The human cranial remains from Gran Dolina Lower Pleistocene site (Sierra de Atapuerca, Spain)

Juan-Luis Arsuaga, Ignacio Martínez, Carlos Lorenzo & Ana Gracia

The human cranial remains from Gran Dolina Lower Pleistocene site (Sierra de Atapuerca, Spain)

Departamento de Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid, Ciudad Universitaria, 28040 Madrid, Spain Instituto de Geología Económica UCM-CSIC, Unidad Asociada de Paleoantropología UCM-CSIC. E-mail: [email protected]

In this article we study the cranial remains of the late Lower Pleistocene human fossils from Gran Dolina (Sierra de Atapuerca, Spain), assigned to the new species Homo antecessor. The cranial remains belong to at least five individuals, both juveniles and adults. The most outstanding feature is the totally modern human morphology of the very complete face ATD6-69, representing the earliest occurrence of the modern face in the fossil record. The Gran Dolina fossils show in the face a suite of modern human apomorphies not found in earlier hominids nor in contemporary or earlier Homo erectus fossils. There are also traits in the Gran Dolina fossils shared with both Neandertals and modern humans, which reinforce the hypothesis that Neandertals and modern humans form a clade, and that the Gran Dolina fossils are a common ancestor to both lineages.  1999 Academic Press

Alberto Mun˜oz Departamento de Radiología y Medicina Física, Hospital Universitario 12 de Octubre, Carretera de Andalucía, Madrid, Spain

Oscar Alonso Departamento de Tecnología de Computadores y Automática, Facultad de Ciencias Físicas, Universidad Complutense de Madrid, Ciudad Universitaria, 28040 Madrid, Spain

Jesu´s Gallego Departamento de Astrofísica, Facultad de Ciencias Físicas, Universidad Complutense de Madrid, Ciudad Universitaria, 28040 Madrid, Spain Received 30 June 1998 Revision received 9 March 1999 and accepted 14 March 1999 Keywords: Lower Pleistocene,

Gran Dolina, Atapuerca, Cranium, Homo antecessor.

0047–2484/99/090431+27$30.00/0

Journal of Human Evolution (1999) 37, 431–457 Article No. jhev.1999.0309 Available online at http://www.idealibrary.com on

 1999 Academic Press

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432 Introduction

The Sierra de Atapuerca (Spain) is renowned for the extraordinary large sample of Middle Pleistocene human fossils found in the Sima de los Huesos site (SH) (Arsuaga et al., 1997a). In the 1994 and 1995 field seasons some 80 human fossils (corresponding to a minimum of six individuals) and around 200 artefacts were found in level 6 (TD6) of the Gran Dolina site, also in Sierra de Atapuerca and close to the Sima de los Huesos site (Figure 1). On faunal and paleomagnetic grounds, TD6 was dated to the late Lower Pleistocene (Carbonell et al., 1995; Parés & Pérez-González, 1995). A new species named Homo antecessor was created with the TD6 fossils (Bermúdez de Castro et al., 1997). In this paper we study the cranial remains of the Atapuerca Gran Dolina site. The Gran Dolina cranial sample Middle and lower facial skeleton The facial skeleton is represented by five fragments, each of which corresponds to a different individual. The most complete specimen is ATD6-69. ATD6-69 (found in 1995) [Figure 2(a)– (c), (f); Table 1]. It preserves most of the left side of the face (lacking only the frontal apophyses of the zygomatic and maxillary bones), the entire maxillary alveolar process, the anterior part of the hard palate with part of the vomer attached to it, a portion of the left pterygoid fossa of the sphenoid bone, the right I2–M1 and the left P3 and M1–M3. The I2 and both P3 and M1 are in place, the canine and P4 are only partially erupted, and the M2–3 are still buried within the alveolar bone. Based on the relative stages of growth and eruption the age at death of this specimen was estimated to have been 10 to 11·5 years (Bermúdez de Castro et al., 1997). No fewer than six different individuals are recognized in the dental sample and ATD6-69 was assigned to hominid 3.

ATD6-58 (found in 1995) [Figure 3(d)]. An adult left large zygomaxillary fragment, lacking only the zygomatic process. It preserves the zygomatic process of the maxilla and most of the zygomatic bone. ATD6-19 (found in 1994) [Figure 3(f)]. An adult right facial fragment, consisting primarily of the body of the zygomatic bone (lacking the frontal, orbital and zygomatic processes), a small fragment of maxilla, and the lower end of the intervening zygomaxillary suture. This fragment is morphologically different from the comparable parts of ATD6-58 and, therefore, represents a different individual. ATD6-19 and ATD6-58 could belong to the two adult hominids recognized in the dental sample. ATD6-14 (found in 1994) [Figure 2(d),(f)]. A left maxillary fragment (ATD614) with dc and dm1 in place and permanent I1, I2 and C still buried within the alveolar bone. The dental development would correspond to that of a modern human child between 3 and 4 years old (Carbonell et al., 1995). It has been assigned to the hominid 2. ATD6-38 (found in 1995) [Figure 3(e)]. An almost complete left zygomatic bone, lacking only the end of the zygomatic process. It is clearly from a subadult, and appears to be from an individual that was older than ATD6-14 (hominid 2) and hominid 6. On the other hand, ATD6-38 is very similar in size and shape to the malar bone of the ATD6-69 juvenile and, therefore, could either belong to hominid 1, an early adolescent around 14 years old, or represent an entirely different individual similar in age to ATD6-69 (10–11·5 years). If the latter is true, the minimum number of individuals of the Gran Dolina sample would be seven rather than six. Upper facial and frontal bone regions ATD6-15 (found in 1994) [Figure 3(a)–(c)]. This specimen is the most complete neurocranial fragment. It consists of a large

   

Figure 1. Map of the Sierra de Atapuerca sites.

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Figure 2. (a) ATD6-69, superior view; (b) ATD6-69, left lateral view; (c) ATD6-69, anterior view; (d) ATD6-14, anterior view; (e) ATD6-69, inferior view; (f) ATD6-14, inferior view. Scale bar=2 cm.

    Table 1

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Osteometric variables of ATD6-69 Bräuer, 1988 M45(1) M45 M41c M41d M46b M49a M57(2) M63 M61 M48d M76a M54 M74(1) M48(1)

Howells, 1973 Bijugal breadth Bizygomatic breadth Maximum malar length Malar subtense Bimaxillary breadth (zm:a–zm:a) Interorbital breadth Upper nasal breadth of nasal bones Internal palatal breadth External alveolar breadth at M1/M2 level Maxillo-alveolar breadth Cheek height Zygomaxillary anterior-zygoorbitale (zm:a–zo) Zygomaxillary angle Nasal breadth Clivus-alveolar plane angle Nasospinale-prosthion distance

JUB ZYB XML MLS ZMB DKB

MAB WMH SSA NLB

(103) (115) 42 6·5 (90) (25) 8 35·5 62·7 (66) 24 28 (114–117) 28 60–65 17

All measurements in millimetres and degrees. Parentheses ( ) indicate estimated values.

portion of the frontal squama (mostly the right side, including the sphenoidal and parietal portions of the coronal suture), with parts of the glabellar region and right supraorbital torus, showing some postmortem distortion. Small articulating fragments of the right parietal bone, right nasal bone and right maxillary frontal process are also preserved. The frontal sinuses are well developed [Figure 3(a)], reaching midorbit laterally and not invading the frontal squama. There is also an ethmoidal cell visible in the right side, that does not communicate with the frontal sinus. Although the frontal sinuses of this specimen are fairly extensive, this individual was probably only subadult as is indicated by the pitted surface of the bone, the sharpness of the orbital margin, the thin bone of the squama and of the anterior walls of the sinuses, and by comparison with the Atapuerca-SH (Arsuaga et al., 1997b) and Neandertal (Smith & Ranyard, 1980) samples of immature frontal bones. In modern humans, the main enlargement of the frontal sinus is completed at around 16 years

for boys and 14 years for girls (Brown et al., 1984). Given the large size of the frontal sinus in ATD6-15, a physiological age close to puberty (i.e., close to the end of the adolescent growth spurt) could be assigned to this specimen (Carbonell et al., 1995). However, since the KNM-WT 15000 specimen, which is roughly the same dental age as the hominid 3 individual, shows a well developed frontal sinus, it is possible that the Gran Dolina frontal bone could have belonged to a pre-adolescent individual, ATD6-69 (hominid 3), in which case, as in H. ergaster, the frontal sinus developed at an earlier age in H. antecessor than in modern humans. This also suggests that supraorbital torus shape of ATD6-15 was still far from the adult condition, and that thickness and projection of the torus, as well as frontal squama thickness, would substantially have increased with age. Occipital bone ATD6-89 (found in 1995) [Figure 4(l)]. This represents most of the basilar part,

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Figure 3. (a) ATD6-15, anterior view; (b) ATD6-15, endocranial surface; (c) ATD6-15, superior view; (d) ATD6-58, anterolateral view; (e) ATD6-38, anterolateral view; (f) ATD6-19, anterior view; (g) ATD6-84, lateral view. Scale bar=2 cm.

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Figure 4. Occipital, sphenoid and temporal bones. (a) ATD6-16, lateral view; (b) ATD6-17, basal view; (c) ATD6-17, endocranial surface; (d) ATD6-17, detail of the glenoid fossa; (e) ATD6-18, basal view; the white arrow points to the styloid process; (f) ATD6-20, lateral view; (g) ATD6-57, lateral view; (h) ATD6-57, posterior view; (i) ATD6-16, endocranial surface; the white arrow points to asterion; (j) ATD6-57, endocranial surface; the white arrow points to asterion; (k) ATD6-77, inferior view; (l) ATD6-89, inferior view. Scale bar=2 cm, except for (d), where scale bar is 1 cm.

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from the sphenooccipital synchondrosis to the region of the pharyngeal spine of an adult individual. It is 24 mm broad at the level of the sphenooccipital synchondrosis and its maximum sagittal length (from the pharingeal spine to the sphenooccipital synchondrosis) is around 13 mm. The sphenooccipital synchondrosis is completely obliterated and the specimen preserves parts of the sphenoid, including the posterior end of the sphenoidal sinuses. ATD6-77 (found in 1995) [Figure 4(k)]. This fossil consists of the right occipital condyle (23·1 mm of maximum condyle length and 12·4 mm of maximum condyle transversal breadth), including the hypoglossal canal, the complete petrooccipital suture and the anterior half of the mastooccipital suture. These two occipital fossils (ATD6-77 and ATD6-89) preserve homologous parts and thus correspond to different individuals. Sphenoid bone ATD6-17b (found in 1995) [Figure 4(b),(c)]. The right lateral part of a sphenoid, including most of the right greater wing and the base of the right pterygoid process. The foramen ovale (6·2 mm 5 mm), the lateral half of the foramen spinosum, and the foramen rotundum are present. The base of the pterygoid process is completely filled by a sphenoideal sinus. Although the specimen lacks the pterygoid plates, it preserves part of the pterygoid and scaphoid fossae. This fossil fits with the temporal fragment ADT6-17a (see below). Temporal bone ATD6-16 (found in 1994) [Figure 4(a),(i)]. This fossil consists of a right mastoid angle. Neither the digastric groove nor the mastoid process are preserved. The parietomastoid suture is preserved from asterion to the incisura parietalis (27 mm) and there is also a short segment (27 mm) of the occipitomastoid suture. None of these sutures show

signs of synostosis. The bone thickness at asterion is 7 mm and there are three small mastoid foramina. Along the crista mastoidea, there are some striations that have been interpreted as cut-marks by Fernández-Jalvo et al. (1996). ATD6-17a (found in 1994) [Figure 4(b–d)]. A small portion of the squamous region of a right temporal bone preserving most of the articular fossa. It fits with the associated sphenoid ATD6-17b (see above). On the temporal fragment ATD6-17a there are signs of an arthropathy across the region of the articular eminence [Figure 4(d)]. The postglenoid process is broken and eroded, as is the zygomatic root. There is no indication of synostosis in the sphenotemporal suture. ATD6-18 (found in 1994) [Figure 4(e)]. This fossil represents the lateral half of a left petrous bone and the medial part of the tympanic plate. Damage has exposed the middle and inner ear. In the inferior face of the petrous bone it is possible to distinguish the carotid foramen, the jugular incisure and the base of the styloid process. Using modern human standards (Madeline & Elster, 1995) closure of the occipitomastoidal synchondrosis corresponds to the adult stage. ATD6-20 (found in 1994) [Figure 4(f)]. This specimen is a partial left pterionic region, including the inferoanterior corner of the parietal bone and the anterior half of the superior border of the temporal squama. The bones are thin (4 mm in the parietal bone, 15 mm above the temporoparietal suture) and there is no sign of synostosis in the completely preserved coronal and temporoparietal sutures. ATD6-57 (found in 1995) [Figure 4(g),(h),(j)]. Most of a right mastoid region, including the region of asterion, a long segment of the occipitomastoid suture (48 mm), the digastric groove and the posterior half of the mastoid process. No signs of synostosis can be found in the preserved sutures. There is a single large mastoid

    foramen and two smaller accessory foramina. Bone thickness at asterion is around 8 mm. In contrast to ATD6-16, the lateral surface of the mastoid region lacks cutmarks. ATD6-84 (found in 1995) [Figure 3(g)]. Central part of an adult left zygomatic arch, including the temporomalar suture. Likely, it could correspond to the same individual as ATD6-58. With the exception of ATD6-18, attributed to an adult, none of the temporal bones from TD6 preserves reliable criteria by which to ascertain age at death. However, in the associated sphenoid ATD6-17b the sphenoidal sinus fills the base of the pterygoid process [Figure 4(c)]. According to Aiello & Dean (1990) in modern humans the hollowing out of the sphenoid bone by the sphenoid sinuses has begun by 6 years of age. In the approximately 14-year-old Cranium 6 from Sima de los Huesos, the base of the pterygoid processes is not hollowed out by the sinuses, but in the adult specimens Cranium 4 and Cranium 5 the sphenoidal sinuses fill all the base of the pterygoid processes. Based on modern human standards and the Sima de los Huesos evidence, we would assign ATD6-17 to a late adolescent or an adult specimen. However, as we mentioned above, the KNM-WT-15000 specimen shows an extensive cranial pneumatization, even in the sphenoid bone (Walker & Leakey, 1993). If the Dolina hominids had a sinus growth pattern as in H. ergaster, ADT6-17 could belong to a pre-adolescent individual. Since ATD6-16 and ATD6-57 are both right mastoid regions, they must represent two different individuals. Similarly, although ATD6-18 (a petrous region) and ATD6-20 (a temporal squama) are both from the left side, their reconstructed ages of death are not compatible. Differences in bone thickness lead us to conclude that ATD6-20 corresponds to an individual younger than those represented by ATD6-

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16, ATD6-17 and ATD6-57, but the latter three could be compatible with ATD6-18. In sum, we think that the five temporal bone fragments from TD6 represent, at least, three individuals. Metric analysis To estimate the bilateral diameters of the ATD6-69 face and the ATD6-15 frontal bone when one of the two terminal landmarks was lacking, we used an instrument especially designed to take the 3D coordinates of a point. The bilateral diameters were calculated by doubling the distance from the preserved landmark to the midplane (defined by three sagittal points). We estimated the zygomaxillary angle of ATD6-69 in similar fashion. We also CT-scanned ATD6-69 and ATD6-15 and obtained three-dimensional reconstructions by postprocessing the CT data. This technique has been shown to be a powerful tool for the study and analysis of fossils (Seidler et al., 1997). Basically, the CT method examines the inside of a three-dimensional object by creating two-dimensional images of crosssections of the object. The images are created by passing radiation through one plane of the object, measuring its attenuation and using that attenuation to map the density of the object in that plane. The data were obtained with aid of a General Electric CT scanner at the 12 de Octubre Hospital in Madrid. The scan parameters used were a slice width and sample step of 1·5 mm, which are the highest resolutions possible on that machine. In the end we obtained 36 slice images of 512512 pixels and 16 bits grey levels, covering a field of view (FOV) of 150 mm. The voxel volume of the scanner covers 0·290·291·5 mm3. The virtual 3D reconstruction of ATD6-69 was obtained using the University of Pennsylvania 3dViewnix software on a DEC Alphastation 200.

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Figure 5. Virtual reconstruction of a Homo antecessor face by postprocessing the fossils ATD6-15 and ATD6-69. Scale bar=3 cm.

The reconstruction procedure was performed by thresholding the slice images in order to segregate the bone density range and distinguish the bone from the mineral matrix. In our case, this was not a critical task both because the differences between bone and air density were great and because most of the carbonated clay matrix that had encrusted the fossil had previously been removed mechanically. The 3D model thus achieved can then be displayed on the computer screen and easily rotated, resized, sliced, measured, etc. In a second step, the

missing parts of these fossils were reconstructed as mirror images from the preserved side (Figure 5). From this reconstruction the bilateral dimensions and the zygomaxillary angle were computed and checked against the measurements obtained using the 3D coordinates technique. Facial dimensions Facial remains of juvenile individuals are rare ocurrences in the fossil record of the genus Homo prior to the Upper Pleistocene.

    In addition to the Atapuerca Gran Dolina and Sima de los Huesos (SH) samples, there is the KNM-WT 15000 skeleton. For this reason our comparisons with the Nariokotome face are of particular importance. The estimated breadths of the ATD6-69 upper and middle face (Table 1) are small compared to adult nonhabiline fossil humans. The bijugal breadth (M45(1) in Bräuer, 1988, and JUB in Howells, 1973) was estimated to have been 103 mm, the distance between the zygotemporal points (i.e., the lower ends of the zygotemporal suture) 115 mm, and the bimaxillary breadth (M46b and ZMB) 90 mm. The distance between the zygotemporal points is close to, although perhaps slightly less than, the bizygomatic breadth (M45, ZYB). In the KNM-ER 3733 cranium, the bijugal breadth is 121 mm (Wood, 1991), the bizygomatic breadth around 138 mm (Wood, 1991) and the bimaxillary breadth 106 mm (Wood, 1991) or 101 mm (Rightmire, 1990). Our estimations of KNM-WT 15000 (corrected for shrinkage) on cast are 115 mm for the bijugal breadth and 102 mm for the bimaxillary breadth. The Swartkrans specimen SK 847 has a narrow face (Arsuaga et al., 1997b), but it yields estimated values for the bijugal breadth and bimaxillary breadth, of 112 mm and 100 mm respectively, which are above the ATD6-69 (the bizygomatic breadth values are the same). SK 847 is referred by some authors to H. habilis and to H. ergaster by other scholars (for this taxonomic discussion see Kimbel et al., 1997). The Steinheim face, which could be considered small, yields much larger values than ATD6-69 in bijugal breadth (112 mm; Wolpoff, 1980), bizygomatic breadth (around 132 mm; Howell, 1960) and bimaxillary breadth (107·5 mm; Wolpoff, 1980). In the Atapuerca SH Cranium 5 these diameters are 131·5 mm, 144 mm, and 118·4 mm, respectively. However, Atapuerca SH Cranium 6, with an age at death

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of approximately 14 years, yields (estimated) figures only slightly larger than those of the Gran Dolina specimen in bijugal (108 mm) and bimaxillary (93 mm) breadths, suggesting that these transversal upper and middle face diameters could grow substantially during adolescence in these Early and Middle Pleistocene populations. In the lower face, the maximum external alveolar breadth which is possible to take (at the level of the M1/M2 alveolar septum [Figure 2(c)]), is 62·7 mm, and the internal palatal breadth is 35·5 mm. However, the absolute maximum external alveolar breadth (M61, MAB) is located at the M2 level, and although it cannot be taken directly on the fossil, this diameter can be estimated (by doubling the distance from the left side to the midsagittal plane) to have been 66 mm. These alveolar dimensions are small, but not extraordinarily so: they lie slightly above those of KNM-ER 3733 and below those of KNM-WT 15000; in fact, the maximum alveolar breadth of KNM-ER 3733 is small compared to later Homo. Interestingly, in KNM-WT 15000, external alveolar breadth at M1 is the same as at M2 (in Walker & Leakey, 1993), reflecting parallel cheektooth rows, whereas the tooth rows are clearly divergent in ATD6-69, in which the external alveolar breadth at M2 is clearly greater than at M1. Cheek height (M48d, WMH) in ATD6-69 is short (24 mm), as also is the zygomaxillary anterior–zygoorbitale (zm:a– zo) distance (28 mm); zm:a–zo is ca. 25 mm in ATD6-38. The figures for ATD6-69 are similar to those of the juvenile Atapuerca SH Cranium 6 (approximately 26·7 mm and 29 mm, respectively). According to Rightmire (1998) cheek height in KNM-WT 15000 is 30 mm. Following Howells (1973) we take this measure as the minimum distance between the inferior orbital margin and the lower margin of the maxilla, mesial to the masseter attachment

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and Rightmire’s definition of the measure seems to be the same. It cannot be stated how much the ATD6-69 dimensions are age-dependent, but the cheek height and zm:a–zo distance are substantially greater in the adult Gran Dolina specimen ATD6-58 (31·6 mm and around 37 mm, respectively). The cheek heights of the SH adult specimens AT-629 (36·3 mm) and AT-404 (37·1 mm) are greater still and similar to those of Petralona (36·5) and Sangiran 17 (38 mm, Wood, 1991; 37 mm, Rightmire, 1990). Atapuerca SH Cranium 5 presents cheek heights of 34 mm (right side) and 33·5 mm (left side); such values are similar to those of KNM-ER 3733 (33 mm, Wood, 1991; 34 mm, Rightmire, 1990), SK 847 (32 mm), and Bodo (34 mm). There are, however, Middle Pleistocene fossils with cheek heights of less than 30 mm: e.g., Broken Hill 1 (29 mm), Zhoukoudian X/II (27·5 mm), Arago 21 (26·7 mm), Steinheim (26·6 mm) and Zuttiyeh (c. 24 mm) (the last four measures taken on casts). Among Neandertals, as far as we know, cheek height is greatest in Saccopastore 2 (33 mm); in Saccopastore 1, however, it is only ca. 26·5 mm. In Atapuerca SH Cranium 5, the length of the zygomaxillary suture (zm:a–zo) is 39·3 mm on the left side and 38·5 mm on the right. In AT-629 zm:a–zo is 38·6 mm, and we estimate it to have been 41·4 mm in AT-404. Figures above 37 mm are obtained for Petralona (41·4 mm), Bodo (39 mm) and Sangiran 17 (37·8 mm; Thorne & Wolpoff, 1981). Arago 21 yields a lower value for the zm:a–zo distance (32 mm, left side, Bouzat, 1982), and in Saccopastore 2 it is 34 mm. In sum, with the exception, perhaps, of the alveolar breadths, the facial dimensions of the juvenile face ATD6-69 are small. This is very likely due to the individual being subadult.

Midfacial topography Midfacial topography is particularly well known for modern humans and Neandertals. For Lower and Middle Pleistocene and Upper Pliocene hominids the evidence is more scarce, and geographically and chronologically disperse. The modern human midface is characterized by an infraorbital bone plate oriented on the coronal plane (in an horizontal crosssection) and with an anterior surface sloping down and slightly backwards (Rak, 1983, 1986). The infraorbital bone plate is composed of the zygomatic process of the maxilla and of the maxillary process of the zygomatic bone; it is divided into two triangles by the zygomaxillary suture. Often this region may bear a depression. In other papers (e.g., Arsuaga et al., 1997b) we have used the classic term canine fossa to refer to this depression, although we concur with Maureille (1994) and Maureille & Houët (1997) that the term canine fossa has been used historically in so many different ways that it is now confusing. Here we use the term to refer to an extended infraorbital depression that affects most, if not the entire zygomatic process of the maxilla. We thus distinguish the canine fossa from other depressions, such as a vertical groove inferior to the infraorbital foramen (this furrow-like sulcus, which would lie lateral to the canine jugum, was called the ‘‘sulcus maxillaris’’ by Weidenreich, 1943). Our definition of canine fossa is coincident with the infraorbital depression sensu Maureille (1994), which produces an horizontal incurvation as well as an incurvation of the zygomaticoalveolar crest. Maureille’s (1994) fossula canina, on the contrary, is more similar to Weidenreich’s ‘‘sulcus maxillaris’’, as according to Maureille it is mainly located below the infraorbital foramen. In ATD6-69 the infraorbital depression is placed laterally to the infraorbital foramen.

    The coronal orientation of the infraorbital plate and the more sagittal one of the lateral nasal wall (i.e., that part of the midface that is lateral to the nasal aperture and medial to the infraorbital bone plate) creates a zone of flexion along the junction of these two maxillary surfaces (infraorbital and nasal, or lateral and medial). This flexure can be easily noticed in a transverse (horizontal) crosssection. The inferior margin of the infraorbital plate (zygomaticoalveolar crest or inferior zygomaxillary border) is generally arced, and sometimes there is also a malar notch. Thus, orientation and inclination of the infraorbital region, as well as maxillary flexion and shape of the zygomaticoalveolar crest, are major determinants of the midfacial topography of H. sapiens. The Neandertal midface is characterized by an infraorbital surface that is oriented as much in a coronal as in a sagittal direction and which is continuous in this plane up to the lateral nasal margins, which are themselves anteriorly projecting. Thus, in Neandertals, this uniplanar facial surface (which may sometimes even be slightly convex) lacks both a canine fossa (as defined here) and maxillary flexion. This configuration describes midfacial prognathism. In frontal view, the zygomaticoalveolar crest is straight and oblique and it has a low root. According to Trinkaus (1987) zygomatic root position changed from the level of M1 or M1–M2 in European Middle Pleistocene hominids (Arago 21, Petralona and Steinheim) to the level of M2 or M2–M3 in Upper Pleistocene Neandertals. An anterior zygomatic root position seems to be the primitive condition for Homo as it is at P4-M1 in KNM-WT 15000, at M1/M2 in Sangiran 17 and at M1 in Gongwanling, according to Rightmire (1998); in SK 847 it is at the M1 level. This shift in zygomatic root position was interpreted by Trinkaus (1987) as the result of a retreat posteriorly of the zygomatic arch and its root, and by Rak (1986) as due

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primarily to shortening of the dental arcade length. To both authors, change in zygomatic root position was also correlated with the development of the retromolar space characteristic of Neandertals. If having an infraorbital surface oriented on the coronal plane is the primitive condition for hominids, as we believe, then midfacial prognathism as seen in Neandertals is a derived state. In our opinion, an anteroinferiorly inclined infraorbital bone table, as found in all australopithecines, is primitive for hominids. In early African Homo this surface is either vertical or even slightly sloped anteriorly. In KNM-WT 15000, which is the best example of the facial morphology of H. ergaster and similar in dental age to ATD6-69, the infraorbital surfaces are anteroinferiorly sloping when viewed laterally with the skull oriented in Frankfurt horizontal. Although there is a shallow furrow below the infraorbital foramen (Weidenreich’s ‘‘sulcus maxillaris’’), there is no canine fossa. The midface of SK 847 from Swartkrans is basically similar, also lacking a canine fossa. Since, with the exception of a more marked canine juga, the adult KNM-ER 3733 is similar in facial morphology to KNM-WT 15000, there would have been little change in facial topography had the latter individual survived to an older age. The Gran Dolina specimen ATD6-69 shows a completely modern pattern of midfacial topography [Figures 2(a),(b),(c), 5 and 6], not only in the coronal orientation of the infraorbital surface, but also in the inferoposterior slope of this plane (with the canine fossa), anterior flexion in the maxillary surface and arcing of the zygomaticoalveolar crest. Maureille & Houët (1997) define an infraorbital angle in which vertices are the most lateral point of the nasal rim, the zygomaxillary anterior point and the deepest point in the infraorbital depression. The wider the angle (the closer to 180) the shallower the infraorbital depression. In

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Figure 6. Transversal section of ATD6-69. Scale bar=3 cm.

ATD6-69 the value of the infraorbital angle is 153, almost the same that the modern human average (154.7) and much smaller than the values of the Neandertal specimens La Chapelle-aux-Saints (182.8), Guattari 1 (175.3) and Shanidar 1 (180.2). The ATD6-38 malar bone is morphologically very similar to that in ATD6-69. Although the zygomatic process of the maxilla is not preserved in ATD6-38, the topography of this malar bone strongly suggests the presence of a canine fossa. There is also a clear canine fossa in the adult specimen ATD6-58. As in ATD6-69, this specimen, as well as the adult represented by ATD619, displays an arced lower zygomaxillary border with a high root. These features, therefore, appear to have been invariant throughout growth. The position of the zygomatic root is at M1 in ATD6-69. If it remained anterior, which we think likely on developmental grounds, this would constitute the primitive condition. The orientation of the malar body is, in ATD6-69, more lateral than is usual in modern humans, according to the figures that Maureille & Houët (1997) give for their index of anterolateral cheek projection,

which is the quotient between Howell’s malar subtense (MLS) and malar length (XML). Simmons et al. (1991) point out that the ‘‘flat-faced’’ condition of archaic human fossils like Zuttiyeh is not homologous to the true orthognathism of modern humans, because although the zygomatic is anteriorly facing, flat faces such as that of Zuttiyeh are, in fact, anteriorly projecting. Although the total facial prognathism cannot be measured in ATD6-69, it can be supposed to be large, this being the primitive condition (Arsuaga et al., 1997b). However, the reduction of the total facial prognathism in modern humans is probably related to more general changes in the skull than to facial remodelling (Spoor et al., 1999). No specimen with the definitive modern midface of the Gran Dolina fossils is known prior to fossils from the late Middle/early Upper Pleistocene (oxygen isotope stages 6/5) such as Djebel Irhoud 1, the Skhul and Qafzeh samples and perhaps the more fragmentary Laetoli H18 specimen (as seen in the reconstruction of Cohen, 1996). In Europe, the Middle Pleistocene Steinheim specimen exhibits maxillary

   

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Figure 7. Comparison between the Sima de los Huesos AT-404 fossil (a) and the Gran Dolina ATD6-58 specimen (b). Both fossils show canine fossae, but note the straight inferior zygomaxillary border of AT-404 and the arced inferior border of ATD6-58. Scale bar=2 cm.

flexion (although it could have been exaggerated by post-mortem distortion). But on the contrary, Arago 21 and Petralona show a uniplanar (and somewhat forwardly angled) infraorbital surface; these specimens are derived in the Neandertal direction (Arsuaga et al., 1996, 1997b, 1998). In the Sima de los Huesos sample, Cranium 5 exhibits midfacial prognathism, although the infraorbital surface is somewhat concave and not completely straight. The Sima de los Huesos adolescent Cranium 6 and the younger individual AT-465+AT-624+ AT-764+AT-765+AT-766+AT-1159 also have a slightly concave infraorbital surface, but it is clearly depressed in the AT-404 maxilla (Figure 7) (Arsuaga et al., 1996, 1997b, 1998). In Cranium 5 of the Sima de los Huesos sample, the zygomatic root lies above M2–M3 (as it does in Neandertals); Cranium 5 also exhibits a marked retromolar space in its mandible as well as a conspicuous ‘‘maxillary retromolar space’’. In the late adolescent AT-1100+AT-

1111+AT-1197+AT-1198, the zygomatic root is level with M2-M3, whereas in the earlier adolescent AT-767+AT-963 it is at M2. In Africa, neither Bodo nor Broken Hill 1 presents a modern midface, but the less well preserved face of Florisbad may have had a hollowed-out maxilla. In Florisbad, an associated hominid tooth has been dated by a newly developed ESR technique to ca. 250 ka (Grün et al., 1996). Another (more fragmentary) Broken Hill 2 face looks modern, but the age of both Broken Hill fossils is problematic. In Asia, the Chinese Middle Pleistocene fossil from Dali, although distorted, looks very modern in all midfacial traits. This is certainly not the case in Sangiran 17. The Zhoukoudian facial fragments have been considered modern-like (Pope, 1992), especially in the arced zygomaticoalveolar crest of Maxillae III and V, and Os Zygomaticum II; they are, unfortunately, too fragmentary to establish the entire midfacial

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pattern, and the presence of a canine fossa, as we define it here, as well as the degree of nasal projection, cannot be evaluated. The two Yunxian skulls are considered as being either late Early Pleistocene or early Middle Pleistocene (Chen et al., 1997). According to Etler (1994), Yunxian 1 and 2 possessed a malar region that faced anteriorly; in this feature and in a lower zygomaxillary border that is horizontal and high rooted, these two fossils would be similar to the modern human condition. Nevertheless, a coronal orientation of the cheek bones is the primitive condition. Only Neandertals and their European Middle Pleistocene ancestors depart from this condition (although the midface of Broken Hill 1 is intermediate between typical Neandertal and modern patterns). Etler (1994) also described canine fossae in the Yunxian specimens, but the heavy postmortem distortion of the specimens casts doubts about the supposed modern topography of their faces. On the other hand, while the shape of the zygomaticoalveolar crest is a very variable feature among fossils, a crest that is straight and oblique in frontal view, with a low root, seems to be common in Neandertals and other hominids; we cannot appreciate, on a cast, the ‘‘clear expression of an incisure’’ that Rightmire (1998) observes in KNM-WT 15000. A clearly arced zygomaticoalveolar crest is seen in modern humans, the Gran Dolina fossils and the Zhoukoudian specimens. In the Sima de los Huesos sample, this crest is not Neandertal-like, but it is gently curved in Cranium 5, and more straight and oblique in other specimens. Although the nasal bones of ATD6-69 are missing, the orientation of the lateral nasal walls clearly indicate that the nasal bones were elevated and forward sloping. A projecting nose is one of the most outstanding features of the modern human face. The modern human projection of the pyriform aperture has two different components,

which can be well appreciated in a lateral view: one is the projection of the nasal bones (well visible in a sagittal cross-section), that brings forward the upper border of the nasal rim (i.e., rhinion); the other component is the advanced position (noticeable in an horizontal cross-section) of the lateral nasal margin with respect to the peripheral face, the zygomatic root for instance (this is a consequence of both the lateral nasal wall eversion and the sloping down and slightly backwards of the infraorbital plate). In early Homo (i.e., H. habilis and H. rudolfensis) the midface is flat and the lateral nasal margin is only slightly in front of the zygomatic root; in fact, in KNM-ER 1470, lateral nasal margin and zygomatic root are almost in the same coronal plane. In KNM-WT 15000, KNM-ER 3733 and SK 847 the nasal projection is still weak. It is interesting to note that, as a result of what Kimbel et al. (1997) call ‘‘the anteroposterior compression of the coronal planes of the face,’’ the ‘‘smooth’’ midface of early Homo and H. ergaster is a derived character with respect to Australopithecus, where the nasal rim is placed well in front of the infraorbital plate (Kimbel et al., 1997) (incidentally, this derived trait, i.e., the anteroposterior compression in early Homo and H. ergaster, is shared with Paranthropus). In consequence, the secondary separation of the coronal planes of the face in later humans would be a derived feature, and it is seen for the first time in ATD669. Unfortunately the preserved faces of H. erectus are too fragmentary or deformed as to assess the character state. One variable frequently used to express metrically the Neandertal midfacial prognathism is the zygomaxillary angle (M76a, SSA), which reflects the projection anteriorly of subspinale relative to the bi–zm:a line. Actually, due to the location of subspinale below the nasal spine, the zygomaxillary angle only expresses the anterior projection of the upper region of the lower

    face, but not the anterior projection of the entire nasal region. In Neandertals this angle ranges between 104 and 117, whereas, among the 18 modern human samples studied by Howells (1973), it ranges from 120.055.77 in Tasman females to 138.944.72 in Buriat males. The SH Cranium 5 presents a low value (111.2), while Petralona falls in the upper end of the Neandertal range (117.7; 119 in Stringer, 1983). In Bodo the angle value is 139 and in Broken Hill 1, it is 117. An open angle seems to be the condition for early Homo: e.g., according to Rightmire (1993) the zygomaxillary angle is 143 in both OH 24 and KNM-ER 1813 and 161 in KNM-ER 1470. Rightmire (1998) obtained a value of 143 for KNM-ER 3733 and 133 for KNM-WT 15000; we independently obtained similar figures on casts of these two specimens. Our estimate of the SSA of SK 847 is 147. In all these African fossils the open angle reflects a ‘‘smooth’’ face (in a horizontal cross-section), except in the case of KNM-WT 15000, where the angle is more closed. However, the projection of subspinale relative to the bi–zm:a line has an horizontal and a vertical component. In KNM-WT 15000, subspinale is located in the face much below the position of the zm:a points and, in our opinion, this is the reason for a zygomaxillary angle more closed in KNM-WT 15000 than in KNM-ER 3733. There are no reliable SSA values for Asian H. erectus specimens, although Rightmire (1998) tentatively suggested that the SSA was ca. 125 in Sangiran 17. We find this estimation very problematic due to the postmortem deformation of the face of this fossil. Our estimate of the SSA in ATD6-69 is 114–117, a value which falls in the upper end of the Neandertal range and in the lower end of the modern human range. But since ATD6-69 was a juvenile, the angle could

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have changed during growth, probably becoming smaller. In modern humans, the face grows forward during adolescence (Enlow, 1990), so that is likely that the angle would remain similar or even decrease with growth. In sum, the fully modern looking midface of the Gran Dolina juvenile face (ATD6-69) was unexpected for a Lower Pleistocene fossil. In our opinion, it indicates that the midface morphology of modern humans is a retention of a juvenile pattern that was not yet present in the species to which KNM-WT 15000 belonged, because this latter fossil (of roughly a similar age at death as the Gran Dolina individual) displays the previously familiar early Homo pattern. In fact, the facial morphology of KNM-WT 15000 is that of an adult of its species (as seen in KNM-ER 3733). On the other hand, the adult Gran Dolina facial fragment, ATD6-58, shows that in the species represented by this sample, expansion of the maxillary sinus led to the canine fossa being partially, but not completely, filled in. The very derived Neandertal midface does not preserve any traces of the ancestral morphology seen in the Gran Dolina fossils, but intermediate fossils like Atapuerca SH AT-404 and Steinheim clearly indicate that the Neandertal pattern could derive from that seen in the Gran Dolina hominids. This model predicts that a more or less attenuated version of the juvenile Gran Dolina morphology is more likely to be found in adult Middle Pleistocene specimens with particularly delicate faces (especially females), and of course in immature individuals, and with a higher frequency in the lineage leading to modern humans. The last sentence points to the African continent, but a facial topography like that found in the Dali specimen could mean that there was some gene flow from Africa to Asia in the second half of the Middle Pleistocene.

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448 Zygomaxillary tubercle

The facial specimen ATD6-69 shows a clear zygomaxillary tubercle on the preserved left side. Using the Hauser & De Stephano (1989) scoring system of epigenetic traits, the expression of the tubercle in this fossil would be considered as medium (ca. 1·5 mm) and placed in a maxillary position. After these authors (op. cit.), this trait appears early in ontogeny in modern humans and therefore it would be under genetic control. In ATD6-19, a small adult zygomaxillary fragment, there is also a zygomaxillary tubercle, placed in a maxillary position and slightly projecting (ca. 2 mm). ATD6-58, another adult zygomaxillary fragment, shows a great zygomaxillary tubercle placed in a maxillary position that projects out 3·3 mm. Weidenreich (1943) stated that in the Sinanthropus sample there were no zygomaxillary tubercles in any of the specimens. But, in our opinion, Zhoukoudian Maxilla II displays a clear medium tubercle and, although the suture is not clearly visible on the cast, it seems to be placed in a maxillary position. Moreover, this represents, together with the Gran Dolina specimens, the unique presence of this morphology in the human fossil record prior to the Upper Pleistocene.

Nasal crests There are marked differences between Neandertals and modern humans in the lower part of the nasal aperture (Arsuaga et al., 1997b). The modern pattern of nasal crests was described by Gower (1923) in the following terms. There is a spinal crest running laterally from the nasal spine across the nasal floor and the internal nasal wall. From the insertion of the inferior turbinal bone in the internal nasal wall descends another crest, called the turbinal crest, which may flow into the spinal crest, although there is

usually a flat area in between the two crests. Finally, an extension of the lateral margin of the nasal aperture forms the lateral nasal crest, which may either run down onto the surface of the premaxilla and eventually fade out, or course medially toward the nasal spine. For modern populations Gower (1923) noted various possible configurations: (1) spinal crest absent; (2) all three crests present and separate; (3) spinoturbinal crest fusion (i.e., the spinal crest continues into the turbinal crest); (4) spinolateral crest fusion (i.e., the spinal crest and the lateral crest are connected); and (5) all three crests coalesce. Sometimes a depression or fossa prenasalis lies between the spinal and lateral crests. And, on occasion, the lateral crest may split into two or more crests. In Neandertals, the lateral crest courses directly to the nasal spine, creating a sharp lower margin of the nasal aperture, and the spinal crest may be continuous with the turbinal crest, forming a well-defined margin (Arsuaga et al., 1997b). Finally, approximately level with and probably anterior to the insertion of the inferior turbinal bone there is a remarkable formation of solid bone that projects medially into the nasal cavity (Schwartz & Tattersall, 1996). This configuration is already present in very young Neandertal individuals and, according to Schwartz & Tattersall (1996), a small medial projection is also discernible in the Steinheim skull. A sharp lower margin of the nasal aperture resulting from spino-lateral crest fusion is evident in Arago 21 face, in which, however, a raised spino-turbinal crest and medial projection are lacking. In the two Saccopastore skulls (attributed to oxygen stage 5e), matrix in the nasal cavity obscures internal structures, but the sharp lower nasal margin is typically Neandertal. In the Sima de los Huesos sample and in the African Middle Pleistocene fossils Bodo or Broken Hill 1, the spinal crest runs posterolaterally (instead of laterally) away

    from the nasal spine and the lateral margin of the nasal aperture descends arcuately onto the nasoalveolar clivus, fading out well lateral to the midline. In these fossils, therefore, the nasal aperture lacks a defined inferior margin. In KNM-WT 15000, the lateral crests are almost vertical, and the clivus is depressed between them as it also is in KNM-ER 3733. In ATD6-69, the spinal crest courses posterolaterally to approach a low crest-like structure descending from the anterior margin of the lacrimal groove and from below the posteriorly restricted conchal crest. The lateral nasal crest bifurcates into a medial crest that ultimately joins the spinal crest lateral to the anterior nasal spine and a short, vertical crest that descends upon the nasoalveolar clivus and quickly fades out. Following Weidenreich (1943), Rightmire (1998) described the lateral crest of H. ergaster/H. erectus (Weidenreich’s ‘‘crista nasalis’’) as extending the lower extremity of the nasal aperture anteriorly, well in front of rhinion, whereas in modern humans it is deeply concave or vertical. In our opinion the H. ergaster/H. erectus morphology reflects the lack of nasal projection. In ATD6-69, the lateral nasal margin is vertical and slightly concave. In this fossil, the maximum nasal aperture breadth (M54) is 28 mm. The nasal septum is bent towards the left side.

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canine juga which extend upward to thicken the lateral margin of the nasal aperture; according to Rightmire (1998), the same condition would probably have characterized KNM-WT 15000, upon eruption of the permanent canines. In ATD6-69, in which the canines are erupting, the canine juga are not marked. For Rightmire (1998) the transverse profile of the clivus is not a useful character in sorting the fossils by geographic origin (i.e., to separate African H. ergaster from Asian H. erectus), because the clivus is flattened in the Koobi Fora and Nariokotome specimens but the trait is variable in Asia; according to him the clivus of the Zhoukoudian and Sangiran specimens is convex, but that of Gongwangling could be flattened or intermediate. Palatally, the moderate incisive foramen is located anteriorly in ATD6-69 [Figure 2(a),(e), 8], i.e. less than 5 mm behind the anterior alveolar margin rather than well behind (10 mm or more), as in the H. erectus and H. ergaster sample (Rightmire, 1998). The large incisive fossae (as preserved intact on the right side) are situated anteriorly in the floor of the nasal cavity and the incisive canal is nearly vertical; in H. ergaster and H. erectus the incisive canal lies obliquely (Rightmire, 1998). In the Sima de los Huesos sample and in Neandertals, the incisive canal is also vertical (Figure 8). In ATD6-69, the floor of the nasal cavity is smooth.

Clivus and palate The clivus of ATD6-69 bows gently outward in the sagittal plane (the angle with the alveolar plane is 60–65), and is strongly arced from side to side. The height of the clivus is 17 mm from nasospinale to prosthion (M48(1)), and 21 mm from the nasal spine to the lowest point between the central incisor sockets. In KNM-ER 3733 and KNM-WT 15000 the flattened clivus is markedly prognathic inferiorly. In KNM-ER 3733 the clivus is bounded by

Frontal bone morphology The estimated minimum frontal breadth (M9) of ATD6-15 is 95–100 mm. These values are obtained by doubling the distance from the right frontotemporale to the sagittal plane and are well above those of KNM-WT 15000, KNM-ER 3733, KNM-ER 3883, Sangiran 2 and Trinil (all of which have cranial capacities below 1000 cc) as well as the Zhoukoudian specimens and OH 9. The minimum frontal

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Figure 8. Sagittal sections of Cranium 5 from Sima de los Huesos and ATD6-69. Scale bar=3 cm.

breadth of ATD6-15 falls in the middle of the very large Afro-European Middle Pleistocene fossil hominid range and at the lower end of the Neandertal range. The adult Cranium 4 from Sima de los Huesos (with a cranial capacity of 1390 cc) had a substantially larger minimum frontal breadth

(117 mm), and Cranium 5 (cranial capacity of 1125 cc) yields also a larger figure (105·7 mm). In the adolescent Cranium 6, with an estimated cranial capacity of 1220 cc (Arsuaga et al., 1997c), the minimum frontal breadth is 100 mm. The bistephanic breadth (M10b, STB) of ATD6-15 is estimated to be 100 mm. This value is much greater than in fossils with small cranial capacities, such as KNM-ER 3733 and 3883, OH 9, Trinil, Sangiran 2, and Zhoukoudian 3 and 11. The preserved frontal squama of ATD6-15 is thin (<5 mm) and shows evidence of sagittal keeling. The supraorbital torus is double arced (in frontal view), and slightly ‘‘swept back’’ (in superior view). The glabellar prominence is well separated from the frontal squama by an extensive supraglabellar fossa which merges with a supratoral sulcus that becomes increasingly more shallow laterally. Altogether the supraorbital region is clearly distinct from the squama behind. The maximum thickness of the supraorbital torus (ca. 13 mm) is found at the medial point (as defined by Smith & Ranyard, 1980), from where the bone thins laterally. The trigone is broken but midorbitally the bone is 7 mm thick. Our estimate of trigone thickness (at the lateral point) is 9·3 mm. Lateral toral thickness in KNM-WT 15000 is 9 mm (Rightmire, 1998). The supraorbital torus is straight in OH 9 and all Javanese H. erectus; in the Ngandong sample maximum toral thickness lies laterally, at the trigone. In the Zhoukoudian sample, KNM-ER 3733, KNM-ER 3883 and (very likely) KNM-WT 15000, the continuously thickened brow is more arced. Although it is difficult to ascertain to what extent the morphology of ATD6-15 reflects that of an adult individual, we believe that its pattern clearly deviates from the straight (horizontally oriented) supraorbital torus and the flattened supratoral

    shelf characteristic of Javanese H. erectus and the African OH 9 calvaria (Carbonell et al., 1995). In ATD6-15 the brow thins laterally. We think that this reflects the immature condition of the Gran Dolina individual because lateral toral thinning characterizes subadult individuals of the Sima de los Huesos sample, in contrast to the adults in which toral thickness is more uniform (Arsuaga et al., 1997b). In ATD6-15 supraorbital toral projection is very marked, and it would be extraordinary for a child of 10–11·5 years, which it very well may have been. Nasal bridge The interorbital breadth of ATD6-15, as expressed by the distance dacryon–dacryon (M49a, DKB), is estimated in 25 mm. Although ATD6-15 is a juvenile specimen, its interorbital breadth is slightly above the female modern human sample of Coimbra (mean=22·1 mm, S.D.=2·8 mm, n=40) and it is almost the same as the male mean of Coimbra (mean=24·8 mm, S.D.= 2·9 mm, n=40). Concerning the African Plio-Pleistocene fossils, the dacryon– dacryon distance of ATD6-15 is similar to the adult specimens KNM-ER 3883 (26 mm, on cast), and KNM-ER 3733 (24·5 mm, on cast) and below OH-9 (28·3 mm, on cast). On the other hand, Bodo (37 mm) and Broken Hill 1 (33 mm) yield high figures for the dacryon–dacryon distance compared to the Dolina fossil and the H. ergaster ones. In Europe, the Middle Pleistocene fossils Atapuerca SH Cranium 4 (38 mm), Atapuerca SH Cranium 5 (33 mm), Petralona (34 mm), and Arago 21 (30 mm, on cast) yield figures for the dacryon– dacryon distance well above the ATD6-15 specimen; there are two other specimens that are closer to ATD6-15: Atapuerca SH Cranium 6 (28 mm) and

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Steinheim (26·6 mm, on cast). In the Asian Zhoukuodian specimens sample, the smallest dacryon–dacryon distance is found in Skull II (24 mm, estimated on cast), while Skull I (34·7 mm, on cast) and Skull XII (32 mm, on cast) display very high values. Another variable of interest is the upper breadth of the two nasal bones (at the level of the naso-frontal suture) (M57(2)). In ATD6-15 the uppermost portion of both nasal bones is present, and they are very narrow along the whole preserved portion. The upper nasal breadth is 8 mm, clearly below both male and female modern human means (Coimbra sample: male mean=13 mm, S.D.=2·8 mm, n=42; female mean=12·5 mm, S.D.=2·8 mm, n=42). Compared to other fossils, this diameter in the ATD6-15 fossil is the smallest observed. The African Early Pleistocene specimens KNM-ER 3733 and OH-9 show low values (9·6 mm and 13·1 mm respectively, both taken on cast), while the Middle Pleistocene sample displays much higher figures: Broken Hill 1, 17 mm; Arago 21, 15 mm (on cast); the Zhoukoudian Skull II, d17 mm; Skull III, 17 mm, and Skull XII, 17·3 mm (all three figures from Weidenreich, 1943) and the Atapuerca SH Cranium 4, 20·5 mm (taken on the frontal bone), Cranium 5, 19·5 mm and Cranium 6, 11·4 mm (estimated value). These figures show the broad nasal bones that these specimens have, at least at the nasofrontal suture. Thus, the upper breadth of the nasal bones of the ATD6-15 specimen seems to be, proportionally, smaller than that of other fossils of similar interorbital breadth. Temporal bone morphology The mastoid process of ATD6-57 is small and less projecting than the occipitomastoid region [Figure 4(h)]. There is no occipitomastoid crest along the occipitomastoid suture, but a low paramastoid crest (22·2 mm

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long) is placed medially to the digastric groove [Figure 4(g)]. The digastric groove is deep and narrow (‘‘U’’-shaped) and it is anteriorly obliterated by an elevation of its floor. The mastoid region of ATD6-57 is reminiscent of those of the Neandertals, both in its small and minimally projecting mastoid process and the anteriorly obliterated digastric groove (Vallois, 1969; Vandermeersch, 1978, 1981, 1985; Stringer et al., 1984; Martínez & Arsuaga, 1997). Although these features are common in Neandertals, they are also present in H. habilis (KNM-ER 1813), in the Zhoukoudian Lower Cave sample (Skull III; the presence of this morphology in Zhoukoudian has been also mentioned by Weidenreich, 1943), Laetoli LH-18 and Sima de los Huesos AT-1122 (Martínez & Arsuaga, 1997). Thus, as this trait is polymorphic, it is not possible to decide, on the basis of one specimen, the condition of the Dolina hominids. On the endocranial surfaces of ATD6-57 [Figure 4(j)] and ATD6-16 [Figure 4(i)], the sigmoid sulcus reaches the occipitomastoid suture below the level of asterion. This morphology is also present in the Sima de los Huesos sample (Martínez & Arsuaga, 1997) and other European Middle Pleistocene fossils as well as in the Neandertals (Arsuaga et al., 1989, 1991). The most relevant feature of the petrous bone ATD6-18 is the presence of the styloid process [Figure 4(e)]. As it is well known, fusion of the styloid process to the basicranium depends on age at death. According to Gray (1976), in modern humans the styloid process is ossified by two centres: one for the base, named tympano-hyal, and other, comprising the rest of the process, named stylo-hyal. The former (tympanohyal ) joins the cranial base during the first year after birth, whereas the stylo-hyal segment joins the rest of the bone after the puberty, and in some individuals never becomes united. In the Sima de los Huesos

sample, all the immature individuals (Cranium 6, Cranium 7, AT-421, AT-643 and AT-644) show styloid processes (i.e. tympano-hyal segment) fused to the basicranium (Martínez & Arsuaga, 1997). On the other hand, a styloid process fused to the cranial base is the common condition in Neandertal immatures (La Quina 18, Le Moustier, Krapina A, and Krapina Tp-4; on the contrary, Engis 2 lacks the styloid process fused to the basicranium). It seems that, as in modern humans, in the Sima de los Huesos hominids and Neandertals, the fusion of the styloid process to the cranial base occurs before puberty. In fact, all the adult individuals from the Sima de los Huesos and most adult Neandertals exhibit styloid processes in their cranial bases (Table 2). On the contrary, the styloid process is not fused to the cranial base in the adult specimens of Asian H. erectus, but it is fused in most of the African Plio-Pleistocene adult representatives of Homo, African and European Middle Pleistocene humans, and late Middle Pleistocene specimens from Asia (Table 2). In our opinion (Martínez & Arsuaga, 1997), the fusion of the styloid process to the basicranium, in the adult specimens, is the plesiomorphic condition for Homo, H. erectus being autapomorphic in this trait. Although ATD6-17 lacks the sphenoidal spine region, from the preserved sphenotemporal suture it seems that the sphenoid contributed to the formation of the medial glenoid wall [Figure 4(b),(d)]. According to Andrews (1984) and Stringer (1984), the non-contribution of the sphenoid to the medial glenoid wall is a plesiomorphy, but Arsuaga et al. (1993) found polymorphism for this feature in the Sima de los Huesos sample and they warn about an uncritical use of this character. On the other hand, Martínez & Arsuaga (1997) established that in modern humans there are high frequencies of sphenoid contribution (77·5% to 100%), while the opposite condition

    Table 2

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Fusion of the styloid process to the basicranium Specimens Early modern humans1 Spy 1 Spy 2 Mte. Circeo La Quina 5 La Chapelle La Ferrassie 1 Shanidar 1 Krapina sample2 Steinheim Petralona3 SH sample4 ER-38845 ES-11693 Laetoli 18 Omo 2 Ndutu6

Specimens Yes Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes Yes No Yes Yes

Broken Hill Yunxian7 Xujiyao7 Hexian7 Dali7 Narmada8 Ngandong sample9 Sangiran 43 Zhoukoudian sample10 OH-93 ER-373311 ER-388312 SK-847 ER-373512 OH-2413 Stw-53

Yes No Yes No Yes Yes No No No Yes Yes No Yes Yes No Yes

1 Early modern humans sample: Zhoukoudian C.102, Kow Swamp 5, Brno 3, Pre´dmostı´ 3 and 4, Dolnı´ Veˇstonice 3, Chancelade, Skhul 5. Qafzeh 9 exhibits the styloid process according to Vandermeersch (1981). 2 Krapina sample: Krapina 1, 3, 4, 38.1, 38.7, 38.12 (in this fossil the styloid process is absent), 38.13, 38.15, 38.17, 39.1, 39.3, 39.13, 39.14, 39.15. 3 Rightmire (1990). 4 SH sample: Crania 1, 4, 5, and 8, AT-84. 5 Bräuer et al. (1992). 6 Clarke (1990) and Rightmire (1984). 7 Etler (1994). 8 Lumley & Sonakia (1985). 9 Ngandong sample: Ngandong 1, 7 and 12 (Rightmire, 1990). 10 Zhoukoudian Lower Cave sample: Skull X, Skull XI, Skull XII (Weidenreich, 1943). 11 We agree with Wood (1991), who states that this specimen exhibits styloid process. However, Rightmire (1990) considers that the styloid process is absent in this fossil. 12 Wood (1991). 13 Tobias (1991).

(noncontribution of the sphenoid) is the common state in other humans: Neandertals: 61%; Sima de los Huesos sample: 66·6%; Asian H. erectus: 71%. The noncontribution of the sphenoid is also the condition found in the specimens OH 24, SK 847, KNM-ER 3733, KNM-ER 3883 and OH 9. As this character is polymorphic, it is not possible to determine, from a single specimen, the character state of the Dolina population. The glenoid fossa of ATD6-17 is moderately shallow and not compressed antero-

posteriorly. However, it was probably relatively deep (as it still is in its posterolateral aspect), but pathology, broadly reflected in a field of reactive bone anterior and posterior to the low articular eminence, has apparently remodelled its anterior aspect [Figure 4(d)]. As in the equivalent region of the Sima de los Huesos Cranium 6, the superior border of the temporal squama of ATD6-20 is high and arced [Figure 4(f)]. This trait is seen in Neandertals, modern humans, European and African Middle Pleistocene fossils

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(Martínez & Arsuaga, 1997), and Asian later Middle Pleistocene specimens (Etler, 1994). A low temporal squama with a straight superior border is found in H. habilis, H. ergaster, OH 9 and Asian H. erectus. This is, in our opinion, the primitive condition (Martínez & Arsuaga, 1997). In sum, not all the relevant features of the Gran Dolina temporal bones can be used to establish the evolutionary position of the TD6 hominids. In the case of the mastoid region as well as in the morphology of the medial glenoid wall, since these traits are polymorphic in Homo, it is not possible to decide the condition of the Dolina population on the basis of a single specimen. Unfortunately, the morphology of the anterior glenoid wall, which is useful in phylogenetics (Martínez & Arsuaga, 1997), seems to be pathologically remodeled in ATD6-17. Fusion of the styloid process to the basicranium is interpreted as a retention of the plesiomorphic condition of Homo which separates the Dolina fossils from the derived H. erectus clade. Finally, the high and convex superior border of the temporal squama unites the Dolina specimens with modern humans, Neandertals, and the European and African Middle Pleistocene fossils. Conclusions The Gran Dolina human sample was assigned to a new human species, named H. antecessor, which was considered to be the last known common ancestor of Neandertals and modern humans (Bermúdez de Castro et al., 1997). In his recent analysis of H. erectus and H. ergaster, Rightmire (1998) concluded that the specimens attributed to these taxa were symplesiomorphic in having a forward sloping ‘‘crista nasalis’’, a ‘‘sulcus maxillaris’’ but not a true canine fossa, a high and massive cheek region, and a posterior position of the incisive canal. If this is true, and

since in all these areas ATD6-69 exhibits the modern (apomorphic) condition, two main conclusions are forthcoming: one that the species represented by the Gran Dolina fossils can be ancestral to modern humans, and the other is that all H. erectus younger than 800 ka cannot be ancestral to modern humans if they lack these apomorphies, as Rightmire states. The fusion of the styloid process to the basicranium in the Gran Dolina fossils is a plesiomorphy that also separates the species represented by the Gran Dolina fossils from the apomorphic H. erectus, which according to this trait could not be ancestral to modern humans. The brow morphology in the Gran Dolina frontal bone (ATD6-15) is arced, and thus different from that of the Javanese H. erectus fossils and OH 9, which show a straight torus. The convex superior border of the temporal squama is an apomorphic feature shared by the Gran Dolina fossils, Neandertals and modern humans. These three taxa also share an anterior position of the incisive canal, which is nearly vertical. From these traits the species represented by the Gran Dolina fossils emerges as the last known common ancestor of Neandertals and modern humans. Moreover, in the Gran Dolina fossils there is a marked nasal prominence, a trait also present in Neandertals and modern humans. In early Homo and H. ergaster the midface is clearly flatter, a primitive condition. This trait reinforces the phylogenetic position of the Gran Dolina fossils as a common ancestor to Neandertals and modern humans, but, in fact, more fossils are needed to establish the H. erectus midfacial topography. The Zhoukoudian fossils, in particular, although very fragmentary, seem to show a midface that is small and with an arced zygomaxillary crest. No Neandertal apomorphies are observed in the facial skeleton: (1) posterior zygo-

    matic root position; (2) uniplanar facial surface, lacking both a canine fossa and maxillary flexion (midfacial prognathism); (3) sharp lower margin of the nasal aperture, secondary ‘‘internal margin’’ and medial projection. Although the Gran Dolina sample lacks the above mentioned Neandertal facial apomorphies, the morphology of the Middle Pleistocene Sima de los Huesos sample shows that the Neandertal morphology could derive from that of the Gran Dolina sample. Since the Gran Dolina facial morphology is the modern human one, the conclusion is that the Neandertal face is more derived than ours.

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