AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 156:148–157 (2015)

Brief Communication: Molar Crown Inner Structural Organization in Javanese Homo erectus ment Zanolli* Cle Multidisciplinary Laboratory, International Centre for Theoretical Physics, Trieste, Italy KEY WORDS structure

Sangiran Dome; Javanese Homo erectus; permanent molars; internal

ABSTRACT This contribution investigates the inner organizational pattern (tooth tissue proportions and enamel–dentine junction morphology) of seven Homo erectus permanent molar crowns from the late Lowerearly Middle Pleistocene Kabuh Formation of the Sangiran Dome (Central Java, Indonesia). The previous study of their external characteristics confirmed the degree of time-related structural reduction occurred in Javanese H. erectus, and also revealed a combination of nonmetric features which are rare in the Lower and early Middle Pleistocene dental record, but more frequently found in recent humans. In accordance with their outer occlusal morphology, the specimens exhibit a set of derived internal features, such as thick to hyperthick enamel, an incomplete expression of the crest pat-

terns at the enamel–dentine junction (EDJ) level, a sharp EDJ topography. As a whole, these features differ from those expressed in some penecontemporaneous specimens/samples representing African H. erectus/ ergaster and H. heidelbergensis, as well as in Neanderthals, but occur in recent human populations. Further research in virtual dental paleoanthropology to be developed at macroregional scale would clarify the polarity and intensity of the intermittent exchanges between continental and insular Southeast Asia around the Lower to Middle Pleistocene boundary, as well as should shed light on the still poorly understood longitudinal evolutionary dynamics across continental Asia. Am J Phys Anthropol 156:148–157, 2015. VC 2014 Wiley Periodicals, Inc.

The Indonesian dentognathic human fossil assemblage has been recognized as one of the most morphodimensionally variable in the fossil record (rev. in Kaifu et al., 2005). This likely results from the sea level oscillations that cyclically affected the Indonesian archipelago during the Quaternary and intermittently allowed, limited, or inhibited the exchanges between continental and insular domains (Djubiantono and Semah, 1991; Voris, 2000). Such palaeoenvironmental variations affected the evolutionary dynamics and were deciding factors in the time-related mammal biodiversity changes (de Vos and Long, 2001; van den Geer et al., 2010). Comparative evidence suggests that, during the transition Lower to Middle Pleistocene, Javanese Homo erectus underwent facial reduction, mandibular ramus lowering, dental arcade widening, and postcanine tooth structural reduction to a greater extent than seen in African H. erectus/ergaster (Wood, 1991; Anton, 2003; Kaifu et al., 2005; Kaifu, 2006; Suwa et al., 2007; Wood and Leakey, 2011). The recent description of a new assemblage of H. erectus permanent molars from the late Lower-Early Middle Pleistocene of the Dome of Sangiran, Java, has provided additional evidence to the degree of heterogeneity characterizing the Indonesian dental hypodigm and also revealed a distinct series of derived features (Zanolli, 2013). Basically, these include marked decrease in crown length associated with the reduction, or even loss, of the hypoconulid, and low frequency of the Y groove pattern (Zanolli, 2013). The combination of these characteristics is rare in the Lower and Early Middle Pleistocene dental record, notably in the early specimens from Sangiran (Kaifu et al., 2005; Kaifu, 2006). However, a similar morphostructural pattern has been reported for the Middle Pleistocene Chinese samples of Zhoukoudian and Lantian (Weidenreich,

1937; Wolpoff, 1999; Kaifu, 2006), as well as for the assemblage of Atapuerca Sima de los Huesos (MartinonTorres et al., 2012), and is more frequently found in recent humans (Bailey and Hublin, 2013). Compared to the morphology expressed at the outer crown surface, inner tooth structural organization and conformation tend to be more conservative (e.g., Macchiarelli et al., 2006; Skinner et al., 2008a; Bailey et al., 2011), but the level of concordance between outer and inner signatures in dental samples having underwent structural reduction still deserves investigation (Bailey and Hublin, 2013) and is unreported in the Indonesian permanent tooth fossil assemblage (cf. Zanolli et al., 2012). By using techniques of three-dimensional (3D) virtual imaging and high resolution quantitative characterization coupled with geometric morphometric (GM) analyses, I investigated here the inner organizational pattern

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Additional Supporting Information may be found in the online version of this article. Grant sponsors: Deutscher Akademischer Austauschdienst and the Soci et e des Amis du Mus ee de l’Homme of Paris. *Correspondence to: C. Zanolli; Multidisciplinary Laboratory, International Centre for Theoretical Physics, via Beirut 31, 34014 Trieste, Italy. E-mail: [email protected] Received 14 May 2014; accepted 27 August 2014 DOI: 10.1002/ajpa.22611 Published online 11 September 2014 in Wiley Online Library (wileyonlinelibrary.com).

JAVANESE HOMO ERECTUS INNER MOLAR STRUCTURE (tooth tissue proportions and enamel–dentine junction morphology) of seven permanent molar crowns of Javanese H. erectus previously reported for their external features (Zanolli, 2013). Given the of potential value of such tooth structural information in taxonomic, phylogenetic, and adaptive/evolutionary studies (e.g., Macchiarelli et al., 2006; Olejniczak et al., 2008a, b; Skinner et al., 2008a), the degree of correspondence between their outer and inner morphology was assessed, and finally compared the present 3D-based results to the evidence currently available for a number of African and European penecontemporaneous and later samples, including extant humans.

MATERIALS AND METHODS The H. erectus s.s. tooth sample investigated in this study consists of seven unworn to moderately worn isolated upper (N 5 2) and lower (N 5 5) permanent molar crowns from the late Lower-Early Middle Pleistocene Kabuh (Bapang) Formation of the Sangiran Dome, Java (Bettis et al., 2009; Semah et al., 2010; Zaim et al., 2011). This material, collected between 1991 and 2009 during field research work jointly developed in the Sangiran Dome area by the Indonesian Archeological Services of Yogyakarta and the French Museum National d’Histoire Naturelle (MNHN), is permanently stored at the Balai Pelestarian Situs Manusia Purba of Sangiran, Java. More specifically, the specimens represent an upper left M1/2 (NG91-G10 n 1: ULM1/2), an upper left M3 (NG0802.1: ULM3), a lower right M2 (NG0802.3: LRM2), a lower left M2/3 (NG92.3: LLM2/3), two lower right M2/3s (NG92 D6 ZE 57s/d 76 and NG0802.2: LRM2/3), and a lower left M3 (NG9107.2: LLM3) (Zanolli, 2011, 2013: Fig. 2). In 2009, these specimens were imaged by microtomography (mCT) at the Centre de Microtomographie of the University of Poitiers (France). The acquisitions were realized with a X8050-16 Viscom AG equipment (camera 1004*1004) according to the following parameters: 110–145 kV voltage; 0.43 mA current; a projection each 0.20 . The final volumes were reconstructed using DigiCT v.2.3.3 (DIGISENS) in 8-bit format, with an isotropic voxel size ranging from 20.9 to 23.7 mm (Zanolli, 2011). Using Amira v.5.3 (Visualization Sciences Group Inc.) and ImageJ v.1.46 (Schneider et al., 2012), a semiautomatic threshold-based segmentation was carried out following the half-maximum height method (HMH; Spoor et al., 1993) and the region of interest thresholding protocol (ROI-Tb; Fajardo et al., 2002), taking repeated measurements on different slices of the virtual stack (Coleman and Colbert, 2007). The following variables describing 3D tissue proportions and structural organization were digitally measured or calculated: Ve, the volume of the enamel cap (mm3); Vcdp, the volume of the coronal dentine, including the coronal aspect of the pulp chamber (mm3); Vc, the total crown volume, including enamel, dentine, and pulp (mm3); SEDJ, the enamel–dentine junction (EDJ) surface (mm2); Vcdp/Vc (5100 3 Vcdp/Vc), the percent of coronal volume that is dentine and pulp (%); 3D AET (5Ve/SEDJ), the 3D average enamel thickness (mm); 3D RET [5100 3 3D AET/(Vcdp1/3)], the scale-free 3D relative enamel thickness (see Kono, 2004; Olejniczak et al., 2008a). Repeated intraobserver tests for measurement accuracy revealed differences inferior to 4%.

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The results were compared to similar 3D evidence from the following specimens/samples: late Lower Pleistocene H. erectus/ergaster from Mulhuli-Amo, Eritrea (HEA; Zanolli et al., 2014); early Middle Pleistocene North African H. heidelbergensis from Tighenif, Algeria (HHNA; Zanolli and Mazurier, 2013); Neanderthals (NEA; Olejniczak et al., 2008a; Kupczik and Hublin, 2010; Macchiarelli et al., 2013; NESPOS Database, 2014); African fossil modern humans (AFMH; Kupczik and Hublin, 2010); and extant humans (EH; Olejniczak et al., 2008a; and original data). The presence and degree of expression at the enameldentine junction (EDJ) level of nonmetric features have been scored following Ortiz et al. (2012) for the Carabelli trait, Skinner et al. (2008a) for the accessory cusps and protostylid, Bailey et al. (2011) and Martınez de Pinillos et al. (2014) for the mid-trigonid crest pattern (see also Macchiarelli et al., 2006), and Martinon-Torres et al. (2014) for the talonid crest. Geometric morphometric (GM) analyses of the EDJ were performed on the unsmoothed virtual surfaces of the five lower molar crowns represented in the Javanese H. erectus sample by placing four landmarks at the apex of the protoconid, metaconid, entoconid, and hypoconid and three additional landmarks at each intermediate lowest point between two dentine horns along the dentine marginal ridge, except between the two distal dentine horns (see Zanolli et al., 2014). Using the package Morpho v.2.0.2 (Schlager, 2014) for R v.3.0.2 (R Development Core Team, 2014), a generalized Procrustes analysis (GPA) and a weighted between-group principal component analysis (bgPCA) based on the Procrustes shape coordinates (Mitteroeker and Bookstein, 2011) were performed. Allometry was tested using the coefficient of determination (R2) of a multiple regression (Bookstein, 1991) in which the explicative variable is the centroid size and the dependent variables are the bgPC scores (see also Mitteroecker et al., 2013). A 10,000 iterations permutations test allowed the statistical assessment of intergroup differences. For the specific purposes of this analysis, uniquely considering mandibular molars, three H. heidelbergensis specimens from Tighenif (HHNA: 1 M2 and 2 M3s; Zanolli and Mazurier, 2013), 12 Neanderthal crowns from Regourdou, France, and Krapina, Croatia (NEA: 7 M2s and 5 M3s; NESPOS Database, 2014), and 26 extant human molars (EH: 17 M2s and 9 M3s; original data) were used. The MA 93 H. erectus/ergaster M1/2 specimen from the Eritrean Danakil (HEA; Zanolli et al., 2014) was projected a posteriori in the bgPCA analysis.

RESULTS The descriptive and comparative results of the analyses for assessing 3D tissue proportions (variables Vcd/Vc, 3D AET and 3D RET) are shown in Table 1 (see also Supporting Information Table S1 for surface and volumetric variables). The two maxillary molars represented in the present Javanese H. erectus sample exhibit crown dentine percent values (Vcd/Vc) slightly lower than those measured in Neanderthals (Olejniczak et al., 2008a). Rather, given also the relatively worn condition characterizing the specimen NG91-G10 n 1 UM1/2, both crowns more closely fit the modern human figures (Table 1 and Fig. 1A). Similarly, even if nearing one estimate from the North African H. heidelbergensis assemblage of Tighenif American Journal of Physical Anthropology

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C. ZANOLLI TABLE 1. 3D tooth tissue proportions of seven upper (UMs) and lower(LMs) Javanese H. erectus molars compared to some Pleistocene and extant specimens/samples Vcdp/Vc (%)

Ums NG91-G10 n 1 NG0802.1 NEA

M1/2 M3 M1 (2) M2 (4) M3 (9)

EH

M1 (5) M2 (5) M3 (14)

LMs NG0802.3 NG92.3 NG92 D6 ZE 57s/d 76 NG0802.2 NG9107.2 HEA HHNA NEA

M1/2 (1) M2 (1) M3 (1) M2 (11)

M2 (3) M3 (2)

EH

M2 (26) M3 (14)

3D RET

1.1 1.5

16.3a 27.7

Mean Range Mean Range Mean Range

58.1 57.4–58.8 58.9 56.3–61.7 58.6 54.1–66.1

1.1 1.1–1.1 1.1 1.0–1.1 1.1 0.9–1.2

14.5 13.9–15.1 15.3 13.7–17.6 15.6 11.6–18.4

Mean Range Mean Range Mean Range

58.8 57.0–61.5 50.6 48.6–53.3 46.1 37.8–52.1

1.1 0.8–1.6 1.5 1.3–1.8 1.5 0.9–1.9

16.6 12.6–23.5 23.9 20.5–31.6 27.2 14.5–34.1

M2 M2/3 M2/3 M2/3 M3

M3 (13) AFMH

54.7 42.4

3D AET (mm)

47.7 49.1 51.1 45.8 52.8

Mean Range Mean Range Mean Range Mean Range Mean Range Mean Range

56.0 57.4 50.0 57.1 51.0–64.2 58.1 47.2–68.6 53.4 50.4–56.6 51.0 49.3–52.7 51.0 42.7–57.3 49.4 44.7–55.4

1.3 1.3 1.3 1.4 1.1 1.0 1.2 1.5 1.1 0.8–1.3 1.1 0.8–1.4 1.3 1.2–1.4 1.3 1.3–1.4 1.3 0.7–2.3 1.3 1.0–1.9

22.1 21.0 19.0 23.6 18.0 14.7 15.0 20.3 15.4 11.9–20.9 16.2 12.7–21.8 17.6 14.7–19.9 19.1 16.9–21.3 20.2 12.6–40.7 21.6 17.8–27.8

AFMH: African fossil modern humans (Kupczik and Hublin, 2010); EH: extant humans (Olejniczak et al., 2008a; and original data); HEA: H. erectus/ergaster from Eritrea (Zanolli et al., in press); HHNA: H. heidelbergensis from Algeria (Zanolli and Mazurier, 2013); NEA: Neanderthals (Olejniczak et al., 2008a; Kupczik and Hublin, 2010; Macchiarelli et al., 2013; NESPOS Database, 2014). See the text for the meaning of the variables. a Moderately worn crown.

(Zanolli and Mazurier, 2013) and the lower limits of the Neanderthal sample, the signal expressed for the same variable by the five lower molars from Sangiran better approximates the modern structural condition (Fig. 1B). The only African H. erectus/ergaster specimen available for comparison (the MA 93 lower M1/2 from Eritrea) displays a higher Vcdp/Vc ratio (Zanolli et al., 2014). For enamel thickness, while the 3D AET values of the Javanese sample are hardly distinguishable from the global variation expressed by the comparative fossil and extant specimens/samples used in this study, the values of the relative enamel thickness (3D RET) are almost invariably higher (Table 1). This thick-enameled condition characterizing Indonesian H. erectus can be fully appreciated through the virtual cartographies imaged in Figure 2, which map topographic thickness variation at the outer enamel surface (OES) and facilitate the site-specific and synthetic comparative assessment of this variable (Macchiarelli et al., 2008). While exhibiting absolutely thicker enamel American Journal of Physical Anthropology

spread across the entire occlusal basin, the molars from the Sangiran Dome share a similar distribution pattern with African H. heidelbergensis and with extant humans, where the thickest enamel is commonly found on the lingual aspect of the protocone and on the buccal aspect of the hypoconid, on the upper and lower molars, respectively (Fig. 2). In this comparative context, the H. erectus/ergaster Eritrean specimen and the Neanderthal specimens similarly display relatively thicker enamel located on the lateral aspect of the functional cusps, but an absolutely thinner occlusal enamel. For each of the seven molar crowns forming the newly described H. erectus sample from Sangiran, the OES and corresponding morphology at the EDJ are rendered in Figure 3. While moderately worn, the UM1/2 specimen NG91G10 n 1 shows four well-developed occlusal cusps (Zanolli, 2013). When its enamel cap is virtually removed, in addition to the four corresponding dentine horns, its EDJ displays: two accessory cuspules lying at

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Fig. 1. 3D tooth tissue proportions of seven Javanese H. erectus (HEJ) molars compared to some Pleistocene and extant specimens/samples. (A, C): upper molars; (B, D): lower molars. Vcdp/Vc: percent of crown dentine (A, B); 3D RET: 3D relative enamel thickness (C, D). AFMH: African fossil modern humans (Kupczik and Hublin, 2010); EH: extant humans (Olejniczak et al., 2008a; and original data); HEA: H. erectus/ergaster from Eritrea (considered here as a LM2; Zanolli et al., in press); HHNA: H. heidelbergensis from Algeria (Zanolli and Mazurier, 2013); NEA: Neanderthals (Olejniczak et al., 2008a; Kupczik and Hublin, 2010; Macchiarelli et al., 2013; NESPOS Database, 2014).

the middle of the thin but sharp mesial marginal ridge; a mesial crest linking the anterior paracone aspect of the mesial marginal ridge to a similarly mesially located point set in front of the protocone, encircling a small mesial fovea; a Carabelli’s trait expressed as a mediumsized Y-shaped depression (grade 3; Ortiz et al., 2012); a low, segmented transversal ridge and an elevated uninterrupted oblique crest; and three short accessory crests in the occlusal basin (Fig. 3A). At the pulp chamber level, only the four main cusps and the oblique crest are expressed. The UM3 specimen NG0802.1, which exhibits a rather mesiodistally compressed outline (Fig. 3A), bears a small protoconule, a large paracone with an accessory cusp lying on its distal aspect, a centrally placed metacone and no hypocone. Carabelli’s trait is expressed as a deep but narrow pit (see Zanolli, 2013). At the EDJ level, this

tooth shows more distinct protoconule, paracone, accessory cusp and metacone apices, as well as a larger, but not Y-shaped, fossa expression of Carabelli’s trait (cf. grade 4 in Ortiz et al., 2012). Both externally and internally, there is no epicrista (only two short segments running lingually from the paracone are barely visible) nor crista obliqua (possibly fused with the distal marginal ridge). At the pulp chamber level, only three horns are detectable in this specimen, with the larger buccal one possibly corresponding to the fusion of paracone and metacone (Fig. 3A). The LM2 NG0802.3 and the LM2/3 NG92 D6 ZE 57s/d 76 crowns show only the four main cusps. In contrast, the LM2/3s NG92.3 and NG0802.2 crowns (Fig. 3B), display four well developed cusps, a small hypoconulid, and a fovea-type C6 (Skinner et al., 2008a). Finally, the presence of five cusps originally observed on the slightly American Journal of Physical Anthropology

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worn outer surface of the LM3 specimen NG9107.2 (Zanolli, 2013) is here confirmed at the EDJ, where also a small fovea-type C6 is found (Fig. 3B). As already reported at the OES (Zanolli, 2013), none of the five Javanese lower molars displays any expression of a tuberculum intermedium (C7) at the EDJ level

(Fig. 3B). Externally, all exhibit a thick interrupted midtrigonid crest (Zanolli, 2013). However, the exploration and 3D rendering of their inner structure reveal a certain degree of morphological variation in the expression of the crest pattern. The trigonid crest is expressed by different combinations of interrupted ridges at the EDJ. Except in the case of the LM2 NG0802.3 that lacks any metaconid crest component (grade 0; Bailey et al., 2011), the EDJ of all the other specimens exhibit at least two middle crest segments running from the protoconid and the metaconid (grade 1; Bailey et al., 2011). The LM2/3s crowns NG92.3 and NG92 D6 ZE 57s/d 76 display a discontinuous mesial trigonid crest expressed at the dentine surface. At the EDJ, their interrupted distal trigonid crest pattern consists of one or more arms originating from the distal segment of the mesial cusps (type 4; Martinez de Pinillos et al., 2014). Also, in the LM2 NG0802.3 and LM2/3 NG0802.2 specimens, an interrupted crest links the distal aspect of the trigonid crest to the tip of the entoconid (type 3; Martinon-Torres et al., 2014). On the contrary, the LM2/3 crown NG92.3 exhibits no expression of this trait, but only a faint accessory ridge located mesially to the entoconid. A different kind of talonid crest pattern is expressed by the LM2/3 specimen NG92 D6 ZE 57s/d 76, with the presence of a crest positioned distally to the distal trigonid crest, which runs briefly from the metaconid in distobuccal direction (type 6; Martinon-Torres et al., 2014). The EDJ of the LM3 specimen NG9107.2 is more complex, including two short crests running from the lingual marginal ridge towards the centre of the occlusal basin and, similarly to NG92 D6 ZE 57s/d 76 (LM2/3) and NG0802.2 (LM2/3), also multiple ridges arising from the entoconid (type 4; Martinon-Torres et al., 2014). Another OES-EDJ structural discrepancy observed within the Javanese sample of lower permanent molars concerns the protostylid. While this feature is absent externally (Zanolli, 2013), it is systematically found at the EDJ level, even if always very weakly expressed in form of a minor furrow on the protoconid buccal aspect (type b; Skinner et al., 2008a) and, in two cases (the LM2/3 NG92.3 and LM3 NG9107.2), it only represents a faint feature on the buccal aspect between hypoconid and hypoconulid (type c; Skinner et al., 2008a). As a whole, except for two specimens where the inner morphology has been partially altered by taphonomic processes (NG0802.3 and NG0802.2), the pulp chamber preserved in the three remaining lower molar crowns from Java show rather high and well-distinguished

Fig. 2. Enamel thickness cartographies of seven Javanese H. erectus upper (A) and lower (B) molars in occlusal view compared to similar evidence from some Pleistocene and extant selected specimens. Topographic thickness variation is rendered by a pseudo-color scale ranging from thinner dark-blue to thicker red; isolated white spots correspond to enamel removal following wear. EH: extant humans (original data); HEA: H. erectus/ergaster from Eritrea (spec. MA 93; Zanolli et al., in press): HHNA: H. heidelbergensis from Algeria (spec. Tighenif 2 [LM2 and LM3]; Zanolli and Mazurier, 2013): NEA: Neanderthals (spec. Krapina D171 [UM1], D135 [UM2], D170 [UM3], D10 [LM2] and D108 [LM3]; NESPOS Database, 2014). Independently from their original side, all upper molars are shown as left, whereas the lower molars are displayed as right antimeres. Scale bar 5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

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Fig. 3. Virtual rendering of the seven Javanese H. erectus upper (A) and lower (B) molars. For each specimen, the outer enamel surface (rows a and b) and the enamel-dentine junction (rows c and d) are illustrated in occlusal and occluso-buccal views, while the virtually extracted pulp cavity (row e) is only shown in occluso-buccal view. Independently from their original side, all upper molars are shown as left, whereas the lower molars are displayed as right antimeres. Scale bar 5 mm. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

horns corresponding to the four or five main outer cusps (Fig. 3). The results of the between-group PCA analysis (bgPCA) realized on the generalized Procrustes coordinates in the shape space of the lower M2 and M3 EDJ conformation are shown in Figure 4. The first two components (bgPC1 and bgPC2) respectively show a weak allometric signal (R2 5 0.12) and no size-dependent shape variation (R2 5 0.00), mostly representing shape variation. Along the bgPC1, all five Javanese H. erectus specimens considered in this analysis show positive values and thus more closely approximate the extant human condition, characterized by nearly equidistant and equally elevated dentine horns. On the other hand, mostly found within the negative values and basically resulting from a more mesiodistally elongated trigonid (as indicated by a more distally set hypoconid), a deeper mesial marginal ridge and a buccolingually narrower EDJ outline, the conformations of North African H. heidelbergensis and Neanderthals are quite distinct. The bgPC2 axis separates the high and regularly-set dentine horn configuration (as seen in the modern human M2s found in the positive space) from the lingually stretched EDJ conformation (where metaconid and entoconid are more closely set to each other and separated from the buccal horns) and the lower reliefs (such as those of the extant human M3s found in the negative space). The results of the permutation tests indicate that the endostructural shape of the Indonesian H. erectus lower molars is statistically distinct from that of North African

H. heidelbergensis and Neanderthals, while it does not significantly deviate from the modern human pattern (Table 2).

DISCUSSION Information on the inner structural organization and tissue proportions in H. erectus s.l. teeth is still rather scanty (Dean et al., 2001; Dean and Smith, 2009; Smith et al., 2009, 2012; Zanolli et al., 2012, 2014). Although samples are small and consist of isolated crowns lacking roots, the availability of a high resolution microtomographic record of a newly reported sample of permanent molars from the Sangiran Dome (Zanolli, 2011, 2013) thus offers, for the first time, a unique opportunity to characterize in a 3D perspective the condition displayed by Indonesian H. erectus s.s. Previous bidimensional (2D) studies based on natural, histological, or virtual sections of permanent molars have revealed the absolutely and relatively thick-enameled condition of H. erectus s.s. (in Smith et al., 2012). Similarly, the mCT-based 3D assessment of this feature in two deciduous and one permanent molars from the late Lower-Early Middle Pleistocene fossiliferous levels outcropping in the Sangiran area (Zanolli et al., 2012; Macchiarelli et al., 2013) showed a structural condition more closely approximating the thickly-enameled modern human pattern than the absolutely and relatively thinner Neanderthal figures (Olejniczak et al., 2008a). Despite the wide range of enamel thickness variation recorded in fossil and extant human molars, evidence American Journal of Physical Anthropology

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Fig. 4. Between-group principal component analysis (bgPCA) of the Procrustes shape coordinates of the EDJs of five Javanese H. erectus lower molars compared to some Pleistocene and extant specimens/samples. EH: extant humans (original data); HEA: H. erectus/ergaster from Eritrea (Zanolli et al., in press); HHNA: H. heidelbergensis from Algeria (Zanolli and Mazurier, 2013); NEA: Neanderthals (Macchiarelli et al., 2013; NESPOS Database, 2014). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

that tends to weaken the value of such trait for assessing intertaxic evolutionary relationships (Smith et al., 2012), two patterns emerge in the comparative context specifically considered in the present study. On the one hand, a condition of intermediate-thick enamel (sensu Martin, 1985) is shared by the only African H. erectus/ ergaster representative available for comparison (see also Smith et al., 2012 for 2D estimates; Zanolli et al., 2014) and the Neanderthals (Olejniczak et al., 2008a) while, on the other hand, relatively and absolutely thicker enamel is systematically found in Indonesian H. erectus, North African H. heidelbergensis, fossil and extant modern humans. However, it is noteworthy here that, while common in Australopithecus and Paranthropus (Olejniczak et al., 2008b) and also found in extant humans (Olejniczak et al., 2008a; Smith et al., 2012), in the human fossil record the hyper-thick condition displayed by the UM3 Javanese specimen NG0802.1 (3D RET 5 27.7) has been reported so far only for a UM2 from South Africa attributed to early Homo (SK 27; Smith et al., 2012). It has been hypothesized that the thicker enamel of early hominin molars was achieved through a different developmental mechanism than in recent humans (Dean et al., 2001). Indeed, the modern human pattern results from the well-documented overall size reduction from the first to the third molar, which can be attained through a differential loss of the dentine component (Grine, 2002, 2005). Interestingly, compared to the Lower Pleistocene figures, the postcanine dentition of Lower-Middle Pleistocene Javanese H. erectus exhibits such marked reduction trend (Kaifu, 2006; Zanolli, 2013) and the results of the present endostructural analysis also provide 3D RET estimates overlapping the extant human values. With this respect, fresh evidence from the early Middle Pleistocene dentognathic assemblage of Tighenif, Algeria, revealed a previously unreported mosaic of features characterizing both decidAmerican Journal of Physical Anthropology

uous and permanent crowns (Zanolli et al., 2010; Zanolli and Mazurier, 2013; see also Bailey et al., 2014). In particular, together with a megadont-like condition, the slightly worn LM3 of the Tighenif 2 left hemi-mandible closely approximates the thick enamel (3D RET) and low crown dentine percent (Vcd/Vc) values reported here for Javanese H. erectus (Zanolli and Mazurier, 2013). In accordance with their outer occlusal morphology, the five lower molars from the Kabuh Formation of the Sangiran Dome exhibit at the EDJ only an interrupted trigonid and talonid crest pattern, but never welldeveloped and complete ridges, a condition which contrasts with the fully developed mid-trigonid crest found in the H. erectus/ergaster LM1/2 from Mulhuli-Amo, Eritrea (Zanolli et al., 2014). Indeed, absence or incomplete expression of this trait at the EDJ has been recorded in only 16.7% (1/6) of A. africanus lower permanent molars (Bailey et al., 2011), in 7% (3/43) of those from the Middle Pleistocene sample of Atapuerca Sima de los Huesos (Martınez de Pinillos et al., 2014), and from 1.4% (1/73) to 2.9% (1/34) of cases in Neanderthals (Bailey et al., 2011; Martınez de Pinillos et al., 2014). The molars of the European H. heidelbergensis mandible from Mauer also lack a mid-trigonid crest pattern (Bailey et al., 2011), whereas this trait is well-expressed in 57% (4/7) of the North African H. heidelbergensis crowns from Tighenif investigated so far for their EDJ structural morphology (Zanolli and Mazurier, 2013). Variably expressed interrupted trigonid crests are also common in extant humans, their frequency fluctuating from 53.6% (15/28) to 64.7% (44/68) (Bailey et al., 2011; Martınez de Pinillos et al., 2014). The inner structural investigation of the Javanese H. erectus lower molars also revealed some degree of expression of the talonid crest pattern (notably, types 3, 4, and 6) absent in the assemblage from Atapuerca Sima de los Huesos (0/63) or in modern humans (0/32), and also rare in Neanderthals (3/40) (Martinon-Torres et al., 2014). The 3D geometric morphometric analysis of the lower molar EDJ shape has revealed a distinct morphology with respect to the condition displayed by the African specimens from Eritrea (H. erectus/ergaster) and Tighenif (H. heidelbergensis) available for direct comparison (Zanolli, 2012; Zanolli and Mazurier, 2013; Zanolli et al., 2014), but also some similarities with the modern human pattern. Indeed, all African fossil crowns used in this analysis share a relatively low EDJ topography associated to a mesiodistally elongated occlusal basin, to some extent reminiscent of the ancestral hominin condition (Macchiarelli et al., 2004; Olejniczak et al., 2008b; Skinner et al., 2008b; Braga et al., 2010). Conversely, the five Javanese H. erectus lower molars display more elevated horns and derived morphology, different from the Neanderthal pattern, but closely approximating the extant human conformation. As shown by other studies, the EDJ shape analysis rather distinctly discriminates among the hominin taxa, even in the case of isolated teeth (e.g., Skinner et al., 2008b; Crevecoeur et al., 2014). However, while the molars from the Kabuh Formation of the Sangiran Dome clearly share a number of features with the modern condition, the lack of adequate information from larger comparative fossil samples, either from Africa and continental Asia, currently prevents any reliable conclusion about the meaning of such similarities in an adaptive evolutionary perspective.

JAVANESE HOMO ERECTUS INNER MOLAR STRUCTURE TABLE 2. P values of pairwise group differences of lower molar endostructural shape based on 10,000 permutations

HEJ HHNA EH

HHNA

EH

NEA

0.010**

0.718 0.018*

0.016* 0.038* 0.001**

EH: extant humans; HEJ: Javanese H. erectus (present study); HHNA: H. heidelbergensis from Algeria; NEA: Neanderthals. *P  0.05. **P  0.01.

CONCLUSIONS The fossil hominid dentognathic assemblage from the Lower Pleistocene Pucangan (Sangiran) Formation and "Grenzbank Zone" and the Lower-Middle Pleistocene Kabuh (Bapang) Formation, Java, consists of c. 230 dental elements, mostly including isolated permanent molars, whose taxonomic assessment and phylogenetic relationships revealed to be frequently controversial (e.g., Anton, 2003; Kaifu et al., 2005; Smith et al., 2009; Zanolli et al., 2014b). This is mainly due to the marked morphodimensional variability expressed by the assemblage as a whole, but also to uncertainties related to the geo-chronological and stratigraphical provenance of some specimens, and even to the convergence (homoplasy) in molar crown size and outer occlusal morphology between Homo and the Ponginae (rev. in Smith et al., 2009). In addition, the climatic-related eustatic oscillations occurred through the Plio-Pleistocene (Rohling et al., 2014) led to intermittent phases of evolution in isolation from the northern continental demes and impacted the local paleobiodiversity (van den Geer, 2010). Recent work also convincingly suggests that some time-related changes in human dentognathic structural morphology observed within the Javanese hypodigm more likely resulted either from replacement and/or introgression by admixture with continental immigrating groups, rather than from intra-population local microevolution alone (Kaifu et al., 2005; Kaifu, 2006; Zaim et al., 2011). In this complex scenario, the inner analysis of the H. erectus permanent molar teeth from the late LowerEarly Middle Pleistocene Kabuh Formation of the Sangiran Dome has revealed a set of morphostructural characteristics distinct from those reported so far for some roughly penecontemporaneous African assemblages (Bailey et al., 2011; Zanolli and Mazurier, 2013; Martinon-Torres et al., 2014; Zanolli et al., 2014) as well from those of Neanderthals (e.g., Macchiarelli et al., 2006, 2013; Olejnickzak et al, 2008a), but otherwise relatively common in recent human populations (e.g., Bailey et al., 2011; Zanolli and Mazurier, 2013). This is in agreement with previous conclusions based on the study of their outer crown morphology (Zanolli, 2013), and is also consistent with the evidence for a relatively “modern-like” signature revealed by the microtomographic-based analysis of two deciduous molars collected near the village of Pucung, in the Sangiran area, likely coming from the same chronostratigraphical context (Zanolli et al., 2012). High resolution virtual tooth imaging coupled with 3D structural (including tissue proportions) and GM analyses of the enamel-dentine junction have the potential for allowing more accurate inter-taxic comparisons than those uniquely based on outer enamel morphology (e.g., Macchiarelli et al., 2008; Smith and Hublin, 2008; Smith

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and Tafforeau, 2008; Skinner et al., 2008a, b; Smith et al., 2012; Macchiarelli et al., 2013; Zanolli and Mazurier, 2013; Crevecoeur et al., 2014). However, the interpretation of the evidence for a certain degree of similarity recorded in this study between late LowerEarly Middle Pleistocene Javanese H. erectus and modern human figures remains open. This resemblance in dental structural organization could be either related to a convergence under a "random walk" evolutionary scenario (e.g., Gomez-Robles et al., 2014), or to a certain degree of evolutionary continuity at macro-regional/continental scale (e.g., Wolpoff and Caspari, 2013), or could simply represent a nearly unavoidable effect of structural arrangement following crown size reduction. The lack of directly comparable data from the Lower Pleistocene tooth remains of the Pucangan Formation and the "Grenzbank Zone" of Sangiran (Smith et al., 2009; Zanolli, 2011), as well as Middle Pleistocene continental Southeast Asia (but see Liu et al., 2013 for late Middle Pleistocene southern China), currently inhibit any conclusive statement about the biological signification of such evidence. Further research in virtual dental paleoanthropology to be developed at macroregional scale would better clarify the polarity and intensity of the intermittent exchanges between continental and insular Southeast Asia around the Lower to Middle Pleistocene boundary, as well as shed light on the still poorly understood longitudinal evolutionary dynamics across continental Asia (Martinon-Torres et al., 2007).

ACKNOWLEDGEMENTS This study, which forms part of my PhD research work realized under the scientific direction of R. Macchiarelli and co-directed by D. Grimaud-Herve, has been possible thank to the long-term collaboration among the MNHN Paris, the Pusat Penelitian Arkeologi of Jakarta, and the Balai Pelestarian Situs Manusia Purba of Sangiran. For having granted access to the collections of fossil hominid teeth stored at Java, I am deeply indebted to H. Widianto and F. Semah; D. Grimaud-Herve assured the temporary transport of the investigated specimens in France for analysis. I am also sincerely grateful to C. Hertler, O. Kullmer, F. Schrenk, and V. Volpato for allowing me access to the fossil collections at the Senckenberg Museum of Frankfurt, and also for their scientific collaboration and warm hospitality during my stay in Frankfurt. In France, C. Argot, A. Froment, C. Lefe`vre, H. Lelie`vre, and P. Mennecier allowed the comparative analysis of extant and fossil specimens stored at the MNHN Paris, and C. Braquard and D. Bouchon put at disposition materials from the zoological collections of the Univ. of Poitiers. For his exceptional analytical support at the Centre de Microtomographie set at the Univ. of Poitiers (CdM), special thanks are due to A. Mazurier, as well as to R. Macchiarelli and P. Sardini for technical and scientific supervision. The virtual depository of the NESPOS Society (http://www.nespos.org) provided useful comparative information. For direct scientific contribution and/or for discussion and comments to the results presented in this study, I sincerely thank P. Bayle, A. Beaudet, F. Bernardini, L. Bondioli, J. Braga, A. Coppa, M.C. Dean, E. Delson, F. Detroit, F.E. Grine, O. Kullmer, A. Le Cabec, R. Macchiarelli, M. Martinon-Torres, L. Mancini, B. Maureille, A. Mazurier, P. O’Higgins, L. Puymerail, M. Skinner, T. Smith, C. Tuniz, T.B. Viola, and B. Wood. Research partially granted by the German Deutscher American Journal of Physical Anthropology

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C. ZANOLLI

Akademischer Austauschdienst and by the French Societe des Amis du Musee de l’Homme, supported by the French INEE-CNRS and the ICTP of Trieste.

LITERATURE CITED Anton SC. 2003. Natural history of Homo erectus. Yearb Phys Anthopol 46:126–170. Bailey SE, Hublin JJ. 2013. What does it mean to be dentally "modern"? In: Scott GR, Irish JD, editors. Anthropological perspectives on tooth morphology. Genetics, evolution, variation, Cambridge: Cambridge University Press. p 222–249. Bailey SE, Benazzi S, Souday C, Astorino C, Paul K, Hublin JJ. 2014. Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens, Homo neanderthalensis and Homo erectus. J Hum Evol. doi: 10.1016/j.jhevol.2014.02.008). Bailey SE, Skinner MM, Hublin JJ. 2011. What lies beneath? An evaluation of lower molar trigonid crest patterns based on both dentine and enamel expression. Am J Phys Anthropol 145:505–518. Bettis III EA, Milius AK, Carpenter SJ, Larick R, Zaim Y, Rizal Y, Ciochon RL, Tassier-Surine SA, Murray D, Suminto, Bronto S. 2009. Way out of Africa: Early Pleistocene paleoenvironments inhabited by Homo erectus in Sangiran, Java. J Hum Evol 56:11–24. Bookstein FL. 1991. Morphometric tools for landmark data: geometry and biology, Cambridge: Cambridge University Press. Braga J, Thackeray JF, Subsol G, Kahn JL, Maret D, Treil J, Beck A. 2010. The enamel–dentine junction in the postcanine dentition of Australopithecus africanus: intra-individual metameric and antimeric variation. J Anat 216:62–79. Coleman MN, Colbert MW. 2007. Technical note: CT thresholding protocols for taking measurements on three-dimensional models. Am J Phys Anthropol 133:723–725. Crevecoeur I, Skinner MM, Bailey SE, Gunz P, Bortoluzzi S, Brooks AS, Burlet C, Cornelissen E, De Clerck N, Maureille B, Semal P, Vanbrabant Y, Wood BA. 2014. First early hominin from Central Africa (Ishango, Democratic Republic of Congo). PLoS One 9:e84652. doi: 10.1371/journal.pone.0084652). Dean MC, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628–631. Dean MC, Smith BH. 2009. Growth and development in the Nariokotome Youth, KNM-WT 15000. In: Grine FE, Fleagle JG, Leakey, RE, editors. The first humans: origin of the genus Homo, New York: Springer. p 101–120. de Vos J, Long VT. 2001. First settlements: relation between continental and insular southeast Asia. In: S emah AM, Semah F, Falgu eres C, Grimaud-Herv e D, editors. Origine des peuplements et chronologie des cultures Pal eolithiques dans le Sud-Est Asiatique, Paris: Artcom’. p 331–358. Djubiantono T, S emah. 1991. Lower Pleistocene marinecontinental transitional beds in the Solo depression and their relation to the environment of the Pucangan hominids. Bull Indo-Pac Prehist Assoc 11:7–13. Fajardo RJ, Ryan TM, Kappelman J. 2002. Assessing the accuracy of high-resolution X-ray computed tomography of primate trabecular bone by comparisons with histological sections. Am J Phys Anthropol 118:1–10. Gomez-Robles A, Berm udez de Castro JM, Arsuaga JL, Carbonell E, Polly PD. 2013. No known hominin species matches the expected dental morphology of the last common ancestor of Neanderthals and modern humans. Proc Natl Acad Sci USA 110:18196–18201. Grine FE. 2002. Scaling of tooth enamel thickness, and molar crown size reduction in modern humans. S Afr J Sci 98:503– 509. Grine FE. 2005. Enamel thickness of deciduous and permanent molars in modern Homo sapiens. Am J Phys Anthropol 126:14–31. Kaifu Y. 2006. Advanced dental reduction in Javanese Homo erectus. Anthropol Sci 114:35–43.

American Journal of Physical Anthropology

Kaifu Y, Baba H, Aziz F, Indriati E, Schrenk F, Jacob T. 2005. Taxonomic affinities and evolutionary history of the Early Pleistocene hominids of Java: dentognathic evidence. Am J Phys Anthropol 128:709–726. Kono R. 2004. Molar enamel thickness and distribution patterns in extant great apes and humans: new insights based on a 3-dimensional whole crown perspective. Anthropol Sci 112:121–146. Kupczik K, Hublin JJ. 2010. Mandibular molar root morphology in Neanderthals and Late Pleistocene and recent Homo sapiens. J Hum Evol 59:525–541. Liu W, Schepartz LA, Xing S, Miller-Antonio S, Wu X, Trinkaus E, Martin on-Torres M. 2013. Late Middle Pleistocene hominin teeth from Panxian Dadong, South China. J Hum Evol 64: 337–355. Macchiarelli R, Bayle P, Bondioli L, Mazurier A, Zanolli C. 2013. From outer to inner structural morphology in dental anthropology. The integration of the third dimension in the visualization and quantitative analysis of fossil remains. In: Scott GR, Irish JD, editors. Anthropological perspectives on tooth morphology. Genetics, evolution, variation, Cambridge: Cambridge University Press. p 250–277. Macchiarelli R, Bondioli L, Deb enath A, Mazurier A, Tournepiche JF, Birch W, Dean MC. 2006. How Neanderthal molar teeth grew. Nature 444:748–751. Macchiarelli R, Bondioli L, Falk D, Faupl P, Illerhaus B, Kullmer O, Richter W, Said H, Sandrock O, Sch€ afer K, Urbanek C, Viola BT, Weber GW, Seidler H. 2004. Early Pliocene hominid tooth from Galili, Somali Region, Ethiopia. Coll Anthropol 28:65–76. Macchiarelli R, Bondioli L, Mazurier A. 2008. Virtual dentitions: Touching the hidden evidence. In: Irish JD, Nelson GC, editors. Technique and application in dental anthropology, Cambridge: Cambridge University Press. p 426–448. Martin LB. 1985. Significance of enamel thickness in hominoid evolution. Nature 314:260–263. Martınez de Pinillos M, Martin on-Torres M, Skinner MM, Arsuaga JL, Gracia-T ellez A, Martınez I, Martin-Franc es L, Berm udez de Castro JM. 2014. Trigonid crests expression in Atapuerca-Sima de los Huesos lower molars: internal and external morphological expression and evolutionary inferences. C R Palevol. doi: 10.1016/j.crpv.2013.10.008. Martin on-Torres M, Berm udez de Castro JM, G omez-Robles A, Arsuaga JL, Carbonell E, Lordkipanidze D, Manzi G, Margvelashvili A. 2007. Dental evidence on the hominin dispersals during the Pleistocene. Proc Natl Acad Sci 104: 13279–13282. Martin on-Torres M, Berm udez de Castro JM, G omez-Robles A, Prado-Sim on L, Arsuaga JL. 2012. Morphological description and comparison of the dental remains from Atapuerca-Sima de los Huesos site (Spain). J Hum Evol 62:7–58. Martin on-Torres M, Martınez de Pinillos M, Skinner MM, Martin-Franc es L, Gracia-T ellez A, Martınez I, Arsuaga JL, Berm udez de Castro JM. 2014. Talonid crests expression at the enamel–dentine junction of hominin lower permanent and deciduous molars. C R Palevol. doi: 10.1016/j.crpv.2013.12.002. Mitteroecker P, Bookstein FL. 2011. Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol Biol 38:100–114. Mitteroecker P, Gunz P, Windhager S, Schaefer K. 2013. A brief review of shape, form, and allometry in geometric morphometrics, with applications to human facial morphology. Hystrix 24:59–66. NESPOS Database. 2014. NEanderthal Studies Professional Online Service. http://www.nespos.org. Olejniczak AJ, Smith TM, Feeney RNM, Macchiarelli R, Mazurier A, Bondioli L, Rosas A, Fortea J, de la Rasilla M, Garcia-Tabernero A, Radovcˇic´ J, Skinner MM, Toussaint M, Hublin JJ. 2008a. Dental tissue proportions and enamel thickness in Neandertal and modern human molars. J Hum Evol 55:12–23. Olejniczak AJ, Smith TM, Skinner MM, Grine FE, Feeney RNM, Thackeray JF, Hublin JJ. 2008b. Three-dimensional

JAVANESE HOMO ERECTUS INNER MOLAR STRUCTURE molar enamel distribution and thickness in Australopithecus and Paranthropus. Biol Lett 4:406–410. Ortiz A, Skinner MM, Bailey SE, Hublin JJ. 2012. Carabelli’s trait revisited: an examination of mesiolingual features at the enamel–dentine junction and enamel surface of Pan and Homo sapiens upper molars. J Hum Evol 63:586–596. R Development Core Team. 2014. R: a language and environment for statistical computing. http://www.R-project.org. Rohling EJ, Foster GL, Grant KM, Marino G, Roberts AP, Tamisiea ME, Williams F. 2014. Sea-level and deep-seatemperature variability over the past 5.3 million years. Nature 508:477–491. Schlager S. 2014. Morpho: calculations and visualizations related to geometric morphometrics. R package version 2.0.2. http://cran.r-project.org/web/packages/Morpho/index.html. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. Semah AM, Semah F, Djubiantono T, Brasseur B. 2010. Landscapes and hominids’ environments: changes between the Lower and the Early Middle Pleistocene in Java (Indonesia). Quat Intl 223–224:451–454. Skinner MM, Gunz P, Wood BA, Hublin JJ. 2008b. Enamel-dentine junction (EDJ) morphology distinguishes the lower molars of Australopithecus africanus and Paranthropus robustus. J Hum Evol 55:979–988. Skinner MM, Wood BA, Boesch C, Olejniczak AJ, Rosas A, Smith TM, Hublin JJ. 2008a. Dental trait expression at the enamel–dentine junction of lower molars in extant and fossil hominoids. J Hum Evol 54:173–186. Smith TM, Hublin JJ. 2008. Dental tissue studies: 2D and 3D insights into human evolution. J Hum Evol 54:169–172. Smith TM, Olejniczak AJ, Kupczik K, Lazzari V, de Vos J, Kullmer O, Schrenk F, Hublin JJ, Jacob T, Tafforeau P. 2009. Taxonomic assessment of the Trinil molars using nondestructive 3D structural and development analysis. Paleo Anthropol 2009:117–129. Smith TM, Tafforeau P. 2008. New visions of dental tissue research: tooth development, chemistry, and structure. Evol Anthropol 17:213–226. Smith TM, Olejniczak AJ, Zermeno JP, Tafforeau P, Skinner MM, Hoffmann A, Radovcˇic´ J, Toussaint M, Kruszynski R, Menter C, Moggi-Cecchi J, Glasmacher UA, Kullmer O, Schrenk F, Stringer C, Hublin JJ. 2012. Variation in enamel thickness within the genus Homo. J Hum Evol 62:395–411. Spoor CF, Zonneveld FW, Macho GA. 1993. Linear measurements of cortical bone and dental enamel by computed tomography: applications and problems. Am J Phys Anthropol 91: 469–484. Suwa G, Asfaw B, Haile-Selassie Y, White TD, Shigehiro Katoh K, WoldeGabriel G, William KH, Nakaya H, Beyene Y. 2007. Early Pleistocene Homo erectus fossils from Konso, Southern Ethiopia. Anthropol Sci 115:133–151. van den Geer AAE, Lyras G, de Vos J, Dermitzakis M. 2010. Evolution of island mammals. Adaptation and extinction of placental mammals on islands, Chichester: Wiley-Blackwell.

157

Voris HK. 2000. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167. Weidenreich F. 1937. The dentition of Sinanthropus pekinensis: a comparative odontography of the hominids. Palaeontol Sin Ser D 1:1–180. Wolpoff MH. 1999. Paleoanthropology, 2nd ed. New York: McGraw Hill. Wolpoff MH, Caspari R. 2013. The origin of modern East Asians. Acta Anthropol Sin 32:377–410. Wood BA. 1991. Koobi Fora Research Project, Vol. 4. Hominid Cranial Remains from Koobi Fora, Oxford: Clarendon Press. Wood BA, Leakey M. 2011. The Omo-Turkana basin fossil hominins and their contribution to our understanding of human evolution in Africa. Evol Anthropol 20:264–292. Zaim Y, Ciochon RL, Polanski JM, Grine FE, Bettis III EA, Rizal Y, Franciscus RG, Larick RR, Heizler M, Aswan, Eaves KL, Marsh HE. 2011. New 1.5 million-year-old Homo erectus maxilla from Sangiran (Central Java, Indonesia). J Hum Evol 61:363–376. Zanolli C. 2011. L’organisation endostructurale de restes dentaires humains du Pl eistoce`ne inf erieur final-moyen initial  esie et d’Afrique, avec une attention particulie`re a d’Indon  haute Homo erectus s.s. Caract erisation comparative a r esolution et probl ematiques taxinomiques, PhD dissertation, Paris: Mus eum National d’Histoire Naturelle. Zanolli C. 2012. Comparative tooth crown endostructural morphology in two penecontemporaneous samples of Indonesian H. erectus (Sangiran) and African H. heidelbergensis (Tighenif). Proc Eur Soc Hum Evol 1:196. Zanolli C. 2013. Additional evidence for morpho-dimensional tooth crown variation in a new Indonesian H. erectus sample from the Sangiran Dome (Central Java). PLoS One 8:e67233. doi: 10.1371/journal.pone.0067233. Zanolli C., Mazurier A. 2013. Endostructural characterization of the H. heidelbergensis dental remains from the early Middle Pleistocene site of Tighenif, Algeria. C R Palevol 12:293–304. Zanolli C, Bacon A-M, Bondioli L, Braga J, Demeter F, Dumoncel J, Tuniz C, Macchiarelli R. 2014b. Lower Pleistocene hominid paleobiodiversity in Southeast Asia: evidence for a Javanese pongine taxon. Am J Phys Anthropol 153:281. Zanolli C, Bayle P, Macchiarelli R. 2010. Tissue proportions and enamel thickness distribution in the early Middle Pleistocene human deciduous molars from Tighenif, Algeria. CR Palevol 9:341–348. Zanolli C, Bondioli L, Coppa A, Dean MC, Bayle P, Candilio F, Capuani S, Dreossi D, Fiore I, Frayer DW, Libsekal Y, Mancini L, Rook L, Medin Tekle T, Tuniz C, Macchiarelli R. 2014. The late Early Pleistocene human dental remains from Uadi Aalad and Mulhuli-Amo (Buia), Eritrean Danakil: macromorphology and microstructure. J Hum Evol 74:96–113. Zanolli C, Bondioli L, Mancini L, Mazurier A, Widianto H, Macchiarelli R. 2012. Two human fossil deciduous molars from the Sangiran Dome (Java, Indonesia): outer and inner morphology. Am J Phys Anthropol 147:472–481.

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Molar crown inner structural organization in Javanese Homo erectus.

This contribution investigates the inner organizational pattern (tooth tissue proportions and enamel-dentine junction morphology) of seven Homo erectu...
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