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The Vindija Neanderthal scapular glenoid fossa: comparative shape analysis suggests evo-devo changes among Neanderthals

Fabio Di Vincenzo a, b, Steven E. Churchill c, d, Giorgio Manzi a, b a Dipartimento di Biologia Ambientale, Sapienza Università di Roma, 00185 Roma, Italy; b Istituto Italiano di Paleontologia Umana, 00197 Roma, Italy; c Department of Evolutio- nary Anthropology, Duke University, Durham, North Carolina 27708, USA; and d Institute for Human Evolution, University of the Witwatersrand, Wits 2050, South Africa.

Contents:

SOM Materials SOM References ...... 3

Sample ...... 1 SOM Figures Sexual dimorphism ...... 2 Figure S1 ...... 4 Table S1 ...... 2 Figure S2 ...... 5 Figure S3 ...... 5 Appendix A Figure S4 ...... 6 Anatomical notes ...... … 2 Figure S5 ...... 6

SOM Materials (134.9 -180°) (Lordkipanidze et al., 2007). This suggests a more ab- ducted/supine orientation of the arm, a more lateral position of the scapu- Sample. The OTUs utilized in the analyses are characterized as follows: la, or a diverse range of arm movement in the Dmanisi hominins relative to H. sapiens (Lordkipanidze et al., 2007). Australopithecus africanus (N = 1). Includes the partial right scapula STS 7 from member 4 of Sterkfontein Cave, South Africa (Partridge, 1978), Homo floresiensis (N = 1). This OTU was included to represent the SGF which has been taxonomically referred to A. africanus (Broom et al., 1950; morphology of the small-bodied hominins from Liang Bua Cave (Flores Isl- Vrba, 1979). There is no evidence of lithic tool manufacture or use in A. and, Indonesia) dated to 15.7–18.7 Ka (Morwood et al., 2005; Larson et al., africanus, which might possibly affect the overall morphology of the SGF. 2009). The SGF of the right scapula of LB 6/4 is well-preserved overall, de- While the functional interpretation of australopith locomotor morphology spite the existence of two main horizontal and several smaller longitudinal is debated, many researchers interpret aspects of australopith shoulder fissures that extend through the middle of the fossa. The outline of the SGF morphology as reflecting climbing adaptations (Oxnard, 1969; Robinson, appears not to be affected by the post mortem distortion that is evident at 1972; Larson, 2009). The SGF of STS 7 and other australopiths was more the root of the spine and scapular neck and that may result in a slight dor- cranially oriented than in modern humans, as reflected in low values of the sal orientation to the glenoid (towards the modern human condition, Lar- axillo-glenoid angle. For STS 7, estimates of this angle have ranged between son et al., 2009). The value of the axillo-glenoid angle is 136° (Larson et al., 103° and 125° (Larson, 2009), with a most probable value of ca.115° 2009), which falls within the range of modern humans, whereas a lack of (Berger et al., 2010). It is likely that the cranially oriented SGF allowed A. humeral torsion (in the type specimen LB 1), estimated between 110° and africanus to achieve a wide range of overhead movements of the upper 121° and with a mean value of 115° (Morwood et al., 2005; Larson et al., limbs in the context of arboreality (Larson, 2009). 2007, 2009), suggests that H. floresiensis was similar to other taxa of early Homo (e.g., Homo georgicus, Lordkipanidze et al., 2007) in upper limb func- Australopithecus sediba (N = 1). Includes the largely complete and as yet tional morphology. This interpretation has been challenged by scholars undescribed right SGF of MH 2 from Malapa, South Africa (Berger et al. supporting a pathological interpretation of the skeletal morphology of the 2010). In its overall morphology, the scapula of MH 2 is similar to that of Flores hominins (see for example Hershkovitz et al., 2007 and Richards, other South African australopiths (such as Sts 7), and is likely to reflect a 2006). It has also been noted that low values of humeral torsion (111°- significant degree of arboreality in the locomotor repertoire of this species. 140°) can be found in non-pathological modern human females among cen- tral African pygmies (Marquer, 1972 but see ref. Larson et al., 2007). Lithic Homo georgicus (N = 1). Includes the glenoid fossa of an otherwise poor- technology associated with the sub-fossil Flores human remains is charac- ly preserved right scapula, D 4166, from the 1.77 Ma Lower Paleolithic site terized by a single reduction sequence from pebble-based ‘core tool’ indus- of Dmanisi, Georgia (Gabunia et al., 2000; Lordkipanidze et al., 2007). The tries to small-sized, flake-based ‘flake tool’ industries (Brumm et al., 2006; archeological context of the Dmanisi scapula is Mode I of Pre-Oldowan (de Moore and Brumm, 2007; Moore et al., 2009), and there is no evidence of Lumley et al., 2005). The SGF is reasonably well-preserved inferiorly (with projectile weaponry. some damage distributed along the inferior border of the fossa), but is damaged in the apical region along its ventral margin. The SGF is somewhat Homo heidelbergensis (N = 5). Detailed morphological descriptions of the cranially-oriented relative to the midaxillary border, with an axillo-glenoid SGFs of the entire sample of the Atapuerca Sima de los Huesos (SH) scapu- angle of 129° (Lordkipanidze et al., 2007), which falls in the lower half of lae are provided by Carretero and colleagues (1997), with the exception of the range of variation of modern humans (119.5-140.1°, N =269, Vallois, the AT-1256 scapula (Scapula VIII). The fossil material from Atapuerca SH 1928-46; Carretero et al., 1997). However this measure was questioned by has been dated to >530 Ka (Bischoff et al., 2003, 2007). No lithic tools are Larson (2009), who instead estimated a higher value of 135°. The upper found in direct association with the SH fossils, except for a Lower Paleolith- limbs are further characterized by low humeral torsion. The low values of ic flaked quartzite handaxe (Mode II) reported by Carbonell et al. (2003). humeral torsion (110° - 104°) in the Dmanisi adult humerus (associated The discovery of Middle Pleistocene (~ 400 Ka) wooden spears at Schönin- with the D 4166 scapula) and a sub-adult individual fall within the range of gen in Northern Germany (Thieme, 1997, 2000) has been taken by some as the australopiths (111°-130°) and well below the modern human range evidence of the use of throwing-based long-range projectile weaponry by

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European H. heidelbergensis. If so, we might expect that high SGF joint reac- 2005), or perhaps between 60-50 ka in the Near East (Shea, 2009), and tion forces generated during abduction and forceful internal rotation of the thus throwing-based projectile weaponry was likely a component of the throwing arm were important selective and epigenetic determinants of subsistence tool kits carried by modern humans as they expanded into Eu- glenoid fossa morphology in this group. However, the claim that the rope during MIS 3 (Shea, 2006, 2009). Schöningen spears were projectile weapons has not been universally ac- cepted (Shea, 2006, 2009; Churchill and Rhodes, 2009). Recent Homo sapiens – Fuegians (N = 14). South American hunter- gatherers who inhabited the extreme southern regions of the continent Homo neanderthalensis from Krapina (N = 5). This sample represents an (Tierra del Fuego) into historic times. The subsistence strategies of Fuegian ‘early’ Neanderthal population from the site of Krapina in Croatia (Smith, groups (Yàmana (Yaghan) and Alacalùf) was based on mixed exploitation 1976; Radovcic et al., 1988), dated to the end of MIS 6 or the beginning of of terrestrial and marine resources. For hunting whales and sea lions, Fu- MIS 5e (Rink et al., 1995). The archaeological context is typical Middle Pa- eginas utilized wooden harpoons with detachable bony tips launched from leolithic (Mousterian) of Charentian tradition with the presence of some canoes without the aid of atlatls (spear-throwers) (Mason, 1902; Orquera Levallois elements in the more recent Mousterian levels of the cave (Simek and Piana, 2009; Piana and Orquera, 2009). Fuegian hunters were also and Smith, 1997). known to use bolas for throwing stone balls at small prey (Bove, 1883).

Homo neanderthalensis – Late European and Near-Eastern samples (N = Recent Homo sapiens – Iron Age Italians (N = 7). Iron Age agro-pastoral 6). This sample includes Near/Middle Eastern and ‘classic’ European Samnite population from the Alfedena necropolis in central Italy (Abruzzo), Würmian Neanderthals, including Neandertal 1 (Germany), La Ferrassie 1 dated to 2600-2400 BP (Sparacello et al., 2011). and 2 (France), Kebara 2 and Tabun C1 (Israel) and Shanidar 4 (Iraq) [chronology and archaeological context for these specimens can be found Recent Homo sapiens – Garamantes (N = 6). Agro-pastoral population of in Schwartz and Tattersall (2002, 2003)]. Neanderthals are characterized southern Libya, dated between 3000-1500 BP (Pace et al., 1951). by a dorsally-positioned SGF, and axillo-glenoid angles ranging between 132°-150°(Trinkaus, 1983; Carretero et al., 1997), which overlaps both the Recent Homo sapiens – Lombards (N = 8). Early medieval rural popula- modern human (119.5-140.1°, Vallois, 1928-46; Carretero et al., 1997) and tion of Lombards from the village of La Selvicciola (Ischia di Castro) in cen- H. heidelbergensis (140-144°, Carretero et al., 1997) range of variation. Ac- tral Italy (Latium), dated to the 7th century A.D. (Manzi et al., 1995; Salva- cording to Trinkaus (Trinkaus, 1983), the less cranial orientation of the dei et al., 2001). fossa in Neanderthals is indicative of more powerful rotator cuff muscles, and in particular M. infraspinatus and subscapularis (external and internal rotators of the humerus, respectively). Humeral torsion is low in Neander- Sexual dimorphism. Intra-specific variation in SGF morphology related to thals compared with modern humans (Carretero et al., 1997; Larson, sexual dimorphism was tested on specimens of H. sapiens for whom rea- 2009). Neanderthals are typically associated with Middle Paleolithic lithic sonable determinations of sex could be derived from other postcranial assemblages(Mode III or Mousterian), often containing Levallois points, elements (Table S1). MANOVA performed on the first 30 PCA's scores (> which were likely sometimes hafted to handles or wooden spears, although 95% of the total variance) was not significant (p = 0.64), confirming pre- firm evidence of throwing-based, long-range projectile weaponry is lacking vious results reporting a lack of sexual dimorphism in overall morphology (Churchill and Rhodes, 2009). of the SGF in our species (Prescher and Klümpen, 1997; Churchill and Trin- kaus, 1990). With respect to the other taxonomic groups, A. africanus, early Homo neanderthalensis from Vindija (N = 1). The left scapular fragment Homo and H. heidelbergensis had insufficient sample sizes to allow for in- Vi-209 from Vindija cave in the Hrvatsko Zagorje of north-west Croatia tra-group analyses, and the sex attribution of some of the specimens is un- (Fig.1) preserves the glenoid fossa, lateral scapular spine and a portion of certain. For H. neanderthalensis, no data are available for the specimens the base of the coracoid process (Wolpoff et al., 1981). The specimen de- from Krapina (based on values of the SGF’s centroid size, a proxy for the rives from Mousterian level G3 (Malez et al., 1980), which has yielded a overall body size, Krapina 127, 129 and 131 could be females and Krapina number of fragmentary hominin fossils that can be confidently identified as 130 and 133 males), whereas sex attributions for Würmian and Near East Neanderthal (Malez et al., 1980; Wolpoff et al., 1981; Smith et al., 1985; Neanderthals are generally well-accepted. However, our sample only in- Smith and Ahern, 1994; Ahern et al., 2004; Janković et al., 2006). cludes two females (Tabun C1 and La Ferrassie 2), both of which are cha- racterized by low values of CS (Tabun C1 is the smallest specimen in abso- Late Pleistocene Homo sapiens (N = 11). Upper Paleolithic and Mesolithic lute size). These two females do not cluster together in any of the analyses, European hunter-gatherers. While the origins of true long-range projectile and this in combination with the lack of sexual shape dimorphism in mod- technology is still somewhat uncertain, evidence suggests that projectile ern humans leads us to conclude that sexual dimorphism in SGF shape was weapons first emerged in the African Middle Stone Age, possibly before 77 also insignificant in the Neanderthals. ka (Churchill and Rhodes, 2009; McBrearty and Brooks, 2000; Brooks et al.,

SOM Table 1. Specimens used in the MANOVA for sexual dimorphism

Males (N = 30) Females (N = 11)

Late Pleistocene H. sapiens Dolní Věstonice 13, 14, 16*; Oberkassel 1* Dolní Věstonice 3*; Oberkassel 2*

Alfedena 126, 130, 132; Fezzan 3334, 3337*, 3338*; Recent H. sapiens Alfedena 128*; Fuegian 4, 9, 13; Selvicciola T86-17; Fuegian 5, 6, 7, 8; Selvicciola T84-3, T89-8, 90-5

(*) Isolated individuals, not antimeric

Appendix A lesser tubercle of the humerus (Prescher and Klümpen, 1997).This area is associated with a reduction of the fibrous rim (labrum) and the presence of Anatomical notes. a small bursa overlying a bevelled lip to the glenoid margin (Prescher and Klümpen, 1997). The reduced size of the labrum in this area could make it The glenoid fossa of the scapula (Fig. S5) is ringed by a fibrocartilagenous prone to anterior dislocation of the humeral head, but this is resisted by the labrum and is completely enclosed in the joint capsule, which in turn is presence of the M. subscapularis itself. Between-group differences in the overlain in places by the rotator cuff muscles (shown in cross section). depth of the glenoid notch likely reflect differences in the relative size of M. Along the superior ventral margin of the glenoid fossa lies the glenoid subscapularis, which in turn might signal differences in the functional de- notch (incisura acetabulare), which is likely developmentally determined mands on this muscles as an internal humeral rotator and stabilizer of the by the presence of the M. subscapularis tendon on its path towards the glenohumeral joint.

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SOM Figures

MH 2

Vi-209

LB 6-4

D 4166

PC3

STS 7

Vindija 209 Malapa (MH 2) Sterkfontein (STS 7; A. africanus) Dmanisi (D 4166; H. georgicus) Flores (LB 6/4; H. floresiensis) Atapuerca SH (H. heidelbergensis) H. neanderthalensis Late Pleistocene H. sapiens H. sapiens (Holocene)

Fig. S1. 3D plot of the first three principal components (explaining 83.92% of the total variance) of the whole sample of SGFs. The size of the spheres is proportional to the centro- id size of each specimen

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PC1 (53.8%) PC1 (55.1%)

0.03

0.02

Iron Age It. LP H. sapiens 0.01 Iron Age It. LP H. sapiens %) %) Fuegians

0.0 PC2 (24.8 PC2 PC 2 (28 .4 PC Fuegians Garamantes

Garamantes -0.01 Lombards Lombards -0.02

-0.02 -0.01 0.0 0.01 0.02 0.03 -0.02 -0.01 0.0 0.01 0.02 0.03

Fig. S2. Total variance along PC1 and PC2 of the averaged Procrustes coordinates for right (a) and left (b) SGF of the H. sapiens sub-sample OTUs

4 Group Homo heidelbergensis Homo neanderthalensis LP H. sapiens Recent H. sapiens Homo neanderthalensis 2 Vi-209 (ungrouped) Group Centroid

Recent H. sapiens

0 Function 2 Function

Homo heidelbergensis

-2 LP H. sapiens

Vi-209 -4

-7.5 -5.0 -2.5 0.0 2.5 5.0 Function 1

Fig. S3. Plot of the results of the Discriminant Analysis (DA) with Vi-209 not assigned to any a priori group

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A. sediba

Fig. S4. Hierarchical cluster-analysis by UPGMA of the whole sample: left (L) and Right (R) specimens.

Coracoid Supraspinatus Long head of Biceps Acromion Superior glenohumeral lig. Subscapularis Glenoid notch Capsule Middle glenohumeral lig. Infraspinatus Glenoid fossa

Glenoid labrum Inferior glenohumeral lig. ant. Teres minor

Inferior glenohumeral lig. post. Bone

Muscles

Tendons and ligaments

Fig. S5. Schematic drawing of the main anatomical structures discussed in the text. 6