Journal of Human Evolution 59 (2010) 445e464
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Journal of Human Evolution
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Evolution of middle-late Pleistocene human cranio-facial form: A 3-D approach
Katerina Harvati a,b,*, Jean-Jacques Hublin b, Philipp Gunz b a Paleoanthropology Section, Department of Early Prehistory and Quaternary Ecology and Senckenberg Center for Human Evolution and Paleoecology, Eberhard Karls Universität Tübingen, Rümelinstr. 23, 72070 Tübingen, Baden-Württenberg, Germany b Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Germany article info abstract
Article history: The classification and phylogenetic relationships of the middle Pleistocene human fossil record remains Received 18 March 2008 one of the most intractable problems in paleoanthropology. Several authors have noted broad resem- Accepted 8 April 2010 blances between European and African fossils from this period, suggesting a single taxon ancestral to both modern humans and Neanderthals. Others point out ‘incipient’ Neanderthal features in the Keywords: morphology of the European sample and have argued for their inclusion in the Neanderthal lineage Homo heidelbergensis exclusively, following a model of accretionary evolution of Neanderthals. We approach these questions Neanderthal using geometric morphometric methods which allow the intuitive visualization and quantification of Geometric morphometrics Temporal features previously described qualitatively. We apply these techniques to evaluate proposed cranio-facial ‘ ’ Occipital incipient facial, vault, and basicranial traits in a middle-late Pleistocene European hominin sample when Face compared to a sample of the same time depth from Africa. Some of the features examined followed the predictions of the accretion model and relate the middle Pleistocene European material to the later Neanderthals. However, although our analysis showed a clear separation between Neanderthals and early/recent modern humans and morphological proximity between European specimens from OIS 7 to 3, it also shows that the European hominins from the first half of the middle Pleistocene still shared most of their cranio-facial architecture with their African contemporaries. Ó 2010 Elsevier Ltd. All rights reserved.
Introduction In the last few decades evidence has mounted for a recent, African origin for modern humans (e.g., Cann et al., 1987; The classification and phylogeny of middle Pleistocene humans Harpending and Relethford, 1997; Harpending et al., 1998; White is one of the most debated subjects in paleoanthropology today and et al., 2003; McDougal et al., 2005; Grine et al., 2007), pointing to remains unresolved despite intense discussion. The specimens that the exclusion of Neanderthals from the direct ancestry of our belong to this group show a mosaic of ancestral, Homo erectus-like species. At the same time several studies have highlighted the traits and derived features of later Homo. In the past they were magnitude of morphological and genetic differences between commonly assigned to ‘archaic Homo sapiens,’ together with Neanderthals and modern humans (e.g., Hublin, 1978, 1988; Santa Neanderthals and other middle-late Pleistocene human forms Luca, 1978; Stringer and Andrews, 1988; Schwartz and Tattersall, (Bräuer, 1981, 1984; Stringer et al., 1984; see also Bräuer [2008] for 1996a,b; Krings et al., 1997; Ponce de León and Zollikofer, 2001; a recent defense of this perspective). In this view, middle Pleisto- Lieberman et al., 2002; Bruner et al., 2003, 2004; Harvati, cene humans, including Neanderthals, were loosely considered as 2003a,b; Harvati et al., 2004, 2007; Bailey and Lynch, 2005; ancestral, ‘archaic’ forms, belonging to our own species (rather than Bailey, 2006; Noonan et al., 2006; Bastir et al., 2007, 2008; Green to H. erectus) but retaining many plesiomorphic, H. erectus-like et al., 2008). The classification of Neanderthals as ‘archaic H. features. They were grouped together based on what was perceived sapiens’ therefore appears increasingly untenable, with many to be a similar level of adaptation, or ‘grade.’ This grade classifica- researchers favoring their assignment to a distinct species, Homo tion of ‘archaic H. sapiens’ acknowledged affinities with later Homo neanderthalensis. In this new configuration, the grade classification but did not confront the thorny issue of the phylogenetic rela- of earlier middle Pleistocene humans has become problematic. tionships and alpha taxonomy of these specimens. Nonetheless, the difficulty in classifying this ‘muddle in the middle’ remains, and stems in part from the mosaic nature of their morphology, which shows a combination of plesiomorphic H. * Corresponding author. erectus features and derived later Homo traits (see above), but not E-mail address: [email protected] (K. Harvati). easily defined autapomorphies.
0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.06.005 446 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464
Currently, two main views dominate the discussion on this relationships. Such methods are often characterized as phenetic, in stage in human evolution. The first of these sees the middle contrast to trait-based, phylogenetically-minded cladistic Pleistocene human fossil record as comprising a single, cross- approaches. In this context, 3-D geometric morphometric methods continental taxon, spanning both Africa and Europe (and possibly (see below) provide an opportunity for bridging the wide gap also Asia), Homo heidelbergensis, deemed the last common between these two methodologies by extending quantification to ancestor to both Neanderthals and modern humans. This stance features that are difficult to capture using traditional caliper stems from the perceived strong morphological and morpho- measurements. The quantification of several features previously metric similarities between the European and African specimens, scored as discrete traits and their statistical analysis, therefore, often based on metric analyses of the fossil record (e.g., Stringer, should help resolve debate stemming from the use of incompat- 1974, 1983; Arsuaga et al., 1997; Rightmire, 1998, 2007, 2008; ible methods among paleoanthropologists. Mounier et al., 2009). Some researchers, however, have Here we assess quantitatively the patterns of variation and the described the European portion of this record as showing ‘incip- polarity of some of the most widely discussed Neanderthal lineage ient’ Neanderthal cranial features, including discrete and not cranio-facial features in the context of the accretion model using easily quantifiable facial, neurocranial, and basicranial traits, to a large sample of fossil hominins and taking into account recent various degrees (e.g., Arsuaga et al., 1997; Martínez and Arsuaga, advances in the dating of crucial specimens. The features studied 1997; Dean et al., 1998; Hublin, 1998; Stringer and Hublin, 1999). include facial, neurocranial, and basicranial traits that are measured Neanderthal-like morphology has also been described in middle and analyzed with the methods of three-dimensional geometric Pleistocene European mandibular specimens (e.g., Rosas, 1995, morphometrics. These techniques preserve the geometry of the 2001; Rosas and Bermudez de Castro, 1998;butseeMounier object studied better than traditional measurements, enable the et al., 2009 for a contrasting interpretation), dental remains identification of landmarks where shape differences occur and the (Bermúdez de Castro, 1988; Bailey, 2006; Martinón-Torres et al., relative levels of difference at each landmark after size has been 2006; Gómez-Robles et al., 2007, 2008), and some postcranial accounted for, and readily provide illustrations of the shape elements (Carretero et al., 1997; Gómez-Olivencia et al., 2007). changes between specimens (Rohlf and Marcus, 1993; O’Higgins, On the basis of this evidence, current consensus sees a distinct 2000). Perhaps their greatest advantage is that they provide European lineage leading from the middle Pleistocene European a way of quantifying shape differences of traits which are difficult to forms to Neanderthals and separate from that which evolved into measure with linear or angular measurements and are therefore modern humans, probably in Africa. Usually this process is thought usually described qualitatively rather than quantitatively (e.g., to have occurred in a gradual, anagenetic manner, according to the Dean, 1993; Harvati, 2003a; Nicholson and Harvati, 2006; Gunz and ‘accretion’ hypothesis (Dean et al., 1998; Hublin, 1998, 2009). Harvati, 2007; Harvati, 2009a,b). The latter aspect of this method- Following this position, most European middle Pleistocene forms ology is critical for our goal, as several of the features we examine are recognized as ancestral to Neanderthals (but not modern are difficult to capture with traditional metric approaches and are humans) and should be classified either as H. neanderthalensis therefore usually described qualitatively. Our approach therefore (Hublin, 1998, 2009) or as exclusively European H. heidelbergensis, combines the quantitative evaluation of features with a metric a chronospecies of the Neanderthal lineage (e.g., Arsuaga et al., analysis of overall cranial morphological variation. 1997; Manzi, 2004; but see Wolpoff et al., 1994; Rosas et al., 2006; Tattersall and Schwartz, 2006; and Bräuer, 2008 for alter- Materials and methods native interpretations of the fossil record). Their African counter- parts, commonly thought to be ancestral to our own lineage, would Samples then be classified as a different taxon, possibly Homo rhodesiensis (Hublin, 2009). In this case, the common ancestor of Neanderthals A large fossil sample was included, comprising several Nean- and modern humans would have to be an older taxon, H. erectus, derthal, European (MPE), and African middle Pleistocene (MPA) Homo antecessor (Bermúdez de Castro et al., 1997), or Homo fossils, late middle-late Pleistocene African specimens (LPA), Upper mauritanicus (Hublin, 2001). Paleolithic Europeans (UPE), and two early African H. erectus (s.l.) Despite the body of evidence supporting this view, the vari- (ER) individuals (Table 1). Although their chronology is often poorly ability and polarity of some of the discussed features are not fully resolved, the European fossils were further subdivided according to understood. While in many instances European middle Pleistocene the accretion model into four steps, from early pre-Neanderthals samples are relatively large, their African counterparts tend to be (MPE Step 1) to classic Neanderthals (Neanderthal Step 4), much more limited or less accessible for study. This is a particular according to rough chronological order (Table 2). We also used problem with the dental evidence, where African samples are a large comparative recent human sample, comprising seven several times smaller than those available from Europe (e.g., widely defined geographical populations (African, Andamanese, Bailey, 2006; Martinón-Torres et al., 2007). Interpretation is also Asian, Khoesan, North America, W. Eurasia, Oceania). Only adults influenced by the fossil samples available for study to each were included, as determined by a fully erupted permanent researcher. Matters are further complicated by the use of different dentition. Since sex assignment is imperfect for recent humans and methodologies by different researchers. Scoring of discrete traits is even more problematic for fossil specimens, sexes were pooled in often used for aspects of morphology that are difficult to measure the analysis. Where original fossils were not available, we but are nonetheless perceived as evolutionarily significant. This measured research quality casts or stereolithographs from the approach has the advantage that it can take into account small, Division of Anthropology, American Museum of Natural History distinct features that may or may not be translatable into (New York) and from the Department of Human Evolution, Max measurements. It can, however, be affected by subjectivity and Planck Institute for Evolutionary Anthropology, Leipzig. All reduced repeatability. Quantitative methods relying on continuous measurements were collected by one observer (KH). measurements, on the other hand, are usually thought to be more rigorous, objective, and repeatable. However, they are criticized for Data collection generally being limited to larger-scale morphology and for thus entirely missing features which cannot be quantified but are Data were collected in the form of three-dimensional coordi- nonetheless critical in the understanding of evolutionary nates of osteometric landmarks, defined as homologous points that K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 447
Table 1 Table 2 Fossil comparative samples used in the analysis Chronology of the specimens used in the analyses
African Homo erectus (s.l.) Specimen Chronology Face: KNM-ER 3733 (3733) African H. erectus (s.l.) Temporal: KNM-ER 3733 (3733), 3883 (3883) OH 9 (OH), KNM-ER 3733 1.75 Ma (Feibel et al., 1989) KNM-WT 15000 (WT) KNM-ER 3883 1.5 Ma (Feibel et al., 1989) Posterior vault: KNM-ER 3733 (3733) 3883 (3883) OH 9 ca. 1.2 Ma (Klein, 1999) Step 1: Middle Pleistocene European hominins KNM-WT 15000 ca. 1.5 Ma (Klein, 1999) a a Face: Arago 21 (Ar), Petralona (Pe), Sima de los Huesos Cranium 5 (Sm) Step 1: Middle Pleistocene European hominins a Temporal: Ceprano (Ce), Sima de los Huesos Cranium 5 (Sm) Arago 21 600e>350 ka (de Lumley and a Posterior vault: Petralona (Pe), Sima de los Huesos Cranium 5 (Sm) de Lumley, 1973; Cook et al., 1982; Step 2: Middle Pleistocene European hominins Falguères et al., 2004) Temporal: Steinheim (St), Reilingen (Re) Ceprano ca. 450 ka (Muttoni et al., 2009) e Posterior vault: Steinheim (St), Reilingen (Re), Swanscombea (Sw) Petralona 670 ca. 250 ka (Harvati et al., 2009) Sima de los Huesos Cranium 5 ca. 530 ka (Bischoff et al., 2007) Step 3: Early Neanderthals Temporal: Krapina 3, 39-1 (Kr3, Kr39-1) Saccopastore 2 (Sc2) Step 2: Middle Pleistocene European hominins e Posterior vault: Biache-St-Vaast (Bc), Tabun C1 (Tb), Saccopastore 1 (Sc1) Reilingen Holstein Late Würm (Ziegler and Dean, 1998). Step 4: Classic Neanderthals Steinheim 500e200 ka (Cook et al., 1982; Face: Gibraltar 1 (Gb), Guattari (Gt), La Chapelle-aux-Saints (Ch), La Ferrassie Klein, 1999) a a 1 (Fr1), Shanidar 1 ,5 (Sh1, Sh5) Swanscombe ca. 400 ka (Stringer and Temporal: Amud 1 (Am), Gibraltar 1 (Gb), Guattari (Gt), La Hublin, 1999) Chapelle-aux-Saints (Ch), La Ferrassie 1, 2 (Fr1, Fr2), La Quina 5, 27 (Qn5, Qn27), Shanidar 1a (Sh1), Spy 1, 2 (Sp1, Sp2) Step 3: Early Neanderthals Posterior vault: Amud 1 (Am), Feldhofer 1a (Fd), Guattari (Gt), La Biache-St-Vaast Late stage 7 (Roebroeks and Chapelle-aux-Saints (Ch), La Ferrassie 1 (Fr1), La Quina 5 (Qn5), Tuffreau, 1999) e Shanidar 1a (Sh1), Spy 1, 2 (Sp1, Sp2) Krapina 3, 39-1 140 120 ka (Rink et al., 1995) Saccopastore 1, 2 120 ka (Manzi et al., 2001) Middle Pleistocene African hominins Tabun C1 135e100 ka (Grün et al., 2005) Face: Bodo (Bd), Kabwe (Kb) Temporal: Kabwe (Kb), Ndutu (Nd) Step 4: Classic Neanderthals Posterior vault: Kabwe (Kb) Saldhana (Sl) Amud 1 ca. 50 ka (Rink et al., 2001) Feldhofer 1 ca. 40 ka (Schmitz et al., 2002) Late middle-late Pleistocene African hominins Gibraltar 71 to 50e35 ka (Klein, 1999) Face: Irhoud 1 (Ir1) Guattari ca. 50 ka (Schwarcz et al., 1991) Temporal: Eliye Springs (ES), Omo 1 (Om1), Singa (Sg), Ngaloba (LH) La Chapelle-aux-Saints 56e47 ka (Grün and Posterior vault: Aduma (Ad), Eliye Springs (ES), Irhoud 1, 2 (Ir1, Ir2), Stringer, 1991) Ngaloba (LH), Omo 1, 2 (Om1, Om2), Singa (Sg) La Ferrassie 1, 2 71 to 50e35 ka (Klein, 1999) La Quina 5, 27 71 to 50e35 ka (Klein, 1999) Early anat. modern humans from the Levant Shanidar 1, 5 ca. 50 ka (Trinkaus, 1983) Face: Skhul 5 (Sk), Qafzeh 6a, 9 (Qz6, Qz9) Spy 1, 2 ca. 36 ka (Semal et al., 2009) Temporal: Skhul 5 (Sk), Qafzeh 9 (Qz9) a Posterior vault: Skhul 5 (Sk), Qafzeh 6 , 9 (Qz6, Qz9) Middle Pleistocene African hominins Bodo ca. 600 ka (Clark et al., 1994) Upper Paleolithic Eurasian modern humans Kabwe Middle Pleistocene Face: Abri Pataud (AP), Chanceladea (Cn), Cro Magnon 1, 2 (CM1, CM2), Dolni (Rightmire, 2009) Vestonice 3, 13, 14, 15, 16 (DV 3, DV 13, DV14, DV15, DV 16), Ein Gev (EG), Ndutu Middle Pleistocene (Klein, 1999) Grimaldia (Gr), Mlade c 1 (Ml1), P redmostí 3a,4a (Pd3, Pd4) Saldhana 1 Mae>600ka (Klein et al., 2006) Temporal: Pataud (AP), Chanceladea (Cn), Cioclovina (Ci), Cro Magnon 1, 2 (CM1), Dolni Vestonice 3, 13, 14, 15, 16 (DV 3, DV 13, DV14, DV15, DV 16), Late middle-late Pleistocene African hominins Ein Gev (EG), Grimaldia (Gr), Mlade c 1, 2, 5 (Ml1, Ml2, Ml5) Ohalo II (Oh), Aduma 105e79 ka (Haile-Selassie Pavlov (Pv), P redmostí 3a,4a (Pd3, Pd4) et al., 2004) Posterior vault: Abri Pataud (AP), Brno 2 (Bn), Chanceladea (Cn), Eliye Springs Late middle-late Pleistocene Cioclovina (Ci), Cro Magnon 1, 2, 3 (CM1, CM2, CM3), Dolni (Klein, 1999) Vestonice 3, 11e12, 13, 14, 15, Irhoud 1,2 ca. 160 ka (Smith et al., 2007) 16 (DV3, DV11, DV13, DV14, DV15, DV 16), Ein Gev (EG), Grimaldia (Gr), Ngaloba ca. 130 ka (Hay, 1987) Mlade c 1, 5, 6 (Ml1, Ml5, Ml6), Ohalo II (Oh), Pavlov (Pv), P redmostí 3a Omo 1, 2 ca. 195 ka (McDougal et al., 2005) 4a (Pd3, Pd4) Singa >130 ka (McDermott et al., 1996) a High-quality casts or stereolithographs were measured for these specimens. Early anat. modern humans from the Levant Qafzeh 6, 9 135e100 ka (Grün et al., 2005) Skhul 5 135e100 ka (Grün et al., 2005) can be reliably and repeatedly located, using a Microscribe Upper Paleolithic Eurasian modern humans Abri Pataud Early Upper Paleolithic (Holt and (Immersion Corp.) portable digitizer (Table 3). These points were Formicola, 2008) chosen so as to quantify Neanderthal features of the face, occipital Chancelade Late Upper Paleolithic (Holt and bone, and basicranium as closely as possible (see below, Table 4). Formicola, 2008) Landmarks were therefore registered on the face, parietal, occipital, Cioclovina ca. 28e29 ka (Holt and Formicola, 2008) and temporal bones. Semilandmarks along the midsagittal profile Cro Magnon 1, 2 27e28 ka (Holt and Formicola, 2008) from bregma to inion and along the lambdoid suture were also Dolni Vestonice 3, 11e12, 13, 14, 15, 16 25e29 ka (Holt and measured (Table 3). In order to maximize the number of specimens Formicola, 2008)) that could be considered for each set of traits, three separate data Ein Gev 1 15e16 ka (Holt and Formicola, 2008) e sets were constructed: a facial, posterior vault, and temporal bone Grimaldi 24 25 ka (Holt and Formicola, 2008) Mlade c 1, 2, 5, 6 ca. 31 ka (Holt and Formicola, 2008) data set. Each includes a different number of fossil specimens (Table Ohalo II 19 ka (Holt and Formicola, 2008) 1) and modern humans (face: 250; temporal bone: 267; posterior Pavlov 1 25e26 ka (Holt and Formicola, 2008) vault: 294). Brno 2 ca. 23 ka (Holt and Formicola, 2008) P redmostí 3, 4 Early Upper Paleolithic (Smith, 1982) 448 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464
Table 3 absence of a canine fossa (see, for example, Bermúdez de Castro Landmarks and semilandmarks used in the analysis et al., 1997)oras‘inflation’ of the maxilla (e.g., Hublin, 1998). In Face landmarks addition to its ‘inflation,’ the infraorbital region of Neanderthals is 1. Glabella (GLA) described as oriented more sagittally than that of modern humans. 2. Post-toral sulcus Minima of concavity on midline Attempts to quantify this feature have relied on measuring the post-toral frontal squama distances between the upper end of the zygomaxillary suture and 3, 4. Mid-orbit torus Superior Right and Left porion and between the lower end of the zygomaxillary suture and Point on superior aspect of porion (e.g., Howells, 1975) or by measuring the area of the triangle supraorbital torus, approximately at the middle of the orbit formed by the two zygomaxillary suture ends and the root of the malar process (Trinkaus and Howells, 1979). More recently, this 5, 6. Mid-orbit torus Inferior Right and Left area has been measured using 3-D surface semilandmarks Point on inferior margin of supraobrital torus, approximately (Maddux and Franciscus, 2009; Freidline et al., 2010). Here we use at the middle of the orbit the infraorbital foramen landmark as an indicator of the position of 7. Nasion the infra-orbital plate relative to other facial landmarks, including 8, 9. Dacryon Right, Left those on the zygomaxillary upper and lower end points and on the 10. Rhinion 11, 12. Alare Right Left malar root; we are thus able to quantitatively assess the degree of 13,14. Zygoorbitale Right Left forward placement of the infra-orbital plate and its orientation 15, 16. Zygomaxillare Right Left relative to other facial landmarks, including ones that are more 17, 18. Infraorbital foramen Right, Left medially as well as more laterally placed than the infraorbital 19, 20. Frontomalare Orbitale Right, Left foramen point. 21, 22. Frontomalare Temporale Right, Left 23. Nasospinale 2. The degree of anteroinferior projection of glabella relative to 24. Prosthion the browridge. This condition is proposed by Dean et al. (1998) to 25, 26. Zygo-temporal suture inferior Right, Left characterize pre-Neanderthals relative to early Neanderthals. The 27, 28. Malar root Right, Left anterior projection of the supraorbital torus is difficult to measure, 29, 30 Jugale Right, Left and in the past it has been scored (e.g., Sládek et al., 2002), or Temporal bone landmarks measured linearly, as chords from the most anterior endocranial 1. Asterion margin of the frontal just above the orbital roof to the most anterior 2. Porion 3. Auriculare point of the supraorbital torus at the same level (Smith and 4. Parietal Notch Raynard, 1980). We were able to evaluate this feature through the 5. Mastoidiale position of glabella relative to the lateral landmarks digitized on the 6. Most inferior point on the juxtamastoid crest (following Hublin, 1978) supraorbital torus. 7. Deepest point of the lateral margin of the articular eminence 3. The relatively forward position and sagittal orientation of the 8. Most inferior point on the entoglenoid process face. This is a proposed Neanderthal autapomorphy, perhaps Posterior vault landmarks related to and building on the morphology of the infraorbital 31. Bregma ‘ 32. Lambda (LBD) region. It is proposed by the accretion model to appear in the pre- 33. Inion (IN) Neanderthal’ (Step 2) stage of Neanderthal evolution. In ‘classic’ 34, 35. Asterion Right, Left (AST) Neanderthal morphology the midface becomes increasingly prog- 36, 37. Parietal Notch Right and Left nathic (see below; Dean et al., 1998; Hublin, 1998). A sagittal 38, 39. Auriculare Right, Left (AUR) orientation of the face has been measured using the distances 40,11. Porion Right, Left (PO) between porion and the lower/upper ends of the zygomaxillary Posterior vault ridge curves suture, or the relationship of the two latter points to the root of the 1. Midsagittal profile 37 semilandmarks from BRE to IN 2. Lambdoid suture 16 semilandmarks from AST malar process. Here we assess the orientation of the face based on right to LBD to AST Left the relative positions of a total of 30 facial landmarks, which include the malar root and zygomaxillary suture points, as well as midline and lateral landmarks on the face. 4. Strong juxtamastoid eminence. A pronounced juxtamastoid Neanderthal features eminence has been described extensively as a Neanderthal feature (e.g., Vallois, 1969; Hublin, 1978, 1988; Santa Luca, 1978; Harvati, According to the accretion hypothesis, Neanderthal features 2003a). We follow Hublin (1978); see also Harvati [2003a], in our accumulated gradually through time in the European middle and definition of the juxtamastoid eminence as the crest on the medial late Pleistocene human fossil record. Earlier specimens show border of the digastric fossa, formed by the insertion of the digastric ‘incipient’ Neanderthal morphology, while the later ones exhibit muscle on the lateral side, and which can be continuous or to some full-blown ‘classic’ Neanderthal anatomy (e.g., Dean et al., 1998; extent merge with the line formed by the attachment of the Hublin, 1998). We focused on eight such features, which we superior oblique muscle postero-medially. This trait is proposed to aimed to capture by our landmark and semilandmark data sets. appear in the early part of the middle Pleistocene (Step 2 of the 1. The shape and orientation of the infraorbital region. The accretion process) and to become fully established among early ‘inflated’ morphology of the infra-orbital plate is among the most Neanderthals (Step 3; Dean et al., 1998; Hublin, 1998). The promi- characteristic features of classic Neanderthal anatomy and has been nence of the juxtamastoid eminence is difficult to quantify and is implicated in functional models of Neanderthal evolution (e.g., Rak, usually scored, with the exception of geometric morphometric 1986; Trinkaus, 1987). This trait is thought to be among those analyses (Harvati, 2003a). We use a similar landmark data set as appearing ‘incipiently’ in the early stages of Neanderthal evolution that employed by Harvati (2003a) to quantify the morphology of according to the accretion model and to be foreshadowed in the juxtamastoid eminence. specimens like Petralona and Arago 21 (Dean et al., 1998; Hublin, 5. Occipital plane convexity, also described as the ‘occipital bun.’ 1998). This trait is difficult to capture with traditional caliper This feature has been frequently described as a Neanderthal trait measurements and is often described in terms of presence or (Thoma, 1965; Hublin, 1988; Lieberman, 1995) and is usually K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 449
Table 4 List of European lineage derived traits and specimens thought to exhibit them reproduced from Dean et al. (1998),a
European Derived Features Landmarks/semilandmarks Specimens Accretion Step 1 Convex and receding horizontal Infraorbital foramina (pts. 17e18) relative Arago, Atapuerca SH, Petralona infraorbital profile to inferior orbital margin (pts 13e14) and Wide occipital torus zygomaxillary points (pts. 15e16, 25e26, 29e30) Accretion Step 2 Bilaterally protruding occipital torus Juxtamastoid point relative to porion, parietal Supra-iniac fossa (incipient to well defined) notch and other temporal bone landmarks Strong juxtamastoid eminence Styloid process not aligned with the stylomastoid foramen and the digastric groove Incipient ‘‘en bombe’’ Increased occipital plane convexity Occipital bone semilandmarks, Lateral post-toral sulcus deepens inferiorly midsagittal profile Glabella moves anteroinferiorly Glabella (pt. 1) relative to supraorbital torus Swanscombe, Steinheim, Reilingen disrupting previously points (pts. 3–4, 5–6) and to frontomalare orbitale horizontal supercilliary ridges (pts. 19–20) and temporale (pts. 20–21) Reduced maxillary buttress Anteriorly advanced and sagittally Midline facial landmarks relative oriented face to the lateral facial and zygomatic landmarks Accretion Step 3 Full supra-iniac fossa Full ‘‘en bombe’’ High occipital plane convexity Occipital bone semilandmarks, midsagittal profile Reduced mastoid process Mastoid point relative to porion, Biache 1, Saccopastore, Krapina, Tabun C parietal notch and other temporal bone landmarks Large juxtamastoid process Juxtamastoid point relative to porion, parietal notch and other temporal bone landmarks Elongate temporal bone Asterion relative to articular eminence points Anterior mastoid tubercle External auditory meatus fully depressed Increased dolichocephaly Accretion Step 4 Exaggerated occipital plane convexity Occipital bone semilandmarks, Supra-iniac fossa midsagittal profile High mid-facial prognathism Rhinion (pt. 10), alare (pts. 11e12) Neanderthal, Spy, Monte Circeo, and nasospinale Gibraltar Forbes Quarry, La (pt. 23) relative to prosthion (pt. 24) Chapelle-aux-Saints, La Quina, La and glabella (pt. 1) Ferrassie Shanidar, Amud Large piriform aperture Rhinion (pt. 10), alare (pts. 11e12) and nasospinale (pt. 23) Rounded circumorbital morphology Post-toral sulcus deepens
a The middle column shows the landmarks and semilandmarks used here to quantify some of these features.
associated with the presence of a depression of the area around (Dean et al., 1998; Hublin, 1998). The interpretation of this feature is lambda (‘‘lambdoid flattening”’) on the occipital and parietal bones, complicated by its implication in sex assignment in modern with a flattened parietal and flat nuchal part of the occipital. humans, and Neanderthals may follow a similar pattern of sexual ‘Bunning’ is expanded laterally in Neanderthals, and its effects can dimorphism (Harvati, 2003a). Different linear measurements (from be observed in both the exterior and interior aspects of the occipital the Frankfurt horizontal plane, from the parietal notch, or from the bone. This morphology is difficult to assess using either traditional floor of the digastric fossa to the tip of the mastoid process) have caliper measurements (Ducros, 1967; Dean et al., 1998; Lieberman been used to capture the height of the mastoid, with conflicting et al., 2000) or landmark-based geometric morphometrics results (e.g., Vandermeersch, 1981; Trinkaus, 1983; Martínez and methods (Yaroch, 1996; Harvati, 2001). Bunning is therefore usually Arsuaga, 1997). Here we follow Harvati (2003a) in using described qualitatively but has previously been quantified using a temporal bone data set that includes the tip of the mastoid semilandmark outline analysis (Reddy et al., 2005; Gunz and process as a landmark, whose position relative to other temporal Harvati, 2007). In order to assess this morphology we use bone landmarks including porion and the juxtamastoid eminence a similar data set as that used by Gunz and Harvati (2007), which can be used to assess the relative mastoid process height. includes the semilandmark outline of the midsaggital profile of the 7. High mid-facial prognathism. A pronounced forward position squamous part of the occipital bone in combination with occipital of the midface is one of the most frequently discussed distinctive bone landmarks. aspects of Neanderthal cranial morphology (e.g., Boule, 1911e1913; 6. Reduced mastoid process. The small size of the Neanderthal Howells, 1975; Rak, 1986; Trinkaus, 1987; Frayer, 1992). Although mastoid process, usually in combination with a large juxtamastoid Step 2 specimens of the accretionary process are thought to show eminence, is considered a derived feature of Neanderthals (Vallois, a degree of relatively anterior placement of the face, a strong degree 1969; Hublin, 1978, 1988; Santa Luca, 1978; Stringer et al., 1984; of mid-facial prognathism characterizes the classic Neanderthals Harvati, 2003a). A small mastoid process is described as first (Step 4; Dean et al., 1998; Hublin, 1998). A variety of angular and appearing with early Neanderthals (Step 3) of the accretion model combined linear measurements have been used to try and capture 450 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 this morphology, including the zygomaxillary angle, the naso- relaxation’). Spline relaxation removes the effects of ‘digitizing frontal angle, the difference between the distances from the error’ in the tangent direction that results from the practical transmeatal axis to the mesial edge of alveolus of upper M1 and to necessity of having to place the semilandmarks somewhere along the lower end of zygomaxillary suture, and the difference between the curves. After relaxation semilandmarks can be treated in the subspinale and zygomaxillare radii (Howells, 1973; Stringer, multivariate analyses as if they had been homologous points in the 1974). Here the degree of mid-facial prognathism is evaluated first place because after spline relaxation they are geometrically through the position of nasion, rhinion, and nasospinale relative to corresponding points across the sample (e.g., Gunz and Harvati, the other midline and lateral facial landmarks, including the 2007; Harvati et al., 2007). All landmark and semilandmark pre- zygomaxillary and malar root landmarks. processing was done in Mathematica (Wolfram Research, Inc., 8. Large piriform aperture. A very large nasal aperture charac- 2007). The landmarks and slid semilandmarks were then super- terizes Neanderthals, a feature that may be related to their imposed with Generalized Procrustes Analysis (GPA; Rohlf, 1990; pronounced mid-facial prognathism and infra-orbital plate Rohlf and Marcus, 1993; Slice, 1996; O’Higgins and Jones, 1998) morphology (e.g., Rak, 1986; Trinkaus, 1987; Schwartz and using the Morpheus software package (Slice, 1998). This procedure Tattersall, 1996a). According to the accretion model, this feature allowed the visual and statistical assessment of shape after scaling appeared late in Neanderthal evolution in Step 4, ‘classic’ Nean- to common centroid size. derthal specimens (Dean et al., 1998). The size of the nasal aperture can be measured using linear measurements such as rhinion to Analysis nasospinale for quantifying height, and alare right to alare left for quantifying width. These four osteometric landmarks are included In order to evaluate the overall shape as well as the individual in our facial data set, and their relative position is used to assess the traits after removal of size differences, the mean configurations of relative size of the nasal opening. taxa were calculated and compared to each other using Morpheus (Slice, 1998). The shape of each feature was evaluated visually (after Missing data reconstruction scaling). For features thought to develop early on (i.e., Stages 1 and 2 of the accretion process as described in Table 4), the European Since morphometric analyses do not accommodate missing middle Pleistocene mean configuration should be more similar to data, some level of data reconstruction was necessary. Landmarks the Neanderthal mean configuration in these traits than it is to the on specimens with minimal damage were estimated during data African middle Pleistocene mean configuration. For traits thought collection using anatomical clues from the preserved surrounding to have developed later on in the Neanderthal lineage (Stages 3 and areas (e.g., the infraorbital foramen landmarks in KNM-ER 3733). 4ofTable 4), Neanderthals should differ both from middle Pleis- Missing landmarks were further reconstructed by superimposing tocene specimens (either African or European) and from later- the landmark configurations of specimens with missing data with Pleistocene African and Levantine specimens. their reflections and by substituting the coordinates for each Additionally, the shape coordinates were analyzed statistically missing landmark with the fitted homologous counterpart on the using principal components analysis (PCA) in order to explore the other side (reflected relabellingdMardia and Bookstein, 2000). partitioning of variation across samples, and inter-individual as This procedure introduces only minimal levels of error (Harvati, well as inter-group Procrustes distances. As PC axes hardly ever 2003b). The whole face of Arago 21, including the midline, is correspond to biological factors we do not interpret individual PC deformed by what appears to be an almost uniform shear. We axes as if they were biologically meaningful variables. Rather we therefore removed the effects of this distortion by symmetrizing use the PCA as an ordination technique to explore large-scale the cranium using the method of reflected relabelling described in trends within the data. These statistics were calculated with the Gunz (2005) and Gunz et al. (2009a). One reflects the landmarks software packages SAS (SAS Institute, 1999e2001), tps (Rohlf, along any axis while swapping the labels (labels of left and right 2003), and R (R Development Core Team, 2007). The similarity landmarks are interchanged); then these two configurations are among individual specimens was evaluated by their position in the superimposed with a Procrustes fit based on the non-missing PCA but also by inter-individual Procrustes distances. Similarity landmarks (Mardia and Bookstein, 2000); the average of these among pre-defined groups was evaluated by Procrustes distances superimposed forms is then perfectly symmetrical. Gunz et al. among the sample mean configurations. These distances were (2009a) have shown that in the presence of relatively small affine plotted in a neighbor joining tree using African H. erectus (s.l.) as the deformations, this is an adequate method for restoring symmetry. outgroup, calculated in NTSYSpc (Rolf, 1986e2000). It should be Further data reconstruction was allowed in the case of LH 18, noted that the Procrustes metric by which we quantify shape a crucial specimen with only minimal damage (missing frontoma- differences between specimens is an overall measure of similarity lare temporale on both sides). These points were estimated by based on all measured landmarks and semilandmarks and has no minimizing the bending energy of the thin-plate spline between a priori assumptions about the value of particular discrete shape the incomplete specimen and the sample Procrustes average, features (Gunz et al., 2009b). following Gunz (2005), Gunz and Harvati (2007), Gunz et al. (2009a,b) and Grine et al. (2010). Results
Data processing Comparisons of mean configurations
All semilandmarks were iteratively allowed to slide along their 1. Convex and receding horizontal infraorbital profile: This curve to minimize the bending energy of the thin-plate spline feature is reflected here in the relative position of the interpolation function computed between each specimen and the infraorbital foramina, zygoorbitale, zygomaxillare, jugale, and sample Procrustes average (Bookstein, 1997; Gunz et al., 2005; zygo-temporal suture landmarks. A comparison of the classic Gunz and Harvati, 2007). This allows points to slide along (Step 4) Neanderthal mean configuration superimposed with tangents to the curve, approximated for each semilandmark by the the mean modern human configuration (Fig. 1A) clearly vector between the two neighboring points. Missing points were shows a more convex maxilla in the former (infraorbital allowed to slide without constraining them to a curve (‘full foramen forward placed relative to the inferior orbital K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 451
margin) and a receding, more sagittally oriented infraorbital profile (more postero-medially placed zygomaxillare, jugale, and zygo-temporal suture, more anteriorly placed malar root). Similar differences are observed between the Nean- derthal mean configuration and the African H. erectus (s.l.) configuration (Fig. 1B), represented by KNM-ER 3733. Step 4 Neanderthals show a greater convexity of the infraorbital plane, reflected here mainly in a more posterior placement of the inferior orbital margin, while H. erectus shows a more or less flat infraorbital region (different also from the concave condition shown by modern humans). Note that the mean shapes in Figure 1 and the subsequent figures are in Procrustes orientation as 3-D thin-plate splines are hard to interpret on paper. When the European middle Pleistocene mean configura- tion is compared with the mean configuration of the African specimens, the two are nearly indistinguishable in both the forward position of their infraorbital foramina relative to the inferior orbital margin and in their relatively anterior place- ment of the malar root compared to the zygomatic landmarks (Fig. 1E). Both are similar in these features to the classic Neanderthal mean configuration, though not as extreme. Irhoud 1 and the mean configuration of the Qafzeh-Skhul sample differs from Neanderthals in the posterior placement of its infraorbital foramina, suggesting a flat or concave infra- orbital plate, the anterior and antero-lateral placement of zygomaxillare, jugale, and zygo-temporal suture, and the malar root point in the same vertical plane as zygomaxillare. 2. Glabella moves anteroinferiorly disrupting previously hori- zontal supercilliary ridges: This feature is proposed to have appeared relatively early on in the European fossil record (Step 2 of the accretion process as suggested by Dean et al.,1998, who included the Sima de los Huesos in that chronological category based on earlier geological age estimates for this site). It is best appreciated in the superior and lateral views. Again, when compared to the African H. erectus (s.l.) and to modern humans, classic Neanderthals have a forward and inferiorly placed glabella, resulting in a supraorbital region that recedes poste- riorly on either side and is no longer horizontally oriented (Fig. 1AeB). Both the European and African middle Pleistocene mean configurations are very similar to that of Neanderthals in the position of glabella relative to the superior mid-orbital torus landmarks (Fig. 1CeD). The African middle Pleistocene configuration shows an even more anteriorly and inferiorly placed glabella relative to the supraorbital torus than do the Neanderthals. The late middle-late Pleistocene specimen Irhoud 1 and the mean configuration of the early anatomically modern human sample from Skhul and Qafzeh both also show an anteroinferiorly displaced glabella relative to the mid- orbital torus landmarks when compared to the African H. erectus (s.l.) and to modern humans. They are similar in this respect to the middle Pleistocene humans and to Neanderthals. 3. Anteriorly advanced and sagittally oriented face: This trait is assessed by examining the position of the midline facial land- marks relative to the lateral facial and zygomatic landmarks. The Neanderthal mean configuration shows a forward placement of Fig. 1. Superimposed mean configurations of fossil samples, facial data set. A. Step 4 all midline landmarks when compared to the modern Neanderthals (red stars) and Modern humans (blue dots). B. Step 4 Neanderthals (red stars) and African H. erectus (s.l.) (black dots). C. Step 4 Neanderthals (red stars) human (except the post-toral sulcus point) and the African and European middle Pleistocene Step 1 specimens (red open squares). D. Step 4 H. erectus (s.l.) (except prosthion) mean configurations Neanderthals (red stars) and African middle Pleistocene specimens (blue open (Fig. 1AeB). It is also narrower and more sagittally oriented, as squares). E. European middle Pleistocene Step 1 specimens (red open squares) and revealed by the more medial and posterior placement of the African middle Pleistocene specimens (blue open squares).(For interpretation of the fi lateral landmarks (zygomaxillare, jugale, zygo-temporal suture, references to color in this gure legend, the reader is referred to the web version of this article.) frontomalare temporale) and the intermediate position of the infraorbital foramen and malar root points. This configuration 452 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464
results in a narrower, ‘backward’ sloping and sagittally oriented (Fig. 2AeB), the Neanderthal temporal bone mean configura- face. tion shows a much larger and medially placed juxtamastoid The European and African middle Pleistocene mean configu- eminence, which is nearly equal in size to the reduced Nean- rations approach the Neanderthal condition in these respects to derthal mastoid process (see below). All of the European pre- a nearly equal degree (Fig. 1CeE). Their faces are less anteriorly Neanderthal specimens, including the Step 1 sample, show placed than the mean Neanderthal configuration, and they are more inferiorly placed (but not necessarily more medial) jux- nearly identical to each other in this respect. The European tamastoid eminences than their African contemporaries, sample shows a somewhat more posterior (although also more though smaller than the classic Neanderthal mean configura- lateral) placement of zygomaxillare, perhaps suggesting a more tion. The mean configurations of early (Step 3) and classic (Step sagittally oriented face than that of their African counterparts. 4) Neanderthals are very similar in this respect (Fig. 2CeH). The one late middle-late Pleistocene African specimen (Jebel 5. Increased occipital plane convexity: When the classic Nean- Irhoud 1) and the Skhul-Qafzeh mean configuration differ from derthal mean configuration of the posterior vault is compared Neanderthals in having more posteriorly positioned midline to the African H. erectus (s.l.) and modern human mean landmarks (except prosthion and glabella), and in showing configurations (Fig. 3AeB), it shows a high occipital plane a wider and more coronally oriented lateral face, similar to convexity, reflected in its anterior and superior placement of modern humans. inion and a posterior displacement of the midline semiland- 4. Strong juxtamastoid eminence: When compared to the marks from inion to lambda. Both the Neanderthal and the modern human and African H. erectus (s.l.) mean configuration modern human mean configurations differ from H. erectus (s.l.)
Fig. 2. Superimposed mean configurations of fossil samples, temporal bone data set. Symbols as in Figure 1. A. Step 4 Neanderthals e Modern humans. B. Step 4 Neanderthals e African H. erectus (s.l.). C. Step 4 Neanderthals e European middle Pleistocene Step 1 specimens. D. European middle Pleistocene Step 1 specimens e African middle Pleistocene specimens. E. European middle Pleistocene Step 1 specimens e Step 2 specimens (black and red dots). F. Neanderthal Step 4 e Neanderthal Step 3 (black and red dots). G. Neanderthal Step 3 (black and red dots) e late middle-late Pleistocene Africans (blue dots). H. Neanderthal Step 3 (black and red dots) e Qafzeh-Skhul (blue dots). (For inter- pretation of the references to color in this figure legend, the reader is referred to the web version of this article.) K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 453
in the forward position of inion, reflecting the loss of the heavy African sample, however, it can be observed that both occipital torus in both later groups. samples show a similar degree of occipital plane convexity, In the European lineage this trait is expressed through time with only classic Step 4 Neanderthals having a clearly according to the expectations of the accretion model. The stronger expression of this feature. The early modern human middle Pleistocene Step 1 specimens (Cranium 5, Petralona) sample from Qafzeh-Skhul, on the other hand, exhibits are very similar to their African counterparts (Kabwe, Sal- a flatter and supero-inferiorly taller occipital plane than dahna) in their occipital plane shape (Fig. 3D), as both groups either the Neanderthal or the middle-late Pleistocene African resemble African H. erectus (s.l.). Step 2 specimens (Reilingen, mean configuration. Steinheim, Swanscombe) do not show a convexity of the 6. Reduced mastoid process: When compared to the modern occipital plane per se, but a filling out of the upper part of the human mean configuration Neanderthals clearly show occipital scale and a reduction of the nuchal region, resulting a reduced mastoid process (Fig. 2A). The African H. erectus (s.l.) in a rounder lateral outline of the occipital bone. Step 3 is quite varied in this respect, with some specimens showing (early) Neanderthals (Biache-St-Vaast, Tabun C1, Saccopas- a large mastoid (OH 9, KNM-ER 3883) and others a much tore 1) exhibit an anterior placement of inion compared to smaller one (KNM-ER 3733, KNM-WT 15000); the mean the Step 2 mean configuration and a slightly less convex mastoid configuration is relatively small (but larger than the occipital plane than the mean configuration of classic (Step 4) Neanderthal mean; Fig. 2B). Neanderthals. When the Step 3 early Neanderthals are The earlier middle Pleistocene European specimens compared to their contemporary late middle-late Pleistocene (Ceprano, and especially Cranium 5) show a relatively large mastoid process. The Step 2 specimens (Reilingen, Steinheim) exhibit a mastoid process that is intermediate in size between Step 1 and early-classic Neanderthals (Fig. 2F). There are no differences in mastoid process size between the latter two categories. In Africa, the middle Pleistocene specimens (Kabwe, Ndutu) are similar to the H. erectus mean configura- tion in their relatively small mastoids, and LPA continue this trend. The latter sample is also quite variable, with LH 18 showing an extremely reduced mastoid process. The Skhul- Qafzeh mean, on the other hand, is similar to that of modern humans (Fig. 2C-H). 7. High mid-facial prognathism: This feature is best appreciated in lateral and superior view, and is reflected by the position of the midfacial landmarks (rhinion, alare, nasospinale) relative to the rest of the face, and specifically relative to glabella and prosthion. The Step 4 Neanderthal configuration clearly shows an anterior displacement of these midfacial landmarks relative to the rest of the face when compared to either the African H. erectus (s.l.) or the modern human mean configurations (Fig. 1A-B). As would be expected in midfacial but not lower face prognathism, prosthion is not displaced anteriorly in these comparisons. When the Neanderthal configuration is compared to the European and African middle Pleistocene sample means (Fig. 1C-D), neither of the latter shows this anterior displacement of the midfacial landmarks, and the European mean configuration is nearly identical in this respect with the African one (Fig. 1E). Jebel Irhoud 1, the only repre- sentative for the late middle-late Pleistocene African sample for the facial data set, shows the opposite pattern to Neanderthals, having an anteriorly projecting glabella and prosthion but posteriorly placed midfacial landmarks. The mean configura- tion of the SKhul-Qafzeh sample is very similar in these respects to Jebel Irhoud 1. 8. Size of the piriform aperture: Here we found that larger piri- form apertures characterize Step 4 Neanderthals compared to modern humans even after overall size has been adjusted. Neanderthal noses are both supero-inferiorly taller and medio-laterally wider than those of modern humans. When Neanderthals are compared to early H. erectus (s.l.) they show taller but narrower piriform apertures. The same pattern was apparent in the comparison between Neanderthals and both Fig. 3. Superimposed mean configurations of fossil samples, posterior vault data set. European Step 1 and African middle Pleistocene specimens, Symbols as in Figures 1 and 2. A. Step 4 Neanderthals e Modern humans. B. Step 4 although in those cases the difference in width was not as Neanderthals e African H. erectus (s.l.). C. Step 4 Neanderthals e European middle marked. The Step 1 European mean configuration (Arago, Pleistocene Step 1 specimens. D. European middle Pleistocene Step 1 specimens e Petralona, Craneo 5), however, also showed a slightly taller African middle Pleistocene specimens. E. European middle Pleistocene Step 1 speci- mens e Step 2 specimens. F. Neanderthal Step 4 e Neanderthal Step 3. G. Neanderthal piriform aperture compared to the African middle Pleistocene Step 3 e late middle-late Pleistocene Africans. H. Neanderthal Step 3 e Qafzeh-Skhul. mean configuration (Kabwe, Bodo). 454 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464
Principal components and Procrustes distance analysis infraorbital region relative to the inferior margin of the orbit (Fig. 3, left panel). Facial data set: The first principal component (17.4% of the total The positive (archaic) end of PC 4 reflected shape differences variance) reflected variation among modern human populations, differentiating archaic specimens in general from modern ones, with some of the Inuit and North Asian specimens showing although middle Pleistocene specimens were generally more extreme morphology along this axis. The Neanderthal fossil sample extreme on this axis than Neanderthals or KNM-ER 3733 (Fig. 5, was separated from modern humans on the negative end of the right panel). The positive end of PC 4 reflected an elongated face second principal component (accounting for 9.6% of the total with pronounced lower prognathism, a posteriorly sloping frontal variance; Fig. 4). Some of the middle Pleistocene specimens squama, prominent supraorbital torus, a wide nasal aperture, more (Kabwe, Cranium 5) clustered with Neanderthals along PC 2, but rounded orbits, as well as, interestingly, a forward position of the most overlapped with the modern human range on this compo- infraorbital region relative to the inferior margin of the orbit. nent, though falling on the negative side of PC 2. KNM-ER 3733, All Neanderthals were nearest neighbors with each other in Irhoud 1, the Skhul and Qafzeh specimens, and the UPE sample all inter-individual Procrustes distances, reflecting the high degree of overlapped with modern humans on this component. morphological homogeneity in this group. Petralona was also Archaic specimens, including Neanderthals, KNM-ER 3733, and nearest neighbor to a Neanderthal, Gibraltar 1, as well as Cranium 5 most middle-late Pleistocene specimens, were also separated from and Kabwe. The other African specimen, Bodo, was also nearest modern humans along PC 4 (7.4% of total variance; Fig. 2). While neighbor to a Neanderthal (Guattari), as was KNM-ER 3733. Arago most Neanderthals overlapped with the extremes of the modern was nearest neighbor to Skhul 5. All other fossil specimens, human range along this axis, most middle-late Pleistocene fossils including Irhoud 1, were closest to modern human specimens. fell beyond the modern range on the positive end of PC 4, with the Despite the distinctiveness of Neanderthal facial morphology, no exception of Irhoud 1, Steinheim, Qafzeh 6, and Skhul 5. Upper clear pattern emerges here of the European middle Pleistocene Paleolithic Europeans fell within the modern human range around specimens being more similar to Neanderthals than their African 0 and mostly on the negative side of PC 4. counterparts. Rather, it appears that the middle Pleistocene sample The shape differences reflected along PC 2 are consistent with is altogether more similar to Neanderthals than it is to later the morphological differences described between Neanderthals humans, including early anatomically modern specimens and the and modern humans (Fig. 5). Specifically, the negative (Nean- late middle-late Pleistocene Irhoud 1. derthal) end of PC 2 is characterized by presumed primitive Table 4 shows the Procrustes distances among group mean facial features, including a posteriorly sloping frontal squama, prom- configurations. The smallest distance is observed between the African inent glabella, and thick supraorbital torus; and presumed middle Pleistocene sample and the classic Neanderthals, followed by Neanderthal derived features, such as a prominent forward the distance between the African middle Pleistocene specimens and placement of rhinion, a narrower face, a wider angle between the their European contemporaries (Step 1). A neighbor joining tree malar root and the zygomatic bone, and a forward position of the calculated from the Procrustes distances among the sample mean
Fig. 4. Principal components analysis, facial data set. PC 2 plotted against PC 4. K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 455
Fig. 5. Shape differences along principal components 2 and 4, facial analysis. configurations and using African H. erectus (s.l.) as an outgroup, placement of asterion and anterosuperior position of the parietal grouped both classic Neanderthals and Step 1 middle Pleistocene notch, resulting in an anteroposteriorly elongated mastoid portion Europeans together with the African middle Pleistocene specimens of the temporal bone; and a more lateral placement of porion and (Fig. 6). The late middle-late Pleistocene African sample (Irhoud 1) auriculare and a more medial position of the entoglenoid, resulting and Qafzeh-Skhul clustered together with modern humans. in a medio-laterally wider glenoid fossa. The negative end of PC 4, Temporal bone data set: In the temporal bone data set PC 1 and where Neanderthals fell, also reflected a reduction in size and PC 2 reflected aspects of modern human variation, and accounted a posterior shift of position of the mastoid process, as well as for 17.91 and 14.35% of the total variance, respectively. PC 2 also a depression of the parietal notch relative to asterion. separated European Step 1e2 specimens from African middle and Nine out of the fourteen Step 3 and 4 Neanderthals were nearest late Pleistocene fossils (with the exception of Omo). Neanderthals neighbors to each other, again suggesting a level of morphological were separated from modern humans along PC 3 and 4, accounting homogeneity in this sample. Amud 1, Saccopastore 2, and Spy 2 for 13.14 and 9.78% of the total variance, respectively, although were nearest to modern human specimens, while Guattari was there was overlap among the samples on all of these axes (Fig. 7). closest to Steinheim and Quina 27 to both KNM-ER 3733 and Amud 1 was most modern human like in its temporal bone a modern human specimen. Out of the middle Pleistocene Euro- morphology due to the large size of its mastoid process (see also peans, only Steinheim was nearest to a Neanderthal. The remaining Harvati, 2003a). PC 3 also separated out most of the H. erectus and Step 1 and 2 specimens (Ceprano, Cranium 5, Reilingen) were middle Pleistocene specimens, but with no obvious segregation nearest to modern humans, as were the other three African H. between the African and European samples. erectus (s.l.). Of the African and Levantine middle-late Pleistocene PC 3 reflected a change in the relative size of the mastoid process specimens all were nearest neighbors to modern humans except and the juxtamastoid eminence, with the negative end of this axis, Ndutu (nearest to Krapina 39-1) and Ngaloba (nearest to Spy 1). where Neanderthals clustered, showing a small mastoid process Aside from the relative distinctiveness of Step 3 and 4 Neander- and a relatively large and anterior-medially placed juxtamastoid thals, it appears that most of the archaic specimens are more eminence (Fig. 8). This end of PC 3 also showed a posteroinferior similar to modern humans than to Neanderthals.
Fig. 6. Neighbor joining tree based on the Procrustes distances, facial analysis. Outgroup: H. erectus (s.l.). 456 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464
Fig. 7. Principal components analysis, temporal bone data set. Plot of PC 3 against PC 4.
The Procrustes distances among mean temporal bone configu- Posterior vault data set: In the posterior vault analysis Nean- rations are reported in Table 4. The smallest distance is observed derthals and other archaic samples were partially separated from between classic (Step 4) and early (Step 3) Neanderthals. Classic modern humans along PC 1 and PC 2 (22.2% and 14.8% of the total Neanderthals show increasing distances to the middle Pleistocene variance, respectively; Fig. 10). The two African H. erectus (s.l.) European samples (Step 1 and 2) but are nearer to the African middle specimens clustered on the extreme opposite end of PC1 from Pleistocene and late middle-late Pleistocene samples, most likely modern humans, close to Neanderthals and the middle Pleisto- because of the relatively small mastoid processes in both latter cene specimens, and separated from other archaics along PC 2. groups. The neighbor joining tree (Fig. 9) shows the African middle Some Neanderthals (Feldhofer 1, Shanidar 1, Spy 1), most of the Pleistocene sample as an outgroup to all other groups (except the late middle-late Pleistocene African (LPA) specimens, and some African H. erectus (s.l.), used here as the outgroup), with all European early modern humans (Skhul 5, Mladec 1, Dolni Vestonice 13) specimens (Step 1 through 4) clustering in one branch and the late occupied an intermediate position between archaic specimens middle-late Pleistocene Africans, Qafzeh-Skhul sample, and modern and recent humans but overlapped with the negative end of the humans clustering together in a second branch. recent human range on PC 1. Qafzeh 6 and 9 and the remaining
Fig. 8. Shape differences along the third (left panel) and fourth (right panel) principal components of the temporal bone data set analysis. K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 457
Fig. 9. Neighbor joining tree based on the Procrustes distances, temporal bone analysis. Outgroup: H. erectus (s.l.).
Upper Paleolithic Europeans fell within the recent human range of differences along PC 2 included a change from a relatively globular variation. neurocranium with an anteriorly placed inion (negative end) to The first principal component reflects a change from a very a flattened occipital plane with a posteriorly projecting inion globular posterior vault at the positive end of the axis to a low, (positive end, H. erectus (s.l.)). elongated shape with a posteriorly convex occipital plane and Nine of the twelve Step 3 and 4 Neanderthals were nearest a higher position of the base (as represented by porion and auric- neighbors to each other in inter-individual Procrustes distance in ulare) relative to the vault on the negative end (where Neander- the posterior vault analysis, and only two were nearest modern thals and other archaic specimens cluster; Fig. 11). The shape human specimens. Two were nearest European Step 1 specimens
Fig. 10. Principal components analysis, posterior vault data set. Plot of PC 1 against PC 2. 458 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464
(Tabun 1dPetralona; Ferrassie 1dCranium 5), but three were effort to bridge the methodological gap created by the use of closest to African specimens (Spy 1 and Shanidar 1dSaldana; La radically different approaches in the analysis of the human fossil ChapelledOmo 1). Of the European middle Pleistocene specimens, record. Metric analyses (e.g., Stringer, 1974, 1983; Stringer et al., Reilingen (Step 2) was nearest neighbor to Cranium 5, Swanscombe 1979; Arsuaga et al., 1997; Rightmire, 2008; Harvati, 2009a,b) to Kabwe, and Steinheim to a modern human. Eliye Springs, Irhoud have found extensive similarities in overall morphology between 1, and Kabwe were also nearest neighbors to Cranium 5. KNM-ER African and European middle Pleistocene specimens, as well as 3733 and 3883 were nearest neighbors to each other and to reduced relative variation in the pooled middle Pleistocene sample Swanscombe. All other fossil specimens were nearest modern when compared to H. erectus or to modern humans, supporting in human individuals. Aside from a certain level of homogeneity general a ‘lumping’ of these specimens together in a single taxon, among Step 3 and 4 Neanderthals, the middle and late Pleistocene H. heidelbergensis. When the emphasis is placed on the description African and European individuals appear more difficult to differ- and analysis of discrete traits, on the other hand, the presence of entiate based on this data set. ‘incipient’ Neanderthal features in European, but not African, The Procrustes distances among group mean configurations middle Pleistocene hominins has suggested an exclusive ances- (Table 5) show a dichotomy between, on the one hand, Qafzeh- traledescendent relationship between the former two fossil Skhul and modern humans, and on the other hand, middle and late human groups, and also the classification of mid-Pleistocene Pleistocene Africans and Europeans, including Step 4 classic Europeans into a separate species than that encompassing their Neanderthals. The neighbor joining tree (Fig. 12) does not show African counterparts (e.g., Arsuaga et al., 1997; Martínez and geographic clustering of the European samples. Modern humans Arsuaga, 1997; Dean et al., 1998; Hublin, 1998; Stringer and are grouped tightly with Qafzeh-Skhul, and with the late middle- Hublin, 1999). The latter view is often summarized in terms of late Pleistocene Africans, with classic Neanderthals as their the accretion model, which proposes the accumulation of Nean- immediate outgroup. Middle Pleistocene Europeans (Step 1) appear derthal derived traits in the European lineage gradually through as an outgroup to all other samples (except African H. erectus (s.l.)). time, with different features proposed to appear at different stages of the process (Dean et al., 1998; Hublin, 1998, 2009). We approached our goal through a combination of mean shape Discussion comparisons of the fossil hominin groups, and multivariate statis- tical analysis of three data sets, representing the face, posterior Our study aims to capture and analyze quantitatively specific cranial vault, and temporal bone. The comparison of mean shapes Neanderthal features proposed to appear in the middle-late indicates that some of the proposed traits of the basicranium and the European human fossil record according to the accretion hypoth- face do follow the expectations of the accretion model. Nonetheless, esis. Our analysis is metric and, like other metric analyses, reflects a few of the features proposed by Dean et al. (1998) as ‘incipient’ overall cranial shape. However, through the choice of 3-D land- Neanderthal traits do not seem to characterize the European clade mark coordinates that we used as variables we also aim to but rather likely represent retained symplesiomorphies shared with quantify the particular detailed shape of relevant features in an some of the middle Pleistocene African hominins.
Fig. 11. Shape changes along the first (left panel) and second (right panel) principal components of the posterior vault data set. K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 459
Table 5 Procrustes distances among mean group configurations
Facial data set H. erectus MPA Step 1 MPE LPA Step 4 Neanderthal Qafzeh-Skhul Modern H. erectus 0.000 MPA 0.123 0.000 Step 1 MPE 0.118 0.065 0.000 LPA 0.125 0.110 0.112 0.000 Step 4 Neanderthal 0.113 0.063 0.071 0.113 0.000 Qafzeh-Skhul 0.119 0.092 0.086 0.099 0.095 0.000 Modern 0.128 0.089 0.093 0.094 0.092 0.072 0.000
Temporal bone data set H. erectus LPA MPA Step 1 MPE Step 2 MPE Step 3 Neanderthal Step 4 Neanderthal Qafzeh Modern H. erectus 0.000 LPA 0.140 0.000 MPA 0.102 0.137 0.000 Step 1 MPE 0.207 0.190 0.191 0.000 Step 2 MPE 0.154 0.140 0.154 0.168 0.000 Step 3 Neanderthal 0.134 0.129 0.136 0.133 0.152 0.000 Step 4 Neanderthal 0.118 0.093 0.109 0.150 0.132 0.061 0.000 Qafzeh 0.137 0.108 0.139 0.198 0.154 0.144 0.118 0.000 Modern 0.149 0.107 0.141 0.159 0.140 0.139 0.120 0.101 0.000
Posterior vault bone data set H. erectus LPA MPA Step 1 MPE Step 2 MPE Step 3 Neanderthal Step 4 Neanderthal Qafzeh-Skhul Modern H. erectus 0.000 LPA 0.115 0.000 MPA 0.100 0.057 0.000 Step 1 MPE 0.085 0.090 0.075 0.000 Step 2 MPE 0.108 0.056 0.047 0.081 0.000 Step 3 Neanderthal 0.098 0.059 0.057 0.072 0.056 0.000 Step 4 Neanderthal 0.112 0.049 0.051 0.097 0.056 0.051 0.000 Qafzeh-Skhul 0.152 0.059 0.097 0.133 0.097 0.098 0.076 0.000 Modern 0.154 0.062 0.098 0.124 0.102 0.099 0.086 0.046 0.000
Four features (sagittally oriented face, strong juxtamastoid condition was seen only in Neanderthals and might be related to eminence, enlarged nasal aperture, pronounced mid-facial prog- their mid-facial prognathism. nathism) follow the predictions of the accretion model. However, Two additional proposed Neanderthal features (high occipital the latter two characterize the terminal stage of Neanderthal plane convexity, reduced mastoid process) were found to be evolution and are therefore of limited value in assessing phyloge- expressed among the highly variable African middle-late Pleisto- netic relationships of earlier middle Pleistocene specimens. cene samples as well as in the European record. The increased Furthermore, a sagittally oriented face in middle Pleistocene convexity of the occipital plane appeared clearly in Step 3 and 4 European specimens was not found to be associated with a forward Neanderthals. However the African middle-late Pleistocene sample advancement of the face, contra Dean et al. (1998). The latter was similar to early Neanderthals in this respect. The ‘occipital bun’
Fig. 12. Neighbor joining tree based on the Procrustes distances, posterior vault analysis. Outgroup: H. erectus (s.l.). 460 K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 morphology has been previously found to be tightly integrated the late middle-late Pleistocene Africans, Qafzeh-Skhul, and with the overall shape of the cranium and is variable within modern humans in another, with middle Pleistocene Africans (and Neanderthals (Gunz and Harvati, 2007; Bastir et al., 2010). This African H. erectus (s.l.)) being outgroups to all other samples. This structural constraint could thus account for similar levels of finding agrees with those reported by Martínez and Arsuaga (1997), occipital convexity in specimens with similarly elongated crania, who, based on an overlapping but different set of features than whether they are of European or African origin. The reduced those used here, found that the temporal bone of middle Pleisto- mastoid process was also found to be expressed in both European cene Europeans was aligned with that of Neanderthals, while that and in some African fossils. This feature is quite variable among of middle Pleistocene Africans with modern humans. modern humans, where its size is related to sex. Its presence in The posterior vault data set was designed to capture the external some African fossils may therefore be related to sexual dimor- morphology of the occipital plane convexity, often referred to as the phism. It is also unclear whether the reduction of the mastoid occipital ‘bun.’ Earlier work (Gunz and Harvati, 2007, see also process might follow similar structural constraints as those Harvati, 2009b) has suggested that the posterior projection of the observed for occipital ‘bunning,’ and this is a question that warrants occipital plane is strongly integrated with the overall shape of the further investigation. cranium and therefore cannot be considered independently from Two further traits examined were found to represent possibly the latter. Our results here agree with this finding, and again call primitive conditions for middle Pleistocene Homo. The convex and into question the utility of the convexity of the occipital plane in receding infraorbital profile, although clearly a characteristic of differentiating Neanderthals from other late Pleistocene samples. classic Neanderthals, was present (in a lesser degree of expression) Nonetheless, unlike the highly variable late middle-late Pleistocene in both African and European middle Pleistocene specimens, rather sample from Africa, the Qafzeh-Skhul sample shows a relatively flat than in European pre-Neanderthals alone. This result agrees with occipital plane and groups with modern humans in all analyses. previous studies based on landmarks, as well as with studies using It must be noted that in all of these analyses the African middle more extensive coverage of the infraorbital region using surface and late Pleistocene specimens showed a great amount of vari- semilandmarks (Harvati, 2009a,b; Maddux and Franciscus, 2009; ability despite the small size of their samples (see also Crevecoeur Freidline et al., 2010). The anteroinferior position of glabella and et al., 2009; Gunz et al., 2009b). This variability tended to encom- disruption of the previously horizontal supercilliary ridges, pass aspects of the variation seen in the European fossils and in proposed to appear in the middle Pleistocene pre-Neanderthal modern humans. This result suggests that the European fossil Europeans, characterizes Neanderthals relative to both African H. record might exhibit a greater level of homogeneity than does the erectus (s.l.) and modern humans. However, we observed this African record. condition in both African and European middle Pleistocene speci- The three data sets used here might not be equally relevant to mens, as well as in Irhoud 1 and in the Skhul-Qafzeh sample. Our phylogenetic analyses. Although the validity of using cranial results suggest that a slight infra-orbital plate convexity and the morphology in phylogenetic analyses has been questioned (see anteroinferior placement of glabella might best be considered Collard and Wood, 2000), multiple recent studies have found ancestral for middle Pleistocene Homo rather than derived for the overall cranial morphology to reflect population history well European lineage. among modern humans (e.g., Relethford, 1994, 2004a,b; Roseman, These findings were broadly corroborated by our PCA and 2004; Harvati and Weaver, 2006a,b; Harvati et al., 2009; Hubbe Procrustes distance analyses (though it must be noted that the et al., 2009; Smith, 2009; von Cramon-Taubadel, 2009). However, results of our principal components analyses may be affected by the whether different anatomical regions (such as the face, vault, or inclusion of a large modern human sample). Here the facial data set basicranium) are better suited for phylogenetic/population history was successful in separating Step 4 Neanderthals from modern reconstruction remains an open question. Several recent studies humans and from late middle-late Pleistocene African fossils, but have found temporal bone morphology to reflect population not from middle Pleistocene Europeans or Africans. This suggests history and phylogeny better than other aspects of the cranium that the one facial feature that seems to appear early in the Euro- (Harvati, 2003a; Lockwood et al., 2004; Harvati and Weaver, pean lineage (more sagittally oriented face) is not expressed 2006a,b; Smith, 2009; von Cramon-Taubadel, 2009). Vault strongly enough to differentiate the African from the European morphology, as measured by both 3-D landmark data and middle Pleistocene specimens and may be obscured by the addi- conventional measurements, is also reported to be relatively highly tional data included in the analysis which reflect more general correlated with population history (e.g., neutral genetic data or dimensions of the face. Our results are similar to those reported by geographic distances; Roseman, 2004; Harvati and Weaver, metric multivariate analyses elsewhere (e.g., Stringer, 1974; 2006a,b; Harvati et al., 2009; Hubbe et al., 2009). However, the Arsuaga et al., 1997). This lack of differentiation is reflected also usefulness of the face in phylogenetic analyses has been questioned in the neighbor joining tree, which clusters the African middle because this region is thought to be differentially affected by Pleistocene specimens with classic Neanderthals (Step 4). On the mastication and climate (e.g., Skelton and McHenry, 1992; Wood other hand, the late middle-late Pleistocene African sample, rep- and Lieberman, 2001; Lieberman et al., 2004; Lieberman, 2008). resented in the facial data set only by Irhoud 1, and the Qafzeh- Recent work testing this hypothesis has produced somewhat Skhul sample clearly group with modern humans both in the PCA contradictory results. Harvati and Weaver (2006b) found a climatic, and in the Procrustes distance neighbor joining tree, showing but not a population history, signal in their 3-D analysis of facial evidence for clear lineage separation at this later time period. morphology in 13 modern human populations. However, Smith The analysis of the temporal bone landmarks for the most part (2009) showed a significant correlation between facial followed the expectations of the accretion process in Europe. The morphology and neutral genetic distances using similar data and 14 temporal bone landmark data set differentiated between Nean- populations. Harvati et al. (2009) and Hubbe et al. (2009) analyzed derthals and modern humans (see also Harvati, 2003a) as well as more than 7,000 specimens from 135 populations and found between European and African middle Pleistocene samples a significant correlation between facial measurements and (although there was much overlap) in the principal components geographic distances (used as a proxy for population history), as and Procrustes analyses. The temporal bone Procrustes distance well as a climatic signal in the face of extreme high-latitude groups. neighbor joining tree was the only one that clustered the Nean- A more recent study tested these hypotheses by examining indi- derthals and pre-Neanderthals together in a common branch and vidual cranial bones as well as cranial regions (von Cramon- K. Harvati et al. / Journal of Human Evolution 59 (2010) 445e464 461
Taubadel, 2009). This approach suggested that the maxilla, the Neanderthals. These traits also provided limited evidence of lineage zygomatic, and the occipital bone are less reliable for reconstruct- separation in the first half of the middle Pleistocene. The sagittal ing phylogenetic relationships. orientation of the face and a stronger expression of the juxtamas- These results paint a complicated picture of the potential toid eminence linked earlier middle Pleistocene Europeans with usefulness of different components of cranial morphology for the later Neanderthals, as proposed by the accretion hypothesis. deciphering phylogenetic relationships. It should be kept in mind However, in most other respects middle Pleistocene Europeans that the majority of these studies were conducted on the micro- were nearly identical to the African middle Pleistocene samples evolutionary scale and therefore may not be relevant for higher until the Holstein period, suggesting that some commonly cited level systematics. Nonetheless, the bulk of the currently available ‘incipient’ Neanderthal features might instead represent pleiso- evidence suggests that the results of the temporal bone and, morphic traits. Our results are consistent with the view that pop- perhaps to a lesser extent, those of the facial analysis may be ulation separation between African and European middle considered most relevant to the reconstruction of middle Pleisto- Pleistocene humans did not occur before 450 ka, as proposed by cene phylogenetic relationships. Hublin (2009). The findings reported here also indicate a high Our findings here must be considered a first approach at variability among African samples, which overlapped with the breaching this problem, and they are affected by limitations variation shown by Neanderthals in some respects. Further inherent in paleoanthropological research. Although quite exten- consideration of additional anatomical regions and elements, as sive, our Pleistocene sample is limited by the scarcity of specimens, well as the biological and evolutionary processes involved in the an imperfect state of preservation, or the lack of accessibility. Step 2 expression of these features, is needed to fully evaluate the in particular is poorly documented. Furthermore, while material for taxonomy of the middle Pleistocene human fossil record. Step 3 and 4 are in chronological continuity, the time distance between the youngest individual of Step 2 and the oldest of Step 3 Acknowledgments could be >120 ka depending on the age of the Reilingen specimen, recovered from an uncertain geological context. To some extent this We thank all curators of fossil and modern human collections at may explain the larger morphological distance observed between various institutions in Africa, Europe, Israel, and the United States Step 2 and 3 than between Step 3 and 4. Future work focusing on for allowing access to their collections. We are grateful to Eric smaller specific anatomical regions might be able to consider Delson, Chris Stringer, Susan Anton and to the anonymous additional important fragmentary specimens that could not be reviewers for their useful comments and discussion. This research included in the present work (see Freidline et al., 2008, 2009). was supported by the “EVAN” Marie Curie Research Training Finally, although our data sets were designed to reflect the Network MRTN-CT-019564 and the Max Planck Society. NYCEP features examined as closely as possible, we may not have been morphometric contribution Nr. 24. able to capture fully the relevant morphology in the case of each individual trait. Future approaches, such as surface semilandmark References analysis of particular traits, may offer additional possibilities for quantification, also for smaller-scale traits (see Freidline et al., 2008, Arsuaga, J.-L., Martinez, I., Gracia, A., Lorenzo, C., 1997. The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. J. Hum. Evol. 33, 2009, 2010; Maddux and Franciscus, 2009). Such future work 219e281. should focus additionally on other features central to the accretion Bailey, S., 2006. 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