we Three new human skulls from the Sima de los Huesos Middle Pleistocene site in Sierra de Atapuerca, Spain LETTERS TO NATURE Juan-Luis Arsuaga’ i, Ignacio Martinez*, Ana Gracia’, José-Miguel Carretero® & Eudald Carbonell! * Departamento de Paleontolss, Universidad Complutense de Maer 28040 Madris. Spin # Latorston Araneta, Uwersfot Rovta Wig, Taragona, Spaia To whnm comespendence shou be addressed ‘THREE. important fossil hominids were found in July 1992 in the Middle Pleistocene cave site called Sima de los Huesos (Sierra de Atapuerea, Burges, Northern Spain). Oneis a complete calvaria 1m 4), the second a virtually complete cranium (cranium 5), 4d sepresents a more fragmentary cranium of an immature individual (cranium 6). There is a large difference in size between the two adult specimens (for example endocranial volume 1,128 em? yersus 1,390 cm’). The Atapuerca human remains are dated to >300,000 years. The Atapnerca cranial sample fits within the ‘archaic Homo sapiens" group, but is well differentiated from the Asian Homo erectus group. The extensive Atapuerca human collection i the most complete sample of Middle Pleistocene ‘humans yet discovered from one site, and appears to document an ‘early stage in Neanderthal evolution. The skulls (Fig. 1) were discovered in a bone-bearing breccia in the Sima de los Huesos cave site (Fig. 2). The Sima de los Huesos human sample so far recovered amounts to more than 700 fossils, belonging to at least 24 individuals (based on dental evidence, refs 1, 2 and J. M. Bermidez de Castto, personal communication). The human fossils are mixed and. without atomic connections, but all skeletal elements are represented inthe sample, without bias". The absence of herbivore bones ‘oF stone implements in the site indicates the human fossils do not derive from a camp site of carnivore activity. The human bone accumulation, therefore could be anthropic or catas: trophic. The faunal composition of the breccia is mainly Ursus deningent* (more than 250 individuals). There are also a few Fossils of carnivores: Pantera leo, Panthera cf. gombaszoegensis, Lynx pardina speloca, Vulpes vulpes, Canidae sp., Mustelidac sp." \ speleothem overlying the human Fossils has been dated to »300,000 years (300 kyr) (J. Bischof, personal communica: tion) (Fig. 2) The cranial capacities of the Atapuerca adult specimens have been measured three times using millet seed, giving a figure of 1,890 cm! (10cm) for cranium 4 and 1,125 em’ (£10 em") for craniuin 5, Thus, although cranium 5 aligns with the smallest European or African Middle Pleistocene specimens (for example Steinheim, Ndutu), the eranial capacity of cranivm 4 Is one of the largest in the Middle Pleistocene record. On the Inasis ef metrical comparisons with the two adult individuals, the cranial capacity of the imm al is estimated a wound 1.100em The vault is high when observed in norma ralis in cranium 4 (height/length mdex = 65.2) and eranium S (Height/length index ~ 67.6; Neandesthal range = 600-66. N= 10, refs 7-10). The maninivm cranial breadth of craniom 4 (164 mm) is much geeater than in cranium 5 (145 mm) and is among the Istpest known in the human fossil record Tn the Atapuerca sample the occipital torus 3s straight in re individ Lnferiow and posterior views, fading towards the asterion. There is always a well defined rough and/or porous surface above the foceipital torus, move o¢ Tess flat but never depressed (which seems to foreshadow the suprainiac fossa found in Swans in Neanderthals). In crania 4, 5 and 6, the opistho. Sat the upper marein of this suprainiae surface, but Deena Te Ructieks © his only slightly fess at the nuchal torus. The tambda-inion-opisthion angles. of ‘cranium 4 (1129") and ‘cranium 5.(116.5*) fall between the values of Petralona and Swanscombe" (Neanderthal range » 122.5°-129", N= 4; ref 8) ‘The ratio (lambda-inion are/lambda-opisthion a¥e)* 100i 61.6 in cranivm 4 and 56.5 in eranium (Neanderthal range 549-66.9, N= 8: refs 7-9). “The mastoid processes are big and projecting in the Atapuerca adult individuals. The juvenite individuals exhibit small m: {oids, which project Tess than the occipitomastoid region, as is common in Neanderthals (both adults and juveniles) and modern human immatures, suggesting retention ofthe immature condition in Neanderthal “The morphology of the supraorbital torus is very consistent in the sample: continuity of the lateral, orbital and glabellar segments and inflated glabellar region without a deep midline depression. A similar pattern can be observed in Bilzingsleben, Stcinheim and Petralona, but notin Arago 21 (which resembles Broken Hill and Bodo). The supraorbital torusis well developed in all the specimens of the Atapuerca sample", including juveniles. Thickness at the midorbital and lateral points of the supraorbital torus" in cranivm 5 (14.1 mm, 146mm) is greater than in cranium 4 (12 mm, 11.5 mm) (Neanderthal ranges: 8. 13.9 mm, 95-133 mm, N'=9). The nasal bones are projecting, dnd the nasal root is at the same level as the glabella, as in Bilzingsleben and Neanderthals (but unlike Petralona and Stein- hheim). The nasiofrontal angle™ is low (137° “The total facial prognathisin is remarkable in cranium 5. The prosthion angle of the upper facial triangle" (60.5°) is close to Petralona (60.2%, ref. 15) and to the lower limit of the Nean- derthal range (59°-72.4", N=7; refs 7-10). The nasoalveolar ‘livus is inclined and the sagittal and transversal facial angles At subspinale indicate a marked midfacial projection, a derived trait shared with Neanderthals (2ygomaxillary angle" = 111.2"; Neanderthal range = 105°-125", N= 8, ref.) The ratio interor- bital breadth/biftontal breadth is high in cranium 4 (32.6) and cranium 5 (29.5) (Petralona ~ 28.7, ref 15; Neanderthal range = 201-299, N~13; ref. 7). The orbits are small (left side breadth 41.2 mm, ‘height 33mm). and mesoconchic. Bi maxillary breadth (1184 mm), cheek height (37 mm) and nasa aperture breadth (38 mm) are very large in absolute terms ane even more in relative terms. The inferior nasal rim morpholog: as Rag aegis peeciecrgrety aeciisaeemoried shen ee ne ce epee Wes Se ee re ear meee ose 17 ner ey Oe ae Seg ric ole sysnaain ge se a ee cae hoa igs eer mmdaranecticmmse roca See teenage don ols is ee! erent ieratars perenne Same Se tee nr ses ca on ees sleet cei pei rey ae NATURE - VoL 362» & APRE 19¢is reminiscent of that of Broken Hull There are no & ie crama 5 and 6 (nor in Petal une Fossa nna and Arago 21). In contrast, 1 canine fossa is present in Steinheim and the Atapuerea speck men AT 404 (a large tragment of the left side of the face) ‘ranivm 5, the maxillary pneumatization is extensive. The frontal sinuses in the Atapuerea sample are well developed but do not reach the supraonbital notch nor penetrate the frontal squama. Cranium 5 exhibits a high and broadly arching inferior zygomaxillary margin asin Bodo, Petratona, Broken Hill, Atago ator Vol 362. # APRIL 198 anium 5 preserves the Hight Fight MO-M? and lef M-M?, a of them heavily ween ‘Lateral view of eraniam 6. Crankim 6 preserves most of the tine andthe fare cho LETTERS TO NATURE 21 oF Steinheim'® but there is no maxillary torus (as is clearly seen in Peualona, Arago 21 or Steinheim). The inferior omanillory margin is also high in cranium 6 and AT-404, but {is straight and more oblique than in cranium 5 Box 1 presents a summary of the morphology of the Atapucrea mple. All appear to exhibit an occipital morpholosy that anticipates the Neanderthal pattern. The supraorbital torus morphology is Neanderthal like, There is a cleat midfacial pro. jection and an inflated manilla in cranium 5. Neanderthal m4. ¢ Facial, of lateral and ¢, posterior view of 535LETTERS TO NATURE 86,2 Map and sections of Sima te los. Huesos, Man view of man excavation areas. & Projected Section along poygonat tine sn a. Staligraphy nd correlations. The Sima de os Hues smote than 500 m from tne entrance ofthe Cen Myer harst system, athengn geophysical stuses torn the surace suggests 2 eaby ancient entrance. row colapsed and sled () Bergamn, personal communeation! Access the ste vs vou 2 413m shall (arrow mb). CR acontenous sala Iii oor extending tm SRA to SRE mostly ‘covered by sterile dark clays ich in bat aro, ‘Bear fossils and te human fossils were found SAM below CR and every sterile hate mar fl Ji SRB thete 1s 3 major accumuation of bear fossis (Utsus deninger). some arteulated below OR crust, together wth tuman fossils. Human ossi5 nluding cranium 4 cranium Sanderanaa 6) were found excanation area 8 together mth some bear bones (Ul dene ed Below a Bone breccia containing only calnnore bones. Other Inumae toss were tour rave 8 (with bear fosss} in aleve! of plastic lays wich vetays Stele laminated sits and sands Speleothem GN covers the bene breccia in alimited ae laquares V0. 16/18). Uranium series dating has een done fon all spelecthems exposed to date within the Sma J Bisco personal communication. Ade ‘of TOkyt was obtaned forthe €PY speleothem, provisng 9 minimum dote. Multiple anahyse of speleothem CR above the section at SHB showed full isotope equitinum indeating a date of 300k ts tempting to project ths speleothem across tothe top of area where the shulls were recovered, bt whether i pinches uta the eter val or wos mechanical emovedby erin expo {ation by cavers is net clear ot present The presence of Numan fossis below CR. however, Inceates o minima age of 300 ye fr the rurnn ‘ssemblage Drawings wore provided by AT Ortega and Grupo Fspelecigice Easiwcis ® ES be EB ow apomorphies have also been found in the Atapuerca mandibular sample!" In the posteranial skeleton there are also many taits shared with Neanderthals, but these could be plesiomorphies"™ ‘The juvenile specimen cranium 6 shows that the morphological pattern of the Atapuerca sample arises early in ontogeny, with the exception of the development of the mastoid processes and the facial prognathism, Apart from the Neanderthal apomor Phies, the Atapuerca cranial sample displays set of tits which ate polymorphic and should therefore be wsed carefully in phylogenetic reconstruction” *!. The Atapuctea ecanial sample departs from the condition generally observed in Asian TT cerecius®** in several traits: more elevated cranial vault, separ- ation of vertex from bregma, doble arched supraorbital torus: Jess angulated occipital bone with opisthocranion net coinel ent 536 16 EE eet FEB tsar poe [EID ssenen EB] sem: with inion, occipital torus reduced laterally, weak tympanic bone, high’and rounded temporal squama. Although the lower Jimit of the cranial capacity range in Atapuerca (and in archaic Homo sapiens’) oveslaps the upper limit of the Asian Homo rectus sample, there 1S a substantial overall increase in brain Asa whole, Atapuerca and the European Middle Pleistocene cranial sample fit a model of local evolution with increasing Frequencies of Neanderthal traits, although @ more accurate chronological framework is needed to establish the evolutionary tempo. Study of the whole Atapuerea cranial, dental, and posteranial sample (which is likely to increase with further excavations will provide an unprecedented documentation of Middle NATURE - VoL 962 + 8 APRN 199 Fesenetic reconstruction many characters, owe hs 9 a a a ‘Sma Fume tg 20 8 1092 Scie on fae 3a 2 21h 2 Eat? thane eae pity ce) EN 16 Rows ti fo sata 27 kaos PE ih smote eS Stam me an ata te yore gah hemes ae fe Scie oar gece ate Ruan hen ase gee tre sr Tone acne apa Eaten ta mena a nt esrch DORSAL Sed Oren Come ar own Cote Toone St