sarawak, Borneo). J. Hum. Evol. 52, 243–261. Barzilai, O., Hershkovitz, I., Marder, O., 2016. The Early Upper Paleolithic period at curred between 60 and 50ka. Manot 1 could potentially represent a Manot Cave, western Galilee, Israel. Hum. Evol. 31 (1–2), 85–100. hybrid between modern humans and Neanderthals, but , based on our Barzilai, O., Hershkovitz, I., Marder, O., Ayalon, A., Bar-Matthews, M., Bar-Oz, G., data, we can neither reject nor prove this hypothesis. Chronologically Boaretto, E., Berna, F., Frumkin, A., Khalaily, H., Weiner, S., Yeshurun, R., 2012. fi Manot cave. Hadashot Arkheologiot 124. younger ndings from the Early Upper Paleolithic period at Manot Cave Benazzi, S., Douka, K., Fornai, C., Bauer, C.C., Kullmer, O., Svoboda, J., Pap, I., Mallegni, might be indicative of variable genetic modern human and Neanderthal F., Bayle, P., Coquerelle, M., Condemi, S., Ronchitelli, A., Harvati, K., Weber, G.W., contributions to the Manot population. 2011. Early dispersal of modern humans in Europe and implications for Neanderthal – Manot 1 could have been a direct descendent of early Homo sapiens behaviour. 479, 525 528. Blinkhorn, J., Achyuthan, H., Ditchfield, P., Petraglia, M., 2017. Palaeoenvironmental in the Levant (Qafzeh, Skhul). The absence of hominin fossils between dynamics and palaeolithic occupation at katoati, Thar desert, India. Quat. Res. 87, the times of Qafzeh/Skhul and Manot, however, is not supportive for 298–313. the hypothesis of a continuous habitation and/or local evolution in the Bookstein, F.L., 1997. 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Palaeohydrological corridors for hominin dispersals in the ~250- Declaration of competing interest 70,000 years ago. Quat. Sci. Rev. 144, 155–185. Cabrera, V.M., Marrero, P., Abu-Amero, K.K., Larruga, J.M., 2018. Carriers of mi- tochondrial DNA macrohaplogroup L3 basal lineages migrated back to Africa from There are no relationships that could give rise to conflicts of in- Asia around 70,000 years ago. BMC Evol. Biol. 18. terest. Clarkson, C., Jacobs, Z., Marwick, B., Fullagar, R., Wallis, L., Smith, M., Roberts, R.G., Gerhard Weber for all authors. Hayes, E., Lowe, K., Carah, X., Florin, S.A., McNeil, J., Cox, D., Arnold, L.J., Hua, Q., Huntley, J., Brand, H.E.A., Manne, T., Fairbairn, A., Shulmeister, J., Lyle, L., Salinas, M., Page, M., Connell, K., Park, G., Norman, K., Murphy, T., Pardoe, C., 2017. Human Acknowledgements occupation of northern Australia by 65,000 years ago. Nature 547, 306–310. Dean, D., Hublin, J.J., Holloway, R., Ziegler, R., 1998. On the phylogenetic position of the pre- specimen from Reilingen, Germany. J. Hum. Evol. 34, 485–508. The excavation at Manot Cave was initiated and supported de Lumley, M.A., 2019. Les Restes Humains Anténéanderthaliens Apidima 1 et Apidima 2. throughout the years by the late D. David, founder of the ‘Dan David CNRS Editions EAN 9782271126351. Prize’, and his son A. David. The ongoing research is financially sup- Demeter, F., Shackelford, L.L., Bacon, A.M., Duringer, P., Westaway, K., Sayavongkhamdy, T., , J., Sichanthongtip, P., Khamdalavong, P., Ponche, J.L., ported by the Dan David Foundation, the Israel Antiquities Authority, Wang, H., Lundstrom, C., Patole-Edoumba, E., Karpoff, A.M., 2012. Anatomically Case Western Reserve University, the Shafran Family Foundation, the modern human in Southeast Asia (Laos) by 46 ka. Proc. Natl. Acad. Sci. U. S. A 109, Leakey Foundation, the Irene Levi Sala CARE Archaeological 14375–14380. Détroit, F., Mijares, A.S., Corny, J., Daver, G., Zanolli, C., Dizon, E., Robles, E., Grün, R., Foundation, the Keren Kayemet L'Israel, Binational Foundation Piper, P.J., 2019. A new species of Homo from the of the . (grant no. 2015303), and the Israel Science Foundation (grant no. Nature 568, 181–186. 2632/18). We thank all the team members and researches that colla- Douka, K., Slon, V., Jacobs, Z., Ramsey, C.B., Shunkov, M.V., Derevianko, A.P., Mafessoni, F., Kozlikin, M.B., Li, B., Grün, R., Comeskey, D., Devièse, T., Brown, S., Viola, B., borated in the excavation. research has been sup- Kinsley, L., Buckley, M., Meyer, M., Roberts, R.G., Pääbo, S., Kelso, J., Higham, T., ported by the Binational Science Foundation (grant no. 2632/18), the 2019. Age estimates for hominin fossils and the onset of the upper palaeolithic at Exilarch's Foundation and the Max Planck Society–Weizman Institute . Nature 565, 640–644. Joint Center for Integrative and Anthropology. 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