Journal of Human Evolution 61 (2011) 363e376

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Journal of Human Evolution

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New 1.5 million-year-old Homo erectus maxilla from Sangiran (Central Java, Indonesia)
Yahdi Zaim a, Russell L. Ciochon b, *, Joshua M. Polanski c, Frederick E. Grine d, E. Arthur Bettis III e, Yan Rizal a, Robert G. Franciscus f, Roy R. Larick g, Matthew Heizler h, Aswan a, K. Lindsay Eaves f, Hannah E. Marsh f
a

Department of Geology, Institute of Technology Bandung, Bandung, Java 40132, Indonesia Department of Anthropology and Museum of Natural History, Macbride Hall, University of Iowa, Iowa City, IA 52242, USA Department of Anthropology, University of Arkansas, Fayetteville, AR 72701, USA d Departments of Anthropology and Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794, USA e Department of Geoscience, University of Iowa, Iowa City, IA 52242, USA f Department of Anthropology, University of Iowa, Iowa City, IA 52242, USA g Helios Laser, 160 East 238th Street, Euclid, OH 44123, USA h New Mexico Bureau of Mines and Mineral Resources, Socorro, NM 87801, USA
b c

a r t i c l e i n f o
Article history: Received 9 January 2009 Accepted 23 April 2011 Keywords: Southeast Asia Hominin evolution Homo habilis Grenzbank Zone Bapang formation Sangiran formation 40 Ar/39Ar dating Zhoukoudian Dmanisi

a b s t r a c t
Sangiran (Solo Basin, Central Java, Indonesia) is the singular Homo erectus fossil locale for Early Pleistocene Southeast Asia. Sangiran is the source for more than 80 specimens in deposits with 40Ar/39Ar ages of 1.51e0.9 Ma. In April 2001, we recovered a H. erectus left maxilla fragment (preserving P3- M2) from the Sangiran site of Bapang. The nd spot lies at the base of the Bapang Formation type section in cemented gravelly sands traditionally called the Grenzbank Zone. Two meters above the nd spot, pumice hornblende has produced an 40Ar/39Ar age of 1.51 0.08 Ma. With the addition of Bpg 2001.04, Sangiran now has ve H. erectus maxillae. We compare the new maxilla with homologs representing Sangiran H. erectus, Zhoukoudian H. erectus, Western H. erectus (pooled African and Georgian specimens), and Homo habilis. Greatest contrast is with the Zhoukoudian maxillae, which appear to exhibit a derived pattern of premolar-molar relationships compared to Western and Sangiran H. erectus. The dental patterns suggest distinct demic origins for the earlier H. erectus populations represented at Sangiran and the later population represented at Zhoukoudian. These two east Asian populations, separated by 5000 km and nearly 800 k.yr., may have had separate origins from different African/west Eurasian populations. 2011 Elsevier Ltd. All rights reserved.

Introduction Originally published under various names, Homo erectus fossils were rst found in the Far East at Trinil (in 1891), Zhoukoudian (in 1921), and Sangiran (in 1937). Initially, an East Asia origin for the species was deemed probable, but as African paleoanthropology ascended during the 1960s, the origins and taxonomy of H. erectus became largely an Afro-centric topic, with East Asian fossils representing a dispersal endpoint. However, as Eurasian paleoanthropology resurged during the 1990s, the spatial center-of-gravity for H. erectus has again shifted eastward. Three Eurasian sites now

* Corresponding author. E-mail address: russell-ciochon@uiowa.edu (R.L. Ciochon). 0047-2484/$ e see front matter 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2011.04.009

account for the vast majority of H. erectus fossils: Dmanisi, Sangiran, and Zhoukoudian. While the assumption remains that H. erectus emerged from an African hominin, the species had its greatest, and, possibly, earliest presence across southern Eurasia (see also Lepre and Kent, 2010). Here, we present a new Sangiran maxilla, increasing the number and known morphometric variation of Java H. erectus specimens. In 1998, the Institute of Technology Bandung and the University of Iowa began joint interdisciplinary research at Sangiran (Central Java, Indonesia). The program has focused on the hominin-bearing sedimentary sequence of the upper portion of the Sangiran Formation and the overlying Bapang Formation. More than 80 H. erectus fossils have been found in this sequence. The earliest H. erectus are found in sediments ranging in age from >1.5 Ma through to about 0.9 Ma (Larick et al., 2001; Ciochon et al., 2001). At

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Sangiran, the research focus has since turned to understanding the local conditions that sustained H. erectus on Sunda, the early Pleistocene emergent landmass currently represented by the Indonesian and Philippine archipelagos (Ciochon et al., 2003, 2007; Bettis et al., 2004, 2009a; Dizon and Pawlik, 2010; Larick and Ciochon, 2012). Sangiran is the only site that represents the early Pleistocene H. erectus population across all Southeast Asia. Work commenced with 40Ar/39Ar age analysis of volcanic heavy minerals, and interpreting the stratigraphic sequence as a set of sedimentary cycles. On April 22, 2001, local team member, Samingan, recovered a partial H. erectus maxilla (Bpg 2001.04) at the base of the Bapang Formation reference section, in a unit traditionally known as the Grenzbank Zone (Larick et al., 2000). The nd spot lay about 2 m below a level from which pumice hornblende produced an 40Ar/39Ar age of 1.51 0.08 Ma (Ciochon et al., 2005). The incontestable provenience linked directly with dated volcanic material makes this maxilla one of the oldest Sangiran dentate specimens. It lies within the geochronological range of H. erectus in Africa, and is twice as old as the oldest from Zhoukoudian in Northeast Asia (Shen et al., 2009). Along with specimens S4, S17, S27 and Tjg 1993.05, Bpg 2001.04 represents the fth H. erectus maxilla recovered from Sangiran. Here, we describe the specimen and its local geological and environmental context. We then turn to inter-site quantitative comparisons of basic maxillary dental morphology. Bpg 2001.04 is compared with the other Sangiran maxillary specimens, and with homologous materials from Northeast Asia, Southwest Eurasia, and Africa.

Geological and paleoclimate background H. erectus fossils are found in a long succession of lowland deposits exposed in the Sangiran area of Central Java (Figure 1a). The upper reaches of the Sangiran Formation contain the oldest H. erectus fossils in Southeast Asia, dating to 1.6 Ma, while the overlying Bapang Formation has yielded a large number of H. erectus remains dating to 1.5e0.9 Ma (Larick et al., 2001). During this period, depositional environments change from lake margin and marsh to riverine. The oldest H. erectus fossils occur as one component of the fully terrestrial and endemic island-type Ci Saat fauna, which occurs within dark-colored siltstones and mudstones in the upper reaches of the Sangiran Formation (Watanabe and Kadar, 1985; de Vos et al., 1994; Larick et al., 2001; Ciochon et al., 2003; Bettis et al., 2004). When H. erectus rst arrived in the Sangiran area, sometime between 1.66 Ma and 1.57 Ma, streams draining nearby volcanic highlands intermittently ooded the lake margins and marshes, and occasional volcanic eruptions deposited thin blankets of ash (Swisher, 1997, 1999; Bettis et al., 2004). Freshwater lake-edge and marsh environments supported sedges, ferns, water-tolerant grasses, and trees (Smah, 1984; Tonkunaga et al., 1985), in addition to a variety of aquatic and semi-aquatic vertebrate (Hexaprotodon, various cervids, crocodiles, turtles, and sh) and invertebrate species. Wet grasslands with scattered shrubs occupied slightly higher parts of the Early Pleistocene landscape, where water tables uctuated from near the land surface to a depth of about 1 m on an annual basis (Bettis et al.,

Figure 1. (a) Plan view showing the location and regional geology of the Sangiran Dome in Central Java. The formations within the large dome map are delineated by the colors as explained in the key. Hominin nd spots are depicted with a skull, calvaria, or mandible, as appropriate. (b) Satellite image of the Bapang site and the Bpg 2001.04 nd spot.

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2009a). Still higher, better-drained parts of the landscape supported savanna vegetation, which was most likely dominated by sedges, grass, and ferns with scattered trees. Between 1.6 Ma and 1.5 Ma, large streams draining volcanic highlands to the northwest and southeast began to locally scour and ll in the lowland in the Sangiran area (Larick et al., 2001; Bettis et al., 2004, 2009a). Local variations in stream ow and channel characteristics and distance from river channels were important elements that inuenced the depth of scour, the nature of sediment that accumulated and that controlled edaphic conditions and vegetation patterns during this time. Riparian forest occupied the active channel belt where shifting channels left many sandbars and shallow abandoned channels, low-lying and frequently ooded areas supported a moist savanna with scattered trees and shrubs, and well-drained terraces and valley slopes were covered with open woodlands (Ciochon et al., 2007; Bettis et al., 2009a). It was in this setting that the hominin reported here lived at about 1.5 Ma. In addition to H. erectus, these environments supported the Trinil H.K. fauna represented by Panthera, various cervids, Sus branchygnatus, and primates (Larick et al., 2000, 2001; van den Bergh et al., 2001). Locally, the Bapang Formation is conformably overlain by uvial deposits of the Pohjajar Formation that have a higher proportion of air-fall tuffs, uvially reworked ash fall, and lahar-formed diamictons. Stratigraphy and dating of the Bpg 2001.04 locality The Bpg 2001.04 H. erectus maxilla was found in the basal Bapang Formation eroding from a carbonate-cemented, pebbly channel sand, which has traditionally been called the Grenzbank Zone, near the low-relief erosional contact between the Bapang and

Sangiran Formations (Figures 1b and 2aeb). At the nd spot, this cemented zone occupies the central portion of a shallow uvial channel locally cut into a 2040 cm-thick basal Bapang Formation matrix-supported conglomerate, dominated by rip-up clasts derived from the underlying Sangiran Formation siltstones and mudstones. The maxilla was located in the upper meter of the channel sand approximately 20 cm above the contact with the Sangiran Formation (Figure 2a; UTM Zone 49 483990E 9174670N). A modern intermittent stream has cut through overlying deposits and exposed the channel sands just north of the nd spot. The cemented channel sands grade laterally into uncemented trough crossbedded pebbly sand that is overlain by a silt-lled trough that contains lenses of reworked tuff (Figure 2a). The silts are overlain by trough crossbedded pebbly sand with lenses of epiclastic pumice. The 40Ar/39Ar date of 1.51 0.08 Ma was obtained on hornblende extracted from pumice in one of these lenses stratigraphically about 2 m above and 45 m northwest of the maxilla nd site. This date agrees well with a 40Ar/39Ar age of 1.58 0.02 Ma from the basal Bapang Formation in the same stratigraphic section (Swisher, 1997, 1999) as well as other 40Ar/39Ar ages from the H. erectus-bearing interval in Sangiran (Larick et al., 2001; Ciochon et al., 2001; Bettis et al., 2004). The sediment at the discovery site is a poorly sorted, subangular to subrounded, carbonate-cemented, volcaniclastic sandstone that contains a few granules. The sandstone is composed of a variety of intermediate igneous rock fragments (granodiorite, diorite, and dacite, but dominantly andesite), as well as welded tuff and pumice, with subordinate amounts of sedimentary rock fragments such as sandstone, limestone, quartzite, phyllite, and fragments of eroded carbonate nodules. The sand and granule matrix is cemented by sparry calcite with euhedral to subeuhedral crystal development.

Figure 2. (a) Bapang Formation stratigraphy, dating, and sedimentary cycles. The Bpg 2001.04 nd spot, at the base of the section, is depicted with a white star. (b) Detailed stratigraphic section showing the precise Bpg 2001.04 nd spot in the Grenzbank Zone, 2 m below the pumice horizon dated to 1.51 0.08 Ma.

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Similar sediment lls the maxillary sinus oor of Bpg 2001.04, tying the specimen to this localized stratigraphic horizon (see Figure 3d and comparative description below). The composition of this uvial sandstone indicates that its clastic grains were derived dominantly from volcanic sources. The fresh appearance of individual feldspar crystals indicates that the grains underwent little to no chemical weathering prior to, during, and subsequent to transport from volcanic highlands into the Solo Basin. Cementation by carbonate occurred at a later date as a precipitate from calcite-saturated groundwater preferentially moving through the coarse channel sands at the Bapang/Sangiran contact. Cementation, the primary distinguishing characteristic of the Grenzbank Zone, is a horizontally discontinuous, postdepositional phenomenon formed in a geochemical environment that postdates the affected sediment. The cementation has no relationship to the age of the affected sediment, and we have

observed similar cemented sediments in other stratigraphic positions in Pleistocene deposits elsewhere in Central Java. Thus, the Grenzbank Zone should not be considered a stratigraphic marker bed as has been done in the past (e.g., Sudijono, 1985). Approximately 15% of the 80 H. erectus specimens recovered in Sangiran have provenience in the thin zone of cemented Grenzbank Zone sediments at the base of the Bapang Formation (Larick et al., 2004). Though uvial reworking that concentrated fossils occurred throughout accumulation of the Bapang Formation, the process was enhanced during development of the uvial erosion surface that marks the contact between the Sangiran and Bapang Formations. This erosion surface, and another marking the contact between the Bapang and overlying Pohjajar Formation, represent periods of net sediment removal from the Sangiran area (Bettis et al., 2009b). During these periods, heavy clasts, including large vertebrate fossils, were concentrated and subjected to multiple

Figure 3. Bpg 2001.04 maxilla: (a) occlusal aspect; (b) buccal aspect; (c) lingual aspect; (d) superior aspect; (e) anterior aspect; (f) posterior aspect. Scale bar is 1 cm.

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reworking events that generally resulted in breakage and selective removal of less dense elements. The general absence in the basal Bapang Formation of low-density skeletal elements such as calvariae, the common occurrence of mandibular and maxillary fragments and teeth, and the overall concentration of fossils in this zone is a product of these geologic processes. Comparative description Root of the zygomatic arch The zygomatic root arises opposite the M1 and follows a gentle upward curve (Figure 3aef). In this respect, its conguration is reminiscent of that exhibited by Sangiran 17 (H. erectus), the eastern and southern African specimens KNM-WT 15000 and SK 847 (H. erectus) (but see Grine et al., [1996] for an alternate taxonomic placement for SK 847), and the D2282 and D2700 crania from Dmanisi, Georgia (H. erectus). The arch of Bpg 2001.04 differs noticeably from the tightly curved zygomatics of Zhoukoudian Skulls XIII and IX. In its placement, the arch arises at the same level as the zygomatics in Sangiran 17, Zhoukoudian Skulls XIII and IX, and Swartkrans SK 847. The KNM-WT 15000 subadult zygomatic arch arises more anteriorly, at the level of P3 P4. Although the zygomatic root of Bpg 2001.04 is incomplete, it appears to have been rather thin anteroposteriorly (c. 1618 mm). This contrasts with the robust arches of Sangiran 17 (c. 26 mm) and KNM-WT 15000 (c. 2223 mm), and is more similar to those of Skull XIII (c. 21 mm) and SK 847 (16 mm). The inferior surface of the zygomatic arch of Bpg 2001.04 appears to level off at about 14 mm above the buccal

cervical margin of the M1. In this respect, it is similar to the arches of Sangiran 17 (c. 12 mm) and Zhoukoudian Skulls XIII and IX (13.0 and 14.5 mm, respectively), and lower than in KNM-WT 15000 (c. 17 mm) and especially SK 847 (est. 21.5 mm). The maxillary sinus The maxillary sinus can be viewed in computed tomography (CT) scans by segmenting the bone from the less dense gravel matrix that covers the sinus (Figure 4aed). The anterior extent of the sinus is a vertical coronal wall superior to the posterior half of P4, possibly similar to A.L. 666-1 when viewed in prole (Kimbel et al., 1997). The sinus extends into the root of the zygomatic arch, although the lateral, posterior, and medial extent of the sinus cannot be fully determined due to fragmentation of the fossil. The sinus lls the observable mid-facial region, but does not inate the external mid-face, or create a short, sloping region between the anterior sinus and the root of the zygomatic arch, which is seen in Homo aff. Homo habilis (Kimbel et al., 1997). The chamber is perforated by the lingual roots of M1 and M2 (Figure 4c). Unlike the A.L. 666-1 maxilla, in which the sinus is partitioned into 2 chambers (Kimbel et al., 1997), the Bpg 2001.04 sinus is not partitioned. The maxillary alveolus The specimen exhibits a very slight degree of physiological alveolar resorption, particularly lingually. Palatal depth cannot be measured from the original, but appears rather shallow. In this respect, the specimen resembles Sangiran 17 more closely than either Sangiran 4 or Sangiran 1a.

Figure 4. Computed tomography (CT) virtual reconstruction of Bpg 2001.04. (a) Posterior view of the original maxillary fragment with matrix-lled sinus. The arrow indicates the M2 lingual root. (b) Scan of maxilla fragment, looking posteriorly at the sinus in-lled with matrix. The arrow points to a bump created by the lingual root of M2. (c) Posterior view of M2, the arrow points to the lingual root of M2 without the encompassing matrix. (d) View with matrix removed from the left maxillary sinus. The rim of the sinus is highlighted. The arrow again indicates the M2 lingual root. [CT scanning by Yahdi Zaim in Bandung. Slice thickness: 1.3 mm].

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Table 1 List of mesio-distal (MD) and bucco-lingual (BL) measurements (mm) for Bpg 2001.04 and for the Homo specimens used in these analyses. The Western H. erectus sample pools the Dmanisi and Africa specimens. Specimen numbers in boldface indicate complete dentitions for this study; ? refers to isolated teeth with side-indeterminate. Additionally, parenthetical numbers indicate estimates. Specimen Side P3 MD/BL Bpg 2001.04 L 8.1 11.3 7.6 7.3 P4 MD/BL 12.2 10.2 12.5 11.0 11.5 12.0 11.6 M1 MD/BL 13.5 12.5 12.6 13.4 12.0 12.5 11.6 M2 MD/BL 13.8 12.5

Sangiran H. erectus R S 7-3a, b, ca S 7-8a L R S 7-9 a S 7-10b R S 7-27c L S 7-29a R a S 7-30 R S 7-31a L a S 7-32 R S 7-35a L S 7-37d R S 7-38a L S 7-40a R a L S 7-53 S 7-58a L c Sangiran 4 AVG Sangiran 15Ae L Sangiran 15Be R Sangiran 16f L Sangiran 17g AVG h Sangiran 27 AVG Tjg 1993.05, Skull IXi R Zhoukoudian H. erectus Zdn Skull Vj L Zdn Skull XIf AVG Zdn Skull XIIIk L Zhoukoudian 104l R l Zhoukoudian 105 L Zhoukoudian 133l L l Zhoukoudian 140 L Zhoukoudian 142j ? Zhoukoudian 143l L Zhoukoudian 144l ? Zhoukoudian 145l ? Zhoukoudian 19f R l Zhoukoudian 25 L Zhoukoudian 26l ? Zhoukoudian 27l L Zhoukoudian 28l R Zhoukoudian 32l R Zhoukoudian 33l L f Zhoukoudian 39 ? f Zhoukoudian 40 L Zhoukoudian 41f L Zhoukoudian 42f R Zhoukoudian 77f L Zhoukoudian 78f R Zhoukoudian 86l ? Zhoukoudian 87l R j Zhoukoudian 88 L Zhoukoudian 94j R Zhoukoudian 95j L Western H. erectus (Dmanisi and Africa) D2700m AVG D2282n AVG l KNM-ER 1808 L l KNM-ER 3733 AVG l KNM-ER 807 R KNM-ER 808o R KNM-WT 15000l AVG OH 38p AVG SE 255f,* R c, * SK 27 L q, * SKX 268 H. habilis (Eastern Africa)* KNM-ER 1506r R KNM-ER 1805f AVG KNM-ER 1813l L OH 13e R

7.8

10.4 8.2 7.9 10.3 10.2

7.9 7.9 8.5

10.6 10.8 12.2 11.4 12.8 13.6 12.5 13.9 13.8 13.5 14.0 15.2

9.1 8.4 7.5 7.1 7.2 8.9 10.1 8.5 7.4 8.0

11.5 12.4 10.1 9.9 10.6 12.8 9.5 12.2 10.5 11.6

8.4 7.8

12.2 11.0

12.2

13.6

13.6

7.3 7.2 7.0 7.4 7.3

12.4

10.8 11.9 11.3 10.5 10.0 10.6

12.6 14.5 11.0 12.0 12.0 12.4

10.7 12.9 10.6 10.0 10.3 10.6 10.3 10.2

12.5 14.8 10.9 11.9 12.8 13.4 12.8 12.8

11.0 11.0 11.1

8.8 8.0 11.6 7.3

11.7 11.1 11.1 10.6 12.4 10.6 13.4 13.7

9.2

12.8 7.9 8.3 8.3 7.2 11.3 11.2 12.1 10.3 11.3 12.1 11.7 13.4 10.5 12.2 11.1 11.4 12.3 12.2 13.2 12.4

8.7 7.4

12.6 10.5 8.9 7.3 7.4 12.5 10.8 11.2 10.0 10.2 11.7 12.3 13.1 12.9 12.7 12.5 11.5 12.4 12.9 12.1 13.0 13.9 (14) 12.2

8.9 8.5 8.7 8.7 8.6 9.6 9.6

11.5 13.8 12.0 12.5 11.8 12.9 13.3

6.8 9.2 8.1

11.5 11.0 12.1

13.0 12.5 12.3 (13) 13.2 11.8 13.4 13.5 13.2

8.3

11.8

(14) 13.0 12.2 13.2 13.7 12.9

13.4

13.7

14.7

8.3 8.0 8.0 8.3

11.9 11.5 11.1 11.4

9.1 9.0 9.0 8.7

12.2 11.6 11.3 11.5

13.2 12.2 12.5

13.4 12.5 12.6

13.1 12.2 12.8

14.3 13.6 13.8

Y. Zaim et al. / Journal of Human Evolution 61 (2011) 363e376 OH 65s Omo L894-1f KNM-ER 42703s AVG AVG R 9.3 8.8 9.0 12.7 12.7 12.0 9.1 9.2 8.8 13.1 12.2 12.4 12.8 12.7 12.6 13.6 13.2 13.3 13.1 11.8 13.0

369

14.4 12.6 14.1

*For this study, we dene Homo habilis as an eastern African early hominin with a temporal range between 1.9 and 1.6 Ma, thus A.L. 666-1 is excluded from our sample. There are specimens from South Africa that have been described as Homo aff. H. habilis or as Homo erectus. At Swartkrans, SK 27 and SKX 268 have been suggested by some to belong to a taxon with closer afnities to H. habilis (sensu stricto) than to H. erectus (e.g., Howell, 1978; Grine et al., 2009). However, for the purpose of this study, we have followed others (e.g., Rightmire, 1990) who have included SK 27 and SKX 268 in Homo erectus. Similarly, at Sterkfontein, SE 255 derives from Member 5 West and while it might represent H. erectus, many workers have considered it to represent the same species as Stw 53 (i.e., something with closer afnities to Homo habilis). Of course, the Member 5 deposit is not a single deposit, and it does contain material that is most likely attributable to H. erectus (e.g., the Stw 80 mandible from Member 5 West [Kuman and Clarke, 2000; Moggi-Cecchi et al., 2006]). Thus, while it is not unreasonable to place SE 255 in the H. erectus sample as we have done, we wish to point out that there is a controversy over the species attribution in Sterkfontein Member 5. That is, Australopithecus sp. for some of the material (Kuman and Clarke, 2000), Homo aff. H. habilis (Tobias, 1978) for some of the material (at least that from Member 5A), and H. erectus for some of the material (at least that from Member 5B, or Member 5 West) (Kuman and Clarke, 2000). a Grine and Franzen, 1994. b Tobias and von Koenigswald, 1964. c Wolpoff, 1971. d Dean, 2007. e Blumenberg and Lloyd, 1993. f Wood, 1991. g Jacob, 1975. h Indriati and Antn, 2008. i Arif, 1998; Arif et al., 2001. j Weidenreich, 1937a. k Weidenreich, 1937b. l Walker and Leakey, 1993. m Rightmire et al., 2006 n Martnon-Torres et al., 2008. o Leakey et al., 1978. p Tobias, 1968. q Grine, 1989. r Boaz and Howell, 1977. s Spoor et al., 2007.

Dental morphology and crown size The P3 crown has an ovorectangular occlusal outline, with a slightly dominant paracone (Figure 3a). The mesial marginal ridge, which is slightly thicker than the distal marginal ridge, is incised by a narrow furrow such that the mesial end of the longitudinal furrow between the paracone and protocone is open. The mesial surface preserves a 3 mm long, oblong contact facet for the canine. Occlusal wear is slight to moderate; both cusps are blunted, and there is a small dentine exposure in the center of the paracone. Its mesio-distal (MD) diameter is 8.1 mm. The bucco-lingual (BL) diameter is 11.3 mm. The crown of P4 also presents an ovorectangular outline, though the lingual face of the protocone is skewed very slightly mesially (Figure 3a). The protocone and paracone are approximately equal in size. The mesial and distal marginal ridges are complete, but low, and the longitudinal furrow between the paracone and protocone cuts through the lingual end of the principal paracone crest, thus separating it from the protocone. Occlusal wear is slight; both cusps are blunted, but dentine is not exposed. It measures 7.6 mm MD. The BL diameter is 12.2 mm. The crown of M1 has a nearly square occlusal outline, with a more prominent mesio-buccal corner compared to the distobuccal corner (Figure 3a). The BL breadth across the trigon (13.5 mm) is slightly greater than across the talon (12.4 mm). The four principal cusps are well developed: the protocone is the largest, and the paracone, metacone, and hypocone are of approximately equal size. The distal marginal ridge is thin and incised at the base of the metacone by a very narrow ssure. The crista obliqua appears to have been complete, although constricted. The mesio-lingual and lingual aspects of the protocone preserve short, slightly oblique ssures at the occlusal margin that represent the remnants of the Carabelli trait. This feature would likely have been fairly large based on the distance between the furrows (3.7 mm). Occlusal wear is moderate. The lingual cusps have been reduced to a at platform and the buccal cusps are rounded. The paracone, metacone, and hypocone exhibit small dentine islands, and there is

moderate, concave exposure on the protocone. The MD diameter of the crown is 12.5 mm. The maximum BL diameter is 13.5 mm. The crown of M2 has a square occlusal outline, although the distobuccal corner is very slightly reduced (Figure 3a). The BL breadth of the trigon (13.7 mm) is somewhat greater than across the talon (12.3 mm). The four principal cusps are present, and the protocone is the largest, followed closely by the paracone. The hypocone is considerably smaller than the paracone, and the metacone is reduced, making it the smallest cusp. The mesial marginal ridge, while worn, appears to have been thick and is complete. The thinner distal marginal ridge is complete, and encloses a fovea posterior (talon basin) that takes the form of a narrow T-shaped ssure, the tines of which comprise a transverse ssure distal to the principal crests of the metacone and hypocone. The crista obliqua is incised by a narrow furrow. There is no evidence of the presence of the Carabelli trait. Occlusal wear is slight, with all cusps reduced and rounded, though dentine is not exposed. The distal surface preserves a slightly concave, moderately broad (c. 5 mm) contact facet for the M3 (Figure 3f). The MD diameter of the crown is 12.5 mm. The maximum BL diameter is 13.8 mm.

Materials and methods Odontometric comparisons The MD, BL, and crown area (CA MD BL) dimensions of Bpg 2001.04, and means for these measurements in several comparative samples, were used to create individual tooth prole graphs to investigate trends in size differences of P3M2 following the methods advocated by Rosas and Bermdez de Castro (1998). As such, most of the comparisons involve shape using Interdental Indices to characterize crown shape relationships (Rosas and Bermdez de Castro, 1998; Bermdez de Castro et al., 1999) and Average Dental Ratios (Bermdez de Castro et al., 1999). To this end, we calculated WF distances (F) to assess phenetic afnities following Rosas and Bermdez de Castro (1998) and Bermdez de

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Castro et al. (1999), and analyzed the WF distances by cluster analysis using the statistical software package NCSS (Hintze, 2001). Only 13 specimens of H. habilis and H. erectus preserve the same four teeth as Bpg 2001.04 (see boldface entries in Table 1). In order to increase the comparative base, site samples using the mean values for each dimension of each tooth were constructed. We included any specimen that possessed at least one of the teeth preserved in Bpg 2001.04, as long as it preserved both BL and MD dimensions. Specimens were assigned to one of four comparative samples, each representing a different Old World hominin population by site or region: Sangiran H. erectus (Early Pleistocene Southeast Asia); Zhoukoudian H. erectus (Middle Pleistocene Northeast Asia); Western H. erectus (Early Pleistocene of Africa and Georgia [Dmanisi]), and H. habilis (Plio-Pleistocene East Africa). The comparative sample groups range temporally from the Late Pliocene (1.9 Ma) to the Middle Pleistocene (0.4e0.78 Ma) (Ciochon and Bettis, 2009; Shen et al., 2009) and derive from all areas of the Old World occupied by H. erectus (Kramer, 1993). Antn (2002) and Kaifu (2006) have emphasized the need to recognize regional and temporal variation among Asian H. erectus samples. Although there is a decrease in mandibular post-canine tooth size during the entire 600 k.yr. of Sangiran H. erectus (Kaifu, 2006), our sample of maxillary dentition is derived from a 300 k.yr. portion of the total H. erectus temporal range; therefore we feel justied in including all relevant individuals for comparison in order to maximize sample size. The goals of the metric analyses performed here are descriptive and do not test for statistical signicance. This is because the individual comparative samples are too small to avoid Type-II comparison errors. Under these conditions, descriptive results that identify metric patterns between samples and specimens and are suggestive of overall trends are preferable to error-prone statistical tests.

Methodology Raw measurements for the MD, BL, and crown area (CA MD BL) dimensions in Bpg 2001.04, and means for these measurements in the comparative samples (Table 1), are used to create individual tooth prole graphs to investigate trends in size differences of P3M2. It has been argued, however, that shape is a more useful indicator than size when taxonomic afnity is concerned (Rosas and Bermdez de Castro, 1998); as such, most of the comparisons in the present study involve shape using the following measurements. Interdental indices Interdental indices (6 in total) were constructed using the CAs for the preserved teeth (e.g., P3/P4) to characterize crown shape differences or similarities (Rosas and Bermdez de Castro, 1998; Bermdez de Castro et al., 1999) of each comparative sample and Bpg 2001.04. Average dental ratios The relative differences in the proportions of Bpg 2001.04 relative to the comparative samples were investigated using average dental ratios (ADR) following Bermdez de Castro et al. (1999). This methodology allows for comparison of the relative proportions of each dimension of each tooth in Bpg 2001.04 to each dimension of each tooth in the comparative sample means. We use the following procedures. First, the raw data are scaled relative to Bpg 2001.04 using the formula:

than that of Bpg 2001.04, the formula will yield a value of <1.0. The values of the resulting formula for each dimension of each tooth (8 in all) are averaged together to form the average dental ratio (ADR). If the ADR < 1.0, this indicates that, on average, the value for each dimension of the comparative sample mean is greater than Bpg 2001.04. These ADR values can be compared in scatter-plots relative to the value from the original formula to investigate relative proportionality of each dimension of the individual teeth to Bpg 2001.04. In the bivariate scatter-plots, points above the X Y line imply that those specimens have proportionately lower values than Bpg 2001.04; those below the line have proportionately higher values than Bpg 2001.04. The greater the difference between the value for the formula and the ADR, the further from the X Y line the comparative sample will be. While the interdental index values and the ADR values are not independentdsince they are both based on the same initial starting valuesdthe precise information each conveys (i.e., specic crown shape differences among the separate paleodemes vs. more precise information regarding why such differences manifest) is useful in quantifying the crown shape relationships of Bpg 2001.04 to the other samples. WF distance (F) WF distances, following Bermdez de Castro et al. (1999), are dened as the variance (s2) of all the values for the formula: Bpg 2001:04Vi $2=Bpg 2001:04Vi Si ; thus, they represent the distance between a given comparative sample and Bpg 2001.04. WF distances were also calculated for the comparative samples relative to each other; e.g., the formula (SA 2)/(SA SB), is used to compare H. erectus and H. habilis where SA Western H. erectus and SB H. habilis for any of the individual dimensions of interest. The resulting WF distances for all pairwise comparisons between samples is used to assess the phenetic afnities following Rosas and Bermdez de Castro (1998) and Bermdez de Castro et al. (1999). Cluster analysis The WF distances are also used in cluster analyses to further assess overall phenetic similarity/dissimilarity in dental crown size and shape patterns among the comparative samples and Bpg 2001.04. All analyses were performed using the statistical software package NCSS (Hintze, 2001). Results Individual tooth prole graphs The BL measurements (Figure 5a) present three congurations. The rst is of increasing length from the P3 to M2, as exemplied in Bpg 2001.04. The second is of virtually no change in the breadth dimension from P3 to P4, as is seen in H. habilis and Sangiran H. erectus. The third is of wide P3s followed by a decrease in the P4 breadth, a conguration shared by Western H. erectus and Zhoukoudian. In all three patterns, M1 is narrower than M2. In the MD dimension (Figure 5b), all the samples show the same pattern of decrease in size from P3 to P4, with the exception of H. habilis, which possesses the opposite pattern. In terms of molar length, the samples and specimen are characterized by little to no change in length from M1 to M2. In the computed crown areas (Figure 5c), Bpg 2001.04 is characterized by a small increase in size from P3 to P4. The Sangiran sample is characterized by virtually no change in crown area between the premolars, while Zhoukoudian and Western H. erectus show a decrease in crown area. H. habilis shows a large increase in premolar crown area. All sample groups, except Western H. erectus, show an increase in molar crown area from M1 to M2. Interdental indices The interdental indices created from the computed crown areas are presented in Table 2. Bpg 2001.04 shows a premolar interdental

Bpg 2001:04Vi $2=Bpg 2001:04Vi Si

where Vi is the raw dimension of Bpg 2001.04 (e.g., P3 BL) and Si is the same dimension of the comparative sample mean (e.g., P3 BL for Western H. erectus). The resulting value of this formula is therefore a size ratio between the comparative sample and Bpg 2001.04. The formula has a value of 1.0 if the Vi for Bpg 2001.04 is equal to the value of that same variable for the comparative sample (Si). If Si is larger

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Figure 5. Individual tooth measurement (raw data) proles for Bpg 2001.04 and mean values for H. erectus (early African, Sangiran, and Zhoukoudian) and H. habilis. From top left to bottom right, they include (a) bucco-lingual length (BL), (b) mesio-distal length (MD), and (c) computed crown area.

index of slightly less than 1.0, revealing that Bpg 2001.04 has a slight increase in overall crown area from P3 to P4. This relationship is not shared by any of the other comparative samples, save for H. habilis, which shows an even larger increase in crown area. The three H. erectus samples are characterized by slight decreases in P4 crown area, with Western and Zhoukoudian H. erectus showing a larger decrease than Sangiran. The molar interdental index for Bpg 2001.04 shows a slight increase in crown area from M1 to M2; this condition is shared with the other samples, and is seen in the most extreme with Western H. erectus and H. habilis. In the P3/M1 index, Bpg 2001.04 displays a third premolar crown area which is roughly half the area of its M1. This same relationship can be seen with Sangiran H. erectus. Western H. erectus and H. habilis share similar values with each other for this index, with a P3 crown area roughly two-thirds the size of their M1 crown area.

Table 2 Interdental indices created from computed crown areas of Bpg 2001.04 and the comparative samples. Specimen/Sample Bpg 2001.04 Sangiran H. erectus Zhoukoudian H. erectus Western H. erectus H. habilis P3/P4 0.99 1.04 1.09 1.23 0.94 M1/M2 0.98 0.94 0.98 0.99 0.94 P3/M1 0.54 0.58 0.72 0.66 0.61 P3/M2 0.53 0.55 0.70 0.66 0.58 P4/M1 0.55 0.56 0.66 0.53 0.65 P4/M2 0.54 0.53 0.64 0.53 0.61

Zhoukoudian is the most disparate, displaying a crown area for P3 that is roughly three-quarters the size of its M1 crown area. Specimen Bpg 2001.04 has a P3/M2 index of 0.53. The Sangiran sample has a nearly identical ratio between these two teeth, and H. habilis has a similar value (0.58). Both the Western H. erectus and Zhoukoudian samples have larger ratios, with Zhoukoudian having the largest P3 crown area relative to its M2 crown area of any sample. The P4/M1 of Bpg 2001.04 equals its P3/M1 index. This result is not surprising given that the premolar crown area index was nearly 1.0. It shares the same value for this index with the Sangiran H. erectus sample, and the Western H. erectus sample. H. habilis and the Zhoukoudian sample have similar index values, both of which are larger than the Bpg 2001.04 index value. The ratios for P4/M2 show that Bpg 2001.04, the Sangiran sample, and Western H. erectus sample are characterized by similar relationships, that is, a fourth premolar with a crown area roughly half the size of the crown area of the second molar. H. habilis and the Zhoukoudian sample have a larger index for these two teeth, with a fourth premolar roughly two-thirds the size of the second molar. Average dental ratios P3 Bucco-lingually (Figure 6a), the distribution of the regional samples relative to Bpg 2001.04 shows both the Western H. erectus and Zhoukoudian samples falling furthest from the line

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in the lower quadrant, indicating that they are relatively larger in this dimension than Bpg 2001.04. While H. habilis is close to the X Y line, Sangiran H. erectus falls directly on the line, indicating that Bpg 2001.04 and the Sangiran sample possess similar BL proportions. In the MD dimension (Figure 6b), all samples fall below the X Y line, indicating that all three regional samples are proportionately larger in this dimension than Bpg 2001.04. The sample closest to the X Y line, and therefore most similar to Bpg 2001.04, is H. habilis, followed closely by the Sangiran H. erectus sample. Zhoukoudian H. erectus and Western H. erectus are further from the line, possessing relatively larger MD dimensions. P4 The BL dimension of Bpg 2001.04 (Figure 6c) is relatively larger than the comparative samples, all of which fall above the X Y line. While the comparative samples do fall close to the line, the Zhoukoudian sample is closest, followed by H. habilis and Western H. erectus. Sangiran H. erectus is furthest from the line, indicating that in this dimension, Bpg 2001.04 least resembles its local analogs. Bpg 2001.04s MD dimension (Figure 6d) is relatively smaller than all the comparative samples. However, Western H. erectus and Sangiran H. erectus fall closest to the X Y line, indicating that these two regional samples are generally similar to Bpg 2001.04 in this dimension. The H. habilis sample, on the other hand, is located far from the line, revealing that in the MD dimension, H. habilis is considerably larger than Bpg 2001.04. Zhoukoudian H. erectus falls below the line, as well, and is relatively larger in this dimension than Bpg 2001.04. M1 Bpg 2001.04 is relatively larger than the comparative samples in the BL dimension (Figure 7a), all of which fall above the X Y line. Western H. erectus and H. habilis are furthest above the line, indicating that these specimens are relatively smaller than Bpg

2001.04, with H. habilis being furthest from the line. Sangiran and Zhoukoudian H. erectus are closer to the line than the Western samples, with Sangiran falling almost directly on the X Y line. The results show an Asian/African dichotomy, with the Asian specimens having larger BL dimensions. Like the BL relationship, the MD dimension (Figure 7b) of M1 shows that Bpg 2001.04 is relatively larger than most of the comparative samples. Sangiran H. erectus, Western H. erectus and H. habilis all cluster tightly around the X Y line, with Western H. erectus falling slightly under the X Y line, and therefore being slightly larger in this dimension to Bpg 2001.04. Zhoukoudian is considerably smaller in this M1 dimension than Bpg 2001.04 or any of the other samples, falling quite far above the line in the upper quadrant. M2 The results for BL analysis (Figure 7c) show that Bpg 2001.04 possesses a relatively larger dimension, with the exception of Sangiran H. erectus. All of the samples show tight clustering around the line. Sangiran H. erectus is on the X Y line, indicating that this population is very similar in its BL dimension to Bpg 2001.04. The next closest sample to the X Y line is H. habilis, followed by Zhoukoudian H. erectus, and nally, Western H. erectus, all of which are relatively smaller than Bpg 2001.04 in the BL dimension. The analysis of the MD dimension of M2 (Figure 7d) shows a nearly identical pattern to that of the MD dimension of M1. Again, H. habilis, Western H. erectus, and the Sangiran H. erectus samples cluster close to the line, with the placement of the H. habilis and Western H. erectus indicating that they are slightly smaller than Bpg 2001.04. Sangiran is nearly identical to Bpg 2001.04, being located just below the X Y line. Zhoukoudian falls far above the line, and its M2 is much smaller in the MD dimension than Bpg 2001.04.

Figure 6. Bivariate scatter-plots of the average dental ratios (ADR) versus the values of equation 1 of the bucco-lingual (BL) and mesio-distal (MD) dimensions of P3eP4. P3 is presented on top from left (a) bucco-lingual length, to right (b) mesio-distal length. P4 is presented on the bottom from left (c) bucco-lingual length, to right (d) mesio-distal length.

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Figure 7. Bivariate scatter-plots of the average dental ratios versus the values of equation 1 of the bucco-lingual (BL) and mesio-distal (MD) dimensions of M1eM2. M1 is presented on top from left (a) bucco-lingual length, to right (b) mesio-distal length. M2 is presented on the bottom from left (c) bucco-lingual length, to right (d) mesio-distal length.

WF distances Overall relationships between samples based on the WF distance statistic are shown in Table 3. The smallest WF distance between Bpg 2001.04 and any of the other samples is with Sangiran H. erectus, which is a reection of the similarity between these groups on nearly all of the tooth dimensions. The next closest to Bpg 2001.04 is Western H. erectus. H. habilis is the next most similar to Bpg 2001.04. Finally, Zhoukoudian H. erectus, more than 800 k. yr. younger than Bpg 2001.04, is the most dissimilar, and this is indicated by virtually all of the individual average dental ratios. A cluster analysis based on the WF values found in Table 3, via the unweighted pair-group method using the arithmetic averages method (UPGMA), is shown in Figure 8. Two main divisions present themselves; an older African-Southeast Asian cluster, and a younger, mainland China group, consisting only of the Zhoukoudian sample. Within the older African-Southeast Asian division, Bpg 2001.04 and the Sangiran H. erectus sample cluster together as most similar, with the Western H. erectus sample being the next most similar to the southeast Asia cluster, and nally H. habilis being the least similar within this division of the dendrogram.

Some variation from this clustering result occurred using various alternative clustering algorithms (e.g., Nearest Neighbor linkage, Wards, etc.) when the WF values were calculated using all eight linear tooth dimensions. However, small sample size effects for P4 BL dimension (see discussion) is likely affecting this result. When the P4 BL dimension was excluded from the calculation of WR values, the alternative clustering algorithms produced identical or nearly identical patterns to that evident in Figure 8. Discussion In East Asia, two fossiliferous sites account for the vast majority of H. erectus fossils: south equatorial Sangiran (07 27.4600 S, 110 50.3600 E) and north temperate Zhoukoudian (39 440 0" N, 115 550 0" E). More than 5000 km separate the localities. The

Table 3 Values of the WF distance.

F
Bpg 2001.04 Sangiran H. erectus Zhoukoudian H.erectus Western H. erectus

Sangiran Zhoukoudian Western H. erectus H. habilis 0.0003245 0.0013852 0.0010153 0.0007482 0.0005934 0.00010783 0.0010206 0.0004798 0.0008221 0.0010314 Figure 8. UPGMA linkage dendrogram on Euclidean distances of the WF distances.

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hominin arrival in Sangiran commenced before 1.6 Ma and lasted at least 700 k.yr. The occupation at Zhoukoudian began at about 0.78 Ma and lasted approximately 400 k.yr. (Shen et al., 2009). The basal occupations at Sangiran precede those of Zhoukoudian by as much as 800 k.yr. Historically, all H. erectus fossils from Sangiran and Zhoukoudian have been lumped together and considered the result of a singular African exodus. Under this model, Bpg 2001.04 and the other Sangiran maxillae should be most similar to Zhoukoudian H. erectus and display lower phenetic resemblance to the Western fossils. Our analysis, however, supports the research of Kaifu et al. (2005a, b), which shows that the Sangiran specimens are morphologically more similar to Western H. erectus populations than they are to the Zhoukoudian H. erectus sample, due to the absolutely and relatively smaller M1 and M2 dimensions of the Zhoukoudian sample. Given that later populations of Sangiran H. erectus have signicantly smaller tooth crowns (Kaifu, 2006), similar to those seen in the Zhoukoudian sample, it is possible that Zhoukoudian was colonized by later hominins from Sangiran, or that Java experienced a second colonization from the same population as did Zhoukoudian. Our results cannot answer that question. They do support the hypothesis, based on the differences in tooth dimensions (particularly the dissimilarity in the preserved molars of Sangiran and Zhoukoudian H. erectus), that Zhoukoudian was not part of the initial wave of hominin dispersal that entered Java approximately 1.6 Ma. In overall morphology of the zygomatic arch root, Bpg 2001.04 and S17 share numerous features with contemporary (Early Pleistocene) Western H. erectus (e.g., D2282 and D2700, SK 847, KNMWT 15000) and the later (Middle Pleistocene) Zhoukoudian sample (e.g., Skulls IX and XIII). However, while the Sangiran sample shares aspects of the zygomatic arch root with the Western H. erectus specimens to the exclusion of the Zhoukoudian sample, the reverse is not true. The similarity between Bpg 2001.04 and other Sangiran H. erectus maxillary fossils is especially strong in the dentition. Bpg 2001.04 and the Sangiran H. erectus fossils cluster together in ADR results. In only one dental dimension in the ADR results (P4 BL diameter) does Bpg 2001.04 cluster more with Zhoukoudian than the Sangiran sample (Figures 6 and 7). Similarities between Bpg 2001.04 and the Sangiran sample can also be seen in the interdental indices (Table 2). While all H. erectus samples possess similar interdental indices in the P3/P4 and M1/M2 crown area ratios, in the premolar/molar indices, the Bpg 2001.04 values are most similar to those of other Sangiran fossils, wherein the premolars are roughly half the size of the molars. The similarity between Bpg 2001.04 and the Sangiran sample can be seen in the WF distance values, where these two samples are the most similar (Table 3). Bpg 2001.04 is next most similar to the Western H. erectus sample, then the H. habilis sample, and nally the Zhoukoudian sample is the most dissimilar to Bpg 2001.04 for this value. The relative similarities between Bpg 2001.04 and Sangiran H. erectus with the Western H. erectus sample is likely due to their close temporal proximity, and the Western H. erectus sample serving as the ancestral stock for the population of Java by H. erectus. As can be seen in Table 2, Zhoukoudian H. erectus has the largest WF distance value from the Sangiran sample. The interdental indices of P3 to M1 and M2 also show this separation between Zhoukoudian H. erectus and Sangiran, with the former having a P3 crown area roughly seventy-ve percent the size of its molar crown areas. This is, in large part, accounted for by the absolutely shorter molars in Zhoukoudian compared to the other samples. This result and others reecting the dissimilarity of the Zhoukoudian and Sangiran H. erectus samples can be understood in a chronological framework.

The Sangiran sample is chronologically much closer to the Western H. erectus sample than it is to Zhoukoudian, for which the most current age analysis suggests a range of 400e780 ka (Shen et al., 2009; Ciochon and Bettis, 2009). With a radiometric age of 1.5 Ma, Bpg 2001.04 is chronologically closer to some of the younger H. habilis specimens included in this study than to the Zhoukoudian fossils. It is therefore likely that the similarities between the Sangiran hominins and both Western H. erectus and H. habilis samples seen in the WF distances (Table 3), the WF-based dendrogram (Figure 8), and the ADR scatter-plots (Figures 6 and 7) reect ancestral retentions. The clustering of Western H. erectus and the Sangiran H. erectus sample (including Bpg 2001.04) with H. habilis (and not with the Zhoukoudian H. erectus sample) is more likely due to the primitive (basal) morphology of the rst hominin to disperse to Southeast Asia. After all, H. habilis-like cranial and dental features are found in the Dmanisi H. erectus population (Rightmire et al., 2006; Macaluso, 2006; Martinn-Torres et al., 2008; Margvelashvili, 2008; Rightmire and Lordkipanidze, 2009). Most authorities now consider H. habilis and H. erectus as sister group species (Lieberman et al., 1996; Spoor et al., 2007). Some even consider these taxa to represent a single chronospecies (Howell, 1982; Tobias, 1989, 1991). If that is the case, then the basal Western H. erectus population that rst dispersed to Southeast Asia may have retained some H. habilislike features in its morphology. Rightmire and Lordkipanidze (2009: 47) reached a similar conclusion in that . the Dmanisi hominins individuals had a habilis-like ancestor. Indeed, Homo oresiensis, thought by many to be a descendant of the founding H. erectus deme in Southeast Asia, appears to retain a H. habilis-like wrist and foot bone morphology (Tocheri et al., 2007; Jungers et al., 2009). The west-east links and south-north contrasts evident in the morphometric data considered here may have implications for dispersal patterns in H. erectus. One contributing factor to the south-north contrasts may have been an ecological barrier to latitudinal displacement in East Asia. There are two lines of evidence in support of this scenario of dual dispersal. First, the regions numerous hominin-like fossil teeth may, in reality, represent a small, as yet unidentied hominoid member of the fauna (Ciochon, 2009). Second, all undisputed mainland H. erectus remains lie north of the Stegodon-Ailuropoda zone: Zhoukoudian (Hebei province), Gongwangling (Shaanxi province), Hexian (Anhui province), and Nanjing (Jiangsu province) (Ciochon, 2010). If H. erectus could not penetrate the Stegodon-Ailuropoda faunal complex, the equatorial and north temperate populations may have had two separate geographic origins and little genetic connection (Ciochon, 2009, 2010). This preliminary hypothesis envisions dispersals from two Western H. erectus populations. One held an early H. erectus/H. habilis-like premolar-molar pattern and dispersed early along a southern route to equatorial Southeast Asia: the result we know as Sangiran (Java) H. erectus. Another population held the more derived premolar-molar pattern and dispersed later along a northerly route toward Northeast Asia. These we know as Zhoukoudian H. erectus. Finally, we note the implications of the Late Pleistocene nuclear genome extracted from a nger bone of an archaic hominin found in Denisova Cave in southern Siberia (Krause et al., 2010; Reich et al., 2010). While the signicance of this discovery is not yet fully digested, the Denisovan-Melanesian link reported by Reich et al. (2010) establishes that, by the Late Pleistocene, there were complex population dynamics between mainland and island Southeast Asia. If one applies the implications of this later dynamic to the earlier Pleistocene, we can no longer regard H. erectus as an undifferentiated paleodeme.

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Conclusion Resurgence in Eurasian paleoanthropology has broadened our knowledge of H. erectus beyond Africa. This species, whose continent of origin remains unknown, quickly came to occupy a diverse set of open-land resources across southern Eurasia. The site of Sangiran represents the Early Pleistocene emplacement of H. erectus in equatorial Southeast Asia. The Bpg 2001.04 partial maxilla is a signicant addition to the Sangiran collection, providing a sample of ve specimens that preserve this part of the face and dentition. Our analysis of the Sangiran maxillary dentition suggests that an east-dispersing H. erectus paleodeme may have carried a H. habilis/early Western H. erectus-like premolar-molar pattern along a southern route to the equatorial zone, while a separate H. erectus paleodeme may have carried the more derived premolar-molar pattern along a northerly route to the temperate zone of China. In any event, the dental patterns revealed here suggest distinct and separate demic origins for the only two true (and highly disparate) H. erectus population samples in East Asia. As additional fossil and genetic evidence accumulates for Early and Middle Pleistocene East Asia, the H. erectus paleodeme may split further into a number of regionally distinct, but still geographically uid populations. Acknowledgments The Institute of Technology Bandung (ITB) and the University of Iowa (UI) collaborated in this research, with assistance from the Indonesian Geological Research and Development Centre (GRDC) in Bandung. This research was carried out under the following eld research permits from the Indonesian Institute of Sciences and RISTEK: 7450/V3/KS/1998, 3174/V3/KS/1999, 4301/1.3/KS/2001, 4212/SU/KU/2003, 03799/SU/KS/2006, 1718/FRP/SM/VII/08, and 04/TKPIPA/FRP/SM/IV/2010. Providing eld assistance were Johan Arif (ITB), Suminto, Sutikno Bronto, the late Sudijono (GRDC), and Sujatmiko (National Archaeological Research Centre, Jakarta). At UI, James W. Rogers rened the digital graphics while Anna Waterman assisted with editing and referencing. Fieldwork funds were provided by the L.S.B. Leakey Foundation and the following UI sources: Center for Global and Regional Environmental Research, Central Investment Fund for Research Enhancement, Ofce of the Vice-President for Research, the Ofce of the Dean of the College of Liberal Arts and Sciences, and the Human Evolution Research Fund at the University of Iowa Foundation. References
Antn, S.C., 2002. Evolutionary signicance of cranial variation in Asian Homo erectus. Am. J. Phys. Anthropol. 118, 301e323. Arif, J., 1998. Morphological study of Homo erectus skull (skull IX) from Sangiran, Central Jawa, Indonesia. Ph.D. Dissertation, Kyoto University. Arif, J., Baba, H., Suparka, M.E., Zaim, Y., Setoguchi, T., 2001. Preliminary study of Homo erectus skull IX (Tjg-1993.05) from Sangiran, central Java, Indonesia. Bull. Natl. Sci. Mus. (Japan) D 27, 1e27. Bermdez de Castro, J.M., Rosas, A., Nicolas, M.E., 1999. Dental remains from AtapuercaTD6 (Gran Dolina site, Burgos, Spain). J. Hum. Evol. 37, 523e566. Bettis III, E.A., Zaim, Y., Larick, R.R., Ciochon, R.L., Suminto, Rizal, Y., Reagan, M., Heizler, M., 2004. Landscape development preceding Homo erectus immigration into central Java, Indonesia: the Sangiran formation lower lahar. Palaeogeogr. Palaeoclimatol. Palaeoecol. 206, 115e131. Bettis III, E.A., Milius, A.K., Carpenter, S.J., Larick, R., Zaim, Y., Rizal, Y., Ciochon, R.L., Tassier-Surine, S.A., Murray, D., Suminto, Bronto, S., 2009a. Way out of Africa: early Pleistocene paleoenvironments inhabited by Homo erectus in Sangiran, Java. J. Hum. Evol. 56, 11e24. Bettis III, E.A., Zaim, Y., Rizal, Y., 2009b. Plio-Pleistocene climatic and volcanic controls on high to moderate accommodation space systems in the Solo Basin, Central Java, Indonesia. AAPG Hedberg Research Conference on Variations in Fluvial-Deltaic and Coastal Reservoirs Deposited in Tropical Environments. Jakarta, Indonesia.

Blumenberg, B., Lloyd, A.T., 1993. Australopithecus and the origin of the genus Homo: aspects of biometry and systematics with accompanying catalog of tooth metric data. BioSystems 16, 127e167. Boaz, N.T., Howell, F.C., 1977. A gracile hominid cranium from upper member G of the Shungura formation. Ethiopia. Am. J. Phys. Anthropol. 46, 93e108. Ciochon, R.L., 2009. The mystery ape of Pleistocene Asia. Nature 458, 910e911. Ciochon, R.L., 2010. Divorcing hominins from the Stegodon-Ailuropoda fauna: new views on the antiquity of hominins in Asia. In: Fleagle, J.G., Shea, J.J., Grine, F.E., Leakey, R.E.F. (Eds.), Out of Africa I: The First Hominin Colonization of Eurasia. Springer, New York, pp. 111e126. Ciochon, R.L., Bettis III, E.A., 2009. Palaeoanthropology: Asian Homo erectus converges in time. Nature 448, 153e154. Ciochon, R.L., Bettis III, E.A., Carpenter, S.J., Zaim, Y., Marsh, H.E., 2007. Paleoecological setting for the arrival and early evolution of Homo erectus in the Solo basin, Java. Am. J. Phys. Anthropol., 87. Suppl. 44. Ciochon, R.L., Bettis III, A.E., Larick, R., Zaim, Y., Suminto, Rizal, Y., Reagan, M., Heizler, M., 2003. Homo erectus landscapes: paleosols in the Bapang and upper Sangiran formations, Solo basin, central Java. Am. J. Phys. Anthropol., 77. Suppl. 36. Ciochon, R.L., Larick, R.R., Zaim, Y., Sudijono, Heizler, M., 2001. Early Pleistocene dates and sedimentary cycles for new bapang formation hominins, central Java, Indonesia. Am. J. Phys. Anthropol., 50. Suppl. 32. Ciochon, R.L., Zaim, Y., Grine, F.E., Rizal, Y., Larick, R.R., Bettis III, E.A., Franciscus, R.G., Polanski, J.M., 2005. A new Homo erectus maxilla from the Bapang basal unit, Sangiran dome, central Java. Am. J. Phys. Anthropol., 86. Suppl. 40. Dean, M.C., 2007. Dental development and life history in primates and a comparison of cuspal enamel growth trajectories in a specimen of Homo erectus from Java (Sangiran S7e37), a Neanderthal (Tabun C1), and an early Homo sapiens specimen (Skhul II), from Israel. In: Faerman, M., Horwitz, L.K., Kahana, T., Zilberman, U. (Eds.), Faces from the Past: Diachronic Patterns in the Biology of Human Populations from the Eastern Mediterranean. Oxford, pp. 21e27. BAR International Series. Dizon, E.Z., Pawlik, A.F., 2010. The lower paleolithic record in the Philippines. Quatern. Int. 223e224, 444e450. de Vos, J., Sondaar, P.Y., van den Bergh, G.D., Aziz, F., 1994. The Homo bearing deposits of Java and its ecological context. In: Franzen, J.L. (Ed.), 100 Years of Pithecanthropus: The Homo erectus Problem, vol. 171. Courier ForschungsInstitut Senckenberg, pp. 129e140. Grine, F.E., 1989. New hominid fossils from the Swartkrans formation (1979e1986 Excavations): craniodental specimens. Am. J. Phys. Anthropol. 79, 409e449. Grine, F.E., Franzen, J.L., 1994. Fossil hominid teeth from the Sangiran dome (Java, Indonesia). In: Franzen, J.L. (Ed.), 100 Years of Pithecanthropus: The Homo erectus Problem, 171. Courier Forschungs-Institut Senckenberg, pp. 75e103. Grine, F.E., Jungers, W.L., Schultz, J., 1996. Phenetic afnities among early Homo crania from East and South Africa. J. Hum. Evol. 30, 189e225. Grine, F.E., Smith, H.F., Heesy, C.P., Smith, E.J., 2009. Phenetic afnities of PlioPleistocene Homo fossils from South Africa: molar cusp proportions. In: Grine, F.E., Fleagle, J.G., Leakey, R.E. (Eds.), The First Humans: Origin and Early Evolution of the Genus Homo. Springer, Dordrecht, pp. 49e62. Hintze, J., 2001. Number Cruncher Statistical Systems. NCSS and PASS, Kaysville, Utah. Howell, F.C., 1978. Hominidae. In: Maglio, V.J., Cooke, H.B.S. (Eds.), Evolution of African Mammals. Harvard University Press, Cambridge, pp. 154e248. Howell, F.C., 1982. Origins and evolution of African Hominidae. In: Clark, J.D. (Ed.), The Cambridge History of Africa. From the Earliest Times to c. 500 BC, vol. 1. Cambridge University Press, Cambridge, pp. 70e156. Indriati, E., Antn, S.C., 2008. Earliest Indonesian facial and dental remains from Sangiran, Java: a description of Sangiran 27. Anthropol. Sci. 116, 219e229. Jacob, T., 1975. Morphology and paleoecology of early man in Java. In: Tuttle, R.H. (Ed.), Paleoanthropology, Morphology and Paleoecology. Mouton, The Hague, pp. 311e326. Jungers, W.L., Harcourt-Smith, W.E.H., Wunderlich, R.E., Tocheri, M.W., Larson, S.G., Sutikna, T., Awe Due, Rhokus, Morwood, M.J., 2009. The foot of Homo oresiensis. Nature 459, 81e84. Kaifu, Y., Aziz, F., Baba, H., 2005a. Hominid mandibular remains from Sangiran: 1952e1986 collection. Am. J. Phys. Anthropol. 128, 497e519. Kaifu, Y., Baba, H., Aziz, F., Indriati, E., Schrenk, F., Jacob, T., 2005b. Taxonomic afnities and evolutionary history of the early Pleistocene hominids of Java: dentognathic evidence. Am. J. Phys. Anthropol. 128, 709e726. Kaifu, Y., 2006. Advanced dental reduction in Javanese Homo erectus. Anthropol. Sci. 114, 35e43. Kimbel, W.H., Johanson, D.C., Rak, Y., 1997. Systematic assessment of a maxilla of Homo from Hadar, Ethiopia. Am. J. Phys. Anthropol. 103, 235e262. Kramer, A., 1993. Human taxonomic diversity in the Pleistocene: does Homo erectus represent multiple hominid species? Am. J. Phys. Anthropol. 91, 161e171. Krause, J., Fu, Q., Good, J.M., Viola, B., Shunkov, M.V., Derevianko, A.P., Pbo, S., 2010. The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 464, 894e897. Kuman, K., Clarke, R.J., 2000. Stratigraphy, artefact industries and hominid associations for Sterkfontein, Member 5. J. Hum. Evol. 38, 827e847. Larick, R.R., Ciochon, R.L., The Early Paleolithic of southeast Asia. In: Renfrew, C., Bahn, P. (Eds.), The Cambridge World Prehistory. Cambridge University Press, Cambridge, in press. Larick, R.R., Ciochon, R.L., Zaim, Y., 2004. Homo erectus and the emergence of Sunda in the Tethys Realm. Athena Rev. 4, 32e39.

376

Y. Zaim et al. / Journal of Human Evolution 61 (2011) 363e376 Spoor, F., Leakey, M.G., Gathogo, P.N., Brown, F.H., Antn, S.C., McDougall, I., Kiarie, C., Manthi, F.K., Leakey, L.N., 2007. Implications of new early Homo fossils from Ileret, east of Lake Turkana, Kenya. Nature 448, 688e691. Sudijono, 1985. The Grenzbank, a key marker bed. In: Watanabe, N., Kadar, D. (Eds.), Quaternary Geology of the Hominid Fossil Bearing Formations in Java: Report of the IndonesiaJapan Joint Research Project, CTA41, 19761979. Geological Research and Development Centre, Bandung, Indonesia, pp. 135e138. Special Publication no. 4. Swisher III, C.C., 1997. A revised geochronology for the Plio-Pleistocene hominidbearing strata of Sangiran Java, Indonesia. J. Hum. Evol. 32, A23. Swisher III, C.C., 1999. The antiquity of Homo erectus in Java: 40Ar/39Ar dating and paleomagnetic study of the Sangiran and Kendungbrubus areas. Abstracts of the International Symposium on Paleoanthropology, in Commemoration of the 70th Anniversary of the Discovery of the First Skull of Peking Man at Zhoukoudian, October 1999, Beijing, China, pp. 78. Tocheri, M.W., Orr, C.M., Larson, S.G., Sutikna, T., 2007. The primitive wrist of Homo oresiensis and its implications for hominin evolution. Science 317, 1743e1745. Tobias, P.V., von Koenigswald, G.H.R., 1964. A comparison between the Olduvai hominines and those of Java and some implications for hominid phylogeny. Nature 204, 515e518. Tobias, P.V., 1968. Olduvai Gorge. In: The Cranium and Maxillary Dentition of Australopithecus ("Zinjanthropus") boisei, vol. 2. Cambridge University Press, Cambridge. Tobias, P.V., 1978. The earliest transvaal members of the genus Homo with another look at some problems of hominid taxonomy and systematics. Z. Morph. Anthropol. 69, 225e265. Tobias, P.V., 1989. The status of Homo habilis in 1987 and some outstanding problems. In: Giacobini, G. (Ed.), Hominidae. Jaca Books, Milan, pp. 141e149. Tobias, P.V., 1991. Olduvai Gorge. In: The Skulls and Endocasts of Homo habilis, vol. 4. Cambridge University Press, Cambridge. Tonkunaga, S., Oshima, H., Polhaupessy, A.A., Ito, Y., 1985. A palynological study of the Pucangan and Kabuh formations in the Sangiran area. In: Watanabe, N., Kadar, D. (Eds.), Quaternary Geology of the Hominid Fossil Bearing Formations in Java: Report of the Indonesia-Japan Joint Research Project, CTA41, 19761979. Geological Research and Development Centre, Bandung, Indonesia, pp. 199e217. Special Publication no. 4. van den Bergh, G., De Vos, J., Sondaar, P.Y., 2001. The late quaternary palaeogeography of mammal evolution in the Indonesian Archipelago. Palaeogeogr. Palaeoclimatol. Palaeoecol. 171, 385e408. Walker, A., Leakey, R. (Eds.), 1993. The Nariokotome Homo erectus Skeleton. Harvard University Press, Cambridge. Watanabe, N., Kadar, D. (Eds.), 1985. Quaternary Geology of the Hominid Fossil Bearing Formations in Java: Report of the Indonesia-Japan Joint Research Project, CTA41, 19761979. Geological Research and Development Centre, Bandung, Indonesia Special Publication no. 4. Weidenreich, F., 1937a. The Dentition of Sinanthropus pekinensis. A Comparative Odontography of the hominids. Palaeont. Sinica New Ser. D 1, 1-181(text), 1e121 (atlas). Weidenreich, F., 1937b. Reconstruction of the entire skull of an adult female individual of Sinanthropus pekinensis. Nature 140, 1010e1011. Wolpoff, M.H., 1971. Metric Trends in Hominid Dental Evolution. The Press of Case Western Reserve University, Cleveland. Wood, B., 1991. Koobi Fora Research Project. In: Hominid Cranial Remains, vol. 4. Clarendon Press, Oxford.

Larick, R.R., Ciochon, R.L., Zaim, Y., Sudijono, Suminto, Rizal, Y., Aziz, F., 2000. Lithostratigraphic context for the Kln-1993.05-SJN, a fossil colobine maxilla from Jokotinkir, Sangiran Dome. Int. J. Primatol 21, 731e759. Larick, R.R., Ciochon, R.L., Zaim, Y., Suminto, Rizal, Y., Aziz, F., Reagan, M., Heizler, M., 2001. Early Pleistocene 40Ar/39Ar ages for Bapang Formation hominins, central Jawa, Indonesia. Proc. Natl. Acad. Sci. 98, 4866e4871. Leakey, R.E., Leakey, M.G., Behrensmeyer, A.K., 1978. The hominid catalogue. In: Leakey, M.G., Leakey, R.E. (Eds.), The Fossil Hominids and an Introduction to Their Context, 1968e1974, Koobi Fora Research Project, vol. 1. Clarendon Press, Oxford, pp. 174e175. Lepre, C.L., Kent, D.V., 2010. New magnetostratigraphy for the Olduvai Subchron in the Koobi Fora formation, northwest Kenya, with implications for early Homo. Earth Planet. Sci. Lett. 290, 362e374. Lieberman, D.E., Wood, B.A., Pilbeam, D.R., 1996. Homoplasy and early Homo: an analysis of the evolutionary relationships of Homo habilis sensu stricto and Homo rudolfensis. J. Hum. Evol. 30, 97e120. Macaluso Jr., P.J., 2006. Descriptions and comparative studies of the hominin dental remains from Dmanisi, Georgia: 1991e2002 collections. Ph.D. Dissertation, State University of New York at Binghamton. Margvelashvili, A., 2008. The morphological description of the dental remains from the Early paleolithic site of Dmanisi (Georgia). Annali dellUniversit degli Studi di Ferrara Museologia Scientica e Naturalistica 2008, 117e122. Volume Speciale. Martinn-Torres, M., Bermdez de Castro, J.M., Gmez-Robles, A., Margvelashvili, A., Prado, L., Lordkipanidze, D., Vekua, A., 2008. Dental remains from Dmanisi (Republic of Georgia): morphological analysis and comparative study. J. Hum. Evol. 55, 249e273. Moggi-Cecchi, J., Grine, F.E., Tobias, P.V., 2006. Early hominid dental remains from Members 4 and 5 of the Sterkfontein formation (1966e1966 excavations): catalogue, individual associations, morphological descriptions and initial metrical analysis. J. Hum. Evol. 50, 239e328. Reich, D., Green, R.E., Kircher, M., Krause, J., Patterson, N., Durand, E.Y., Viola, B., Briggs, A.W., Stenzel, U., Johnson, P.L.F., Maricic, T., Good, J.M., MarquesBonet, T., Alkan, C., Fu, Q., MallickLi, S.H., Meyer, M., Eichler, E.E., Stoneking, M., Richards, M., Talamo, S., Shunkov, M.V., Derevianko, A.P., Hublin, J.-J., Kelso, J., Slatkin, M., Pbo, S., 2010. Genetic history of an archaic hominin group from Denisova cave in Siberia. Nature 468, 1053e1060. Rightmire, G.P., 1990. The Evolution of Homo erectus. Cambridge University Press, Cambridge. Rightmire, G.P., Lordkipanidze, D., 2009. Comparisons of early Pleistocene skulls from east Africa and the Georgian Caucasus: evidence bearing on the origin and systematics of genus Homo. In: Grine, F.E., Fleagle, J.G., Leakey, R.E. (Eds.), The First Humans e Origin and Early Evolution of the Genus Homo. Springer, Dordrecht, pp. 39e48. Rightmire, G.P., Lordkipanidze, D., Vekua, A., 2006. Anatomical descriptions, comparative studies and evolutionary signicance of the hominin skulls from Dmanisi, Republic of Georgia. J. Hum. Evol. 50, 115e141. Rosas, A., Bermdez de Castro, J.M., 1998. On the taxonomic afnities of the Dmanisi mandible (Georgia). Am. J. Phys. Anthropol. 107, 145e162. Smah, A.-M., 1984. Palynology and Javanese Pithecanthropus paleoenvironment. In: Andrews, P., Franzen, J.L. (Eds.), The Early Evolution of Man with Special Emphasis on Southeast Asia and Africa, vol. 69. Courier Forschungs-Institut Senckenberg, pp. 237e243. Shen, G., Gao, X., Gao, B., Granger, D.E., 2009. Age of Zhoukoudian Homo erectus determined with 26Al/10Be burial dating. Nature 458, 198e200.