Evolutionary Anthropology 13:25–41 (2004)

ARTICLES

The Atapuerca Sites and Their Contribution to the Knowledge of Human Evolution in Europe J. M. BERMU´ DEZ DE CASTRO, M. MARTINO´ N-TORRES, E. CARBONELL, S. SARMIENTO, A. ROSAS, J. VAN DER MADE, AND M. LOZANO

Over the last two decades, the Pleistocene sites of the Sierra de Atapuerca use of terms such as “advanced,” (Spain) have provided two extraordinary assemblages of hominin fossils that have “primitive,” “early archaic,” “archaic,” helped refine the evolutionary story of the genus Homo in Europe. The TD6 level of and “late archaic” to modify Homo the Gran Dolina site has yielded about one hundred remains belonging to a sapiens. These terms and other similar minimum of six individuals of the species Homo antecessor. These fossils, dated ones2,3 have no taxonomical validity, to the end of the Lower Pleistocene (800 kyr), provide the earliest evidence of but suggest a need to describe mor- hominin presence in Western Europe. The origin of these hominins is unknown, but phological diversity. they may represent a speciation event from Homo ergaster/Homo erectus. The The cladogenetic model also has TD6 fossils are characterized by a significant increase in cranial capacity as well as difficulties. Cladistics requires the es- the appearance of a “sapiens” pattern of craniofacial architecture. At the Sima de tablishment of character polarities los Huesos site, more than 4,000 human fossils belonging to a minimum of 28 (the phylogeny of the characters), the individuals of a Middle Pleistocene population (ca. 500–400 kyr) have been re- selection of independent traits, and covered. These hominins document some of the oldest evidence of the European the identification of homoplasies. roots of Neanderthals deep in the Middle Pleistocene. Their origin would be the These difficulties have opened several dispersal out of Africa of a hominin group carrying Mode 2 technologies to Europe. debates concerning the recognition of Comparative study of the TD6 and Sima de la Huesos hominins suggests a one or more species in a given hyp- replacement model for the European Lower Pleistocene population of Europe or odigm. One of the most prominent ex- interbreeding between this population and the new African emigrants. amples concerns the possible parti- tion of a large portion of the Early Pleistocene fossil record into two spe- Since the late 1980s, paleoanthro- the genus Homo.1 The anagenetic evo- cies, Homo erectus, Dubois 1892, and pology has witnessed a paradigm shift lutionary model, which postulate an Homo ergaster, Groves and Mazak in interpretation of the evolution of unbroken lineal temporal succession 1975. Homo ergaster would be re- of the reproductive continuity of stricted to Africa (if we consider the Homo habilis, Homo erectus, and hominins found in the Dmanisi site, Homo sapiens, representing three evo- Republic of Georgia, to belong to a Jose´ Marı´a Bermu´ dez de Castro is Re- lutionary grades, is gradually being different species4), while Homo erec- search Professor at the Consejo Superior replaced by the cladogenetic model of tus may have representatives in Asia de Investigaciones Cientı´ficas(CSIC), Spain 1 and co-director of the Atapuerca Research speciation, which recognizes several and Africa. The distinctions are Project. E-mail: [email protected] speciation events throughout the evo- based on the absence of some specific Eudald Carbonell is Professor at the Uni- lution of the genus Homo. These traits in the African fossils that are versity Rovira i Virgili of Tarragona, Spain and co-director of the Atapuerca Re- events (cladogenesis) might have been present in the Asian ones, to which the search Project. favored by successive dispersals of species name erectus applies. These Marı´a Martino´ n-Torres, Susana Sarmiento and Marina Lozano are researchers with hominins out of Africa and migratory include a midline keel on the vault, the Atapuerca team, having a primary inter- movements between Africa and Eur- strong reduction of the postglenoid est in dental anthropology. asia during the Pleistocene, as well as process, an angular torus at the pos- Antonio Rosas is Research Fellow at the CSIC, Spain and member of the Atapu- events of reproductive isolation due to terior-inferior corner of the parietal erca Research Team. climatic and ecological changes. bone, overall thickening of the brain- Jan van der Made is Research Fellow at the CSIC, Spain and member of the Ata- The anagenetic model divides the case, and reduced superstructures in puerca Research Team. fossil record, or the morphological the temporal-occipital region. More- space of the genus Homo, into three over, Homo erectus ss exhibits a Key words: Homo antecessor; ergaster; heidel- evolutionary grades. As the morphos- styloid process, as well as differences bergensis; Neanderthals pace is filled with new findings, it is in the size and shape of the supraor- becoming increasingly difficult to bital torus.5–7 The debate about the © 2004 Wiley-Liss, Inc. agree on the exact boundaries be- partitioning of the fossil record is be- DOI 10.1002/evan.10130 Published online in Wiley InterScience tween species. The difficulties of this yond the scope of this paper but, from (www.interscience.wiley.com). model are exemplified by the frequent this point on, we assign the specimens 26 Bermu´dez de Castro et al. ARTICLES

THE SIERRA DE ATAPUERCA SITES The Sierra de Atapuerca is a small hill of about twelve square kilometers that rises 1,079 meters above sea level and approximately 100 meters above the alluvial flatness of the Arlanzo´n river. The Sierra de Atapuerca is lo- cated in northern central Spain (Du- ero Basin) fourteen kilometers east of the historical city of Burgos. It con- tains numerous karst cavities in Cre- taceous limestones that are filled with Pleistocene sediments (Fig. 1). The Sima de los Huesos is a blind cavity of 8 ϫ 4m2 located well inside the Cueva Mayor-Cueva del Silo cave system of the karst of Sierra de Ata- puerca (Fig. 1). The access to this chamber is a vertical conduit 14 m deep, which ends with a steep inclined ramp about 9 m long. The first human remains, associated with a large as- semblage of cave-bear (Ursus deningeri) fossils, were found here in 1976.12 This site has been systemati- cally excavated since 1984. Over sev- eral decades, tons of sediment were turned over by cavers hunting for cave-bear teeth.13 A meticulous and methodical excavation began in Figure 1. Map of the Trinchera del Ferrocarril and Cueva Mayor, showing the location of the 1988.14 Arsuaga and coworkers14 de- main Atapuerca sites. TD: Gran Dolina; TG: Galerı´a; TN: Trinchera Norte; TZ: Covacha de los scribed the stratigraphy and many Zarpazos; TE: Sima del Elefante; SH: Sima de los Huesos. other aspects of the Sima de los Hue- sos site and other nearby cavities. They also published cross-sectional of the African Early Pleistocene, in- Despite the internal debate gener- diagrams of the Sima de los Huesos cluding KNM-ER 992 (the holotype of ated by the cladogenetic model, most site and a map of the excavation grid. the species), KNM-ER 3733, KNM-ER authors have abandoned the gradual- The stratigraphy, geological history, 3883, and KNW-WT 15000 (the Tur- ist model for the “phylogenetic species and preliminary dating of the site can kana boy) to the species Homo er- concept” and the recognition of a be found in Bischoff and coworkers.15 gaster. larger number of species in the fossil All the human fossils were recovered Most authors suggest the use of record of the genus Homo. This situ- from the same unit, which is shaped apomorphies (unique derived traits) ation has triggered an ongoing debate by breccias of clay-supporting bones, for the recognition of a species in a about the number of cladogenetic blocks, and clasts15 of varying thick- strict application of the cladogenetic events, the nomenclature of the iden- ness along the site’s profile. Appar- model.8 However, trait exclusiveness tified species, and possible evolution- ently, all fossils were deposited in the is not as common in the fossil record ary scenarios. For the past thirty site during the same sedimentation as it might seem. Given this situation, years, the research team of the Sierra period.15 criteria that are less strict, such as the de Atapuerca sites (Spain) has con- Previous radiometric and paleo- presence of a unique combination of tributed to this debate through the magnetic analyses, as well as biochro- apomorphic (derived) and plesiomor- discovery of two hominin fossil as- nological data, pointed to an age of phic (primitive) traits frequently has semblages from the Sima de los Hue- 200 to 320 kyr (oxygen isotope stages been used.9,10 Furthermore, due to the sos and Gran Dolina sites. These as- 7 to 9) for the Sima de los Huesos difficulties we have noted, some au- semblages, as well as other specimens hominins.15–17 However, recent radio- thors consider that the species diag- discovered in the last decade in Africa metric studies (U-series) of a 14-cm- nosis does not need a cladistic basis, and Europe, give insight into the rela- thick in-situ speleothem overlying the but can be made through the phenetic tionship between Early Pleistocene mud-breccia containing the human determination of a distinctive mor- Homo and the lineage that gave rise to bones has provided a minimum age of photype.11 Homo sapiens. 350 kyr for these hominins.18 An esti- ARTICLES The Atapuerca Sites 27 mated age of 400 to 500 kyr (oxygen continuous from TD3 to TD11 and per part of TD6, the Aurora stratum, isotope stages 12 to 14) for these some levels (TD4, 5, 6, 7, 10, and 11) corresponds to a Mediterranean forest hominins is based on the rate of contain abundant stone tools. composed of Quercus (oak, holm, gall- growth of the speleothem, correlation In 1993, with the aim of performing oak) and Cupresaceae (cypress), as of the fauna (micro- and macro-mam- a more detailed stratigraphic study of well as Olea, Celtis, and Pistacea. The mals) at Sima de los Huesos with that the Gran Dolina site, our team exca- structure and composition of the at other Atapuerca sites (for example, vated an archeological survey pit of 6 mammals and avian paleocommuni- TD6, TD8, TD10, and TD11 levels of m2. In July 1994, the test pit reached ties is consistent with a Mediterra- Gran Dolina), and the normal magne- level 6 (TD6). In one of its strata, nean climate similar to the present tization of the Sima de los Huesos fos- known since then as the Aurora stra- one.26,27 Therefore, the Aurora stra- silifereous mud.18 tum, a rich assemblage of fossils and tum could be correlated with the oxy- The current hominin sample from lithic industry was found.22 The exca- gen isotope stage 21 (warm). The TD6 Sima de los Huesos consists of more vation of this stratum was completed macromammals include Vulpes sp., than 4,000 fossil remains. Consider- in 1996. The human sample recovered Canidae indet., Mustelidae indet., ing all skeletal elements, it represents includes a total of 86 hominin re- Panthera sp., Felis silvestris, Ursus sp., more than the 80% of the worldwide mains, 250 lithic pieces, and hundreds Proboscidea indet., Equus sp. Stenon- Middle Pleistocene record for the ge- of macrovertebrate remains. iano, Stephanorhinus etruscus, Sus nus Homo.18 The relative homogene- The first paleomagnetic investiga- scrofa, Dama dama vallonetensis, Cer- ity of the sample and the fact that all tion of the Gran Dolina site was per- vus elaphus cf. acoronatus, Megaloc- fossils were recovered from the same formed by Pare´s and Pe´rez-Gonza´- eros cf. verticornis, Capreolus capreo- level strongly support the notion that lez.23 They found a paleomagnetic lus.28,29 The fauna is considered all of these hominins belonged to the typical of the end of the Early Pleisto- same biological population. cene and beginning of the Middle The Sima de los Huesos hypodigm The current hominin Pleistocene. Among microvertebrates, represents a minimum of 28 individ- the presence of Mimomys savini, also sample from Sima de los 30 uals. The most plausible explanation represented in TD7 and TD8, is for this striking fossil accumulation is Huesos consists of more noteworthy, as this taxon persisted at the use of this cavity by the human other European sites until 450 kyr than 4,000 fossil remains. 31,32 population of Atapuerca as a place to ago. deposit corpses. The group may have Considering all skeletal The TD6 human fossil record com- died over a relatively short period or elements, it represents prises more than 85 fragmented bones because of a catastrophic event.14,19 In belonging to the cranial and postcra- 1998, the finding of a handaxe with more than the 80% of nial skeleton. The sample includes more than 43 parts of clavicles, radii, exceptional characteristics provided the worldwide Middle femora, vertebrae, ribs, and patellae, the first evidence of lithic industry at Pleistocene record for metacarpal, and metatarsal bones, this site.20 In our opinion, this discov- and pedal and manual phalanges. The ery reinforces the hypothesis of the the genus Homo. cranial sample is represented by frag- anthropic accumulation of the homi- ments of frontal, parietal, temporal, nin remains with possible symbolical occipital, maxillary, zygomatic, sphe- rituals. noid, and mandibular bones. A total Near the end of the nineteenth cen- of 30 deciduous and permanent teeth tury, a British mining company inversion of the TD7 level 1 m above were identified as human. The human opened a railway trench in the south- the Aurora stratum, which they iden- remains were assigned to a minimum western slope of the Atapuerca Hill tify with the Matuyama-Brunhes of six individuals identified by the less than 1 km from the entrance of boundary. Another study by these au- 21 maxillae, mandibles, and teeth (Table the Cueva Mayor. Since 1978, some of thors confirmed that the lower levels 1). Two isolated lower incisors were the exposed cave infillings along the (TD1–TD6) displayed reversed polar- attributed to two adult individuals now-abandoned railway trench have ity, whereas the upper levels (TD7– TD11) were normal. At the bottom of whose age at death is difficult to as- been systematically explored, sam- sess, but were probably young adults. pled, and excavated. The vertical sec- the TD section, Pare´s and Pe´rez- tion of one of these deposits, Gran Gonza´lez reported evidence of a short Dolina, is 18 m high, formed by 11 normal polarity event, which they in- THE ATAPUERCA HOMININS successive levels deposited from the terpreted as being the Jaramillo or late Early Pleistocene to the end of the Kamikatsura event. The electron spin Sima de Los Huesos Middle Pleistocene.21 The lowest resonance and U-series results ob- Study of the human fossils from stratigraphic levels (TD1 and TD2) tained by Falgue`res and coworkers24 Sima de los Huesos has revealed prim- contain sediments of interior facies also confirm an age range between itive features not found in Upper typical of a closed cave. With the ex- 780 and 857 kyr for TD6. Pleistocene Neanderthals, transitional ception of TD9, the paleontological Pollen studies of the Atapuerca sites traits associated with the Neanderthal record (pollen and faunal remains) is by Garcı´a Anto´n25 suggest that the up- morphology, and some more derived 28 Bermu´dez de Castro et al. ARTICLES

TABLE 1. Mesiodistal (MD) and Buccolingual (BL) Dimensions of the Canines and Postcanine Teeth of the Atapuerca Sima de los Huesos and TD6 Hominins Maxilla Mandible N X S.D. Range N X S.D. Range MD 17 8.6 0.3 8.1–9.6 19 7.6 0.4 6.9–8.5 SH C BL 18 9.7 0.5 8.8–10.7 18 8.5 0.7 7.3–10.1 MD 8.9 8.1 TD6 H1 BL 11.0 10.0 MD 13 8.0 0.5 7.2–8.9 19 7.9 0.4 7.2–9.0 SH BL 13 10.7 0.6 9.7–11.8 19 8.9 0.6 7.9–10.0 P3 MD 8.4 8.8 TD6 H1 BL 11.7 10.6 MD 8.8 TD6 H3 BL 12.1 MD 12 7.6 0.5 7.1–8.4 23 7.2 0.5 6.0–8.0 SH BL 13 10.4 0.6 9.5–11.3 23 8.6 0.6 7.2–10.1 P4 MD 8.0 8.2 TD6 H1 BL 11.7 10.2 TD6 H3 BL 11.6 MD 16 11.1 0.6 9.9–12.3 23 11.2 0.5 10.3–12.1 SH BL 16 11.5 0.7 10.3–13.0 23 10.4 0.5 9.6–11.6 M1 MD 12.1 12.2 TD6 H1 BL 13.1 11.8 MD 11.9 TD6 H3 BL 12.1 MD 17 9.9 0.9 8.1–11.6 26 11.0 0.5 9.9–12.1 SH BL 17 12.1 0.8 11.0–13.8 26 10.2 0.5 9.3–11.5 M2 MD 12.1 13.5 TD6 H1 BL 13.7 12.0

Neanderthal traits, especially in the su- phies, and incipient Neanderthal-like dependent hominin clade evolved into praorbital torus, facial skeleton, and traits, suggesting the inclusion of the Neanderthal human population, mandible.33–36 The dental sample also these specimens in the species Homo which, according to several authors, displays a general morphology and pro- heidelbergensis as a chronospecies of should be included in the species portions that are very similar to those the European-Neanderthal lineage. Homo heidelbergensis.36,45,46 observed in Neanderthals.37,38 There- This taxon was proposed by Otto fore, this sample supports the Euro- Schoetensack40 to name the mandible pean roots of Neanderthals deep in the found in 1907 in the fluvial deposits of Gran Dolina, TD6 Level Middle Pleistocene. This lineage can be the Neckar river near the small Ger- Studies of the TD6 human fossils tracked through the specimens recov- man locality of Mauer, nor far from reveal that most of the dental traits ered at other Middle Pleistocene Euro- the city of Heidelberg. The Mauer are plesiomorphic for the genus pean sites such as Arago, Montmaurin, mandible is probably the oldest spec- Homo, with a tendency toward en- Petralona, Pontnewydd, Steinheim, and imen from the European Middle Pleis- larged anterior teeth. This appears to Swanscombe. In all these specimens, tocene population. This mandible be a derived trait in Homo ergaster we can observe one or more Neander- shows clear affinities to other Euro- that is shared with European and Af- thal apomorphies in combination with pean specimens such as Arago 2, rican Middle Pleistocene populations. primitive traits lost in Upper Pleisto- Arago 13, and the first mandible dis- The TD6 mandible displays a general- cene Neanderthals.33,36,39 covered at Sima de los Huesos (Ata- ized morphology in common with Af- According to Arsuaga and col- puerca 1).41,42 Rosas and Bermu´ dez rican, Early European, and Middle leagues,36 “Middle Pleistocene Euro- de Castro43 showed that the Mauer Pleistocene hominins. However, it peans and Neanderthals represent the mandible displays a set of traits that does not demonstrate distinctive Afri- same ‘evolutionary’ species, an ances- form the structural basis through can traits such as corpus robustness tral-descendant sequence of popula- which Neanderthal apomorphies and strong alveolar prominence. tions without rupture of the reproduc- eventually were fully developed. The assessment of these traits, as tive continuity.” However, these Moreover, study of the Mauer mandi- well as the chronological and geo- authors also state that the European ble dental morphology and propor- graphic situation of the TD6 level of Middle Pleistocene population can be tions reveals the proximity between it Gran Dolina, initially led us to con- defined by a combination of various and the Sima de los Huesos and Ne- sider the Aurora stratum hominins as plesiomorphies not found in later Ne- anderthal samples.43,44 It is clear that a representation of a primitive form of anderthals, Neanderthal apomor- during the Middle Pleistocene an in- Homo heidelbergensis.22 However, the ARTICLES The Atapuerca Sites 29

1995 finding of several remains be- bossing, the high contour of its tem- Kabwe, Elandsfontein, and Ndutu in longing to the facial skeleton drasti- poral squama, and the minimum and Africa, and maybe Dali, Jinniushan, cally modified our original assess- maximum dimensions of its frontal and Yunxian in Asia. This fossil assem- ment. The most striking attribute of breadth, exceeds the values for Homo blage would represent the stem group the find was the modern morphology erectus/Homo ergaster. Furthermore, for Neanderthals and modern humans. in the facial skeleton, representing the the crista nasalis falls vertically from This model had been suggested previ- earliest occurrence of a modern face the rhinion, projecting the nose in a ously by Stringer50,51 and Stringer and in the fossil record. These TD6 human way similar to that in modern popu- McKie,52 and defended by Tattersall,53 remains exhibit a unique combination lations. Nevertheless, the Bodo cra- reviving use of the designation Homo of a modern face with a primitive den- nium shows a very inflated maxilla heidelbergensis. tition. They were subsequently attrib- without a canine fossa. Finally, the The one-million-year-old specimen uted to a new species that the Atapu- incisive canal follows a nearly vertical from Buia (Northern Danakil Depres- erca research team named Homo trajectory, having an anterior position sion, Eritrea), which was partially de- antecessor.47 We further suggested 6 to 8 mm behind the septum separat- scribed by Abbate and coworkers,54 that this species might represent the ing the central incisor sockets. The displays primitive traits, including its last common ancestor to both the Ne- Bodo cranium shares this trait with 750 to 800-cc cranial capacity, that anderthal and modern human lin- are characteristic of Homo erectus/ eages. This hypothesis implies that Homo ergaster. However, this speci- Homo antecessor had an ancestor-de- . . . TD6 human remains men also shows some “progressive scendant relationship with both Euro- exhibit a unique traits,” such as the high position of its pean and African Middle Pleistocene greatest biparietal breadth. According populations. combination of a to Abbate and colleagues,54 the Buia modern face with a cranium could provide the key to un- derstanding the time, place, and A SPECIATION EVENT IN THE primitive dentition. They model of the origins of Homo sapiens. LATE EARLY PLEISTOCENE? were subsequently Asfaw and coworkers55 have recently described the calvarium recovered In 1996, Rightmire48 proposed that attributed to a new a speciation event occurred either in from the Dakanihylo Member of the Africa or Western Eurasia early in the species that the Bouri Formation (Middle Awash, Middle Pleistocene or before. Right- Atapuerca research Ethiopia), which is from the same pe- mire reached this conclusion from his riod as the Buia cranium. The Daka study of a cranium recovered in 1976 team named Homo calvarium has a cranial capacity of at the locality of Bodo, in the Middle antecessor. We further 995 cc and has morphological similar- Awash region of Ethiopia. The Upper ities to the Buia specimen. Asfaw and suggested that this 55 Bodo Sand Unit, from which this associates believe that this skull specimen was collected, has been species might represent should be included in the species dated by the argon-argon method to the last common Homo erectus. They propose an evolu- about 640 kyr (Middle Pleistocene). tionary continuity in Africa, from fos- This age was later ratified by archeo- ancestor to both the sils such as KNM-ER3733 and KNM- logical and paleontological evi- Neanderthal and ER3883 to OH9, Daka/Buia, and dence.49 Rightmire48 pointed to clear Bodo, but suggest that a speciation similarities between the Bodo cra- modern human lineages. event in Africa may have taken place nium and the species Homo erectus/ approximately one million years ago. Homo ergaster, such as the great Manzi, Bruner, and Passarello56 agree breadth and heavy buttressing of the that the Daka calvarium should be face (massive zygomatic bones), very considered as part of an African evo- Middle Pleistocene European homi- thick vault bones, the low and archaic lutionary lineage spanning the inter- nins, Neanderthals, and modern hu- appearance of the braincase, a flat- val from approximately 1,800 kyr up mans. tened frontal profile, and a prominent to about 1,000 kyr. However, these au- angular torus. In combination with Consequently, the speciation sug- thors do not believe that the Bodo and 48 these primitive traits, Rightmire also gested by Rightmire would be charac- Kabwe Middle Pleistocene specimens described the Bodo cranium as having terized by the appearance of some de- indicate a continuation of the same some synapomorphies with later Mid- rived traits in both the face and the African lineage. dle Pleistocene populations and mod- braincase. According to his view, the The common idea underlying these ern humans. In particular, the cranial most appropriate interpretation of the studies is the presence of one or more capacity of Bodo is around 1,300 cc, data would be to include the Bodo spec- evolved forms of Homo erectus/Homo exceeding the upper limit of 1,100 cc imen in the species Homo heidelbergen- ergaster having derived traits pointing in Homo erectus. The large capacity of sis, together with other Middle Pleisto- to the origin of modern populations. the Bodo cranium, reflected in its cene specimens sch as those from This idea was proposed some years broad midvault with signs of parietal Arago, Mauer, or Petralona in Europe, ago with the notion of “archaic” 30 Bermu´dez de Castro et al. ARTICLES

Figure 2. The partial face ATD6-69 (Hominid 3 from TD6) exhibits a completely modern pattern of midfacial topography. ATD6-69 shares with Neanderthals and modern humans an anterior position of the incisive canal, which has a nearly vertical course.

Homo sapiens (see, for instance, enough for precise estimation of the of the Ceprano basin, as well as the Wood2, Stringer, Howell, and Melen- cranial capacity of the TD6 hominins, available K/Ar dating, give an age to tis,57 and Rightmire.58 Following the the estimated minimum frontal this fossil or more than 700 kyr, prob- concept of “evolutionary grade,” this breadth of the ATD6-15 frontal bone ably 800 to 900 kyr.62 The first study suggested a progression toward Homo (around 100 mm) suggests a cranial of the Ceprano calvarium revealed sapiens and the Neanderthals. The capacity greater than 1,000 cc for similarities to Homo erectus, although TD6 hominin findings are crucial in Hominid 3.22 The TD6 hominins share some general traits related to the large solving this problem. The ATD6-69 three derived traits with modern hu- cranial capacity of this specimen, es- maxilla (Hominid 3) has a fully mod- mans, Neanderthals, and African and timated at 1,185 cc, suggested the ern pattern of midfacial morphology59 European Middle Pleistocene popula- need for prudence in its taxonomic (Fig. 2). Clearly, this specimen be- tions59; these are a convex superior assignment.62 Later, Ascenzi and as- longed to an adolescent47 with incom- border of the temporal squama, an sociates63 assigned the specimen to plete facial growth. However, anterior position of the incisive canal, late Homo erectus. A new reconstruc- ATD6-19 and ATD6-58, which repre- and a marked nasal prominence. As a tion of the Ceprano calvarium by R. J. sent two adults, also exhibit modern result, Homo antecessor appears to be Clarke, M. A. de Lumley, and F. Mal- traits (see Figs. 3d and 3e in Arsuaga the common ancestor of all of legni confirmed the previous taxo- and coworkers59). ATD6-58 shows them.59, With regard to the postcra- nomic assessment.63,64 More recently, expansion of the maxillary sinus that nial skeleton, Carretero, Lorenzo, and Manzi, Mallegni, and Ascenzi65 per- reduces expression of the canine Arsuaga60 and Lorenzo, Arsuaga, and formed a comparative study of the Ce- fossa.59 From this evidence, we sug- Carretero61 concluded that the more prano calvaria. They obtained a ma- gest that the face of Homo sapiens completely preserved specimens, trix of Manhattan phenetic distances. may have appeared by a paedomor- which include clavicles, radii, a fe- The unrooted trees generated from phic process in which adults retained mur, vertebrae, and hand and foot this matrix show that the Ceprano the facial developmental rate of juve- bones, display morphological traits specimen occupies an intermediate niles. that resemble modern humans more position between Homo erectus/Homo Another derived trait of the TD6 than they do either Middle Pleistocene ergaster specimens and the African hominins with respect to Homo erec- hominins or the Neanderthals. and European Middle Pleistocene tus/Homo ergaster is the shape of the The calvarium found in 1994 near ones. Consequently, these investiga- squamosal suture, which depicts a the Italian locality of Ceprano has tors conclude that “Ceprano repre- high arch (ATD6-20 specimen). Al- provided relevant information. The sents a unique morphological bridge though there are no tools robust geostratigraphy and biostratigraphy between the clade Homo ergaster/ ARTICLES The Atapuerca Sites 31

del Elefante, also located in the rail- way trench of the Sierra de Atapuerca, and Barranco Leo´n and Fuente Nueva 3, in the Guadix-Baza basin (Andalu- cı´a). The lower levels of Sima del Ele- fante (E8-E12) give a reverse polarity. The micromammal association of these levels is consistent with the Matuyama cron, suggesting an age of about 1,000 kyr for a small sample of flint flakes recovered from the E11 level.70 With regard to the paleomag- netic data and the faunal assemblages recovered from Barranco Leo´n and Fuente Nueva 3, the lithic artifacts (Mode 1) may be older than 1,070 kyr.71 The metrical and morphological differences between the hominins from Dmanisi and TD6 are remark- Figure 3. The angle of inclination of the mylohyoid groove in relation to the alveolar margin at the level of M1 and M2 is compared in different hominid samples. The mylohyoid groove in the ATD6-5 mandible forms a 34° angle and can be traced to the level of M2/M3. No other Homo mandible shows a mylohyoid groove located in such an extreme position. In . . . the appearance of OH13, attributed to Homo habilis, the mylohyoid groove is more vertical (about 60°), and Homo antecessor ends at the distal end of the M3. Similar inclinations are found in African Middle Pleistocene mandibles such as Tighenif II and III, OH22, and BK67. However, in all of them the groove fails appears to be the best to reach M3. In the European hominids, the mylohyoid groove is more posterior and less inclined (x ϭ c. 55°, n ϭ 12). Thus, with regard to this feature, the Gran Dolina specimen is candidate for the clearly different from the African and European Middle Pleistocene mandibles. Three speciation event that, mandibles in the fossil sample resemble ATD6-5: KNM-WT 15000, mandible C from Sangiran, and an Upper Palaeolithic specimen from Arene Candide (Italy). around one million years ago, preceded the origin of later hominin Homo erectus and later Middle Pleis- ios for the phylogenetic position of tocene specimens commonly referred this species? lineages. Given this to Homo heidelbergensis (and/or to framework, several Homo rhodesiensis).” Manzi, Mal- legni, and Ascenzi65 subscribe to the THE ORIGIN AND questions arise. . . notion of attributing the Ceprano cal- PHYLOGENETIC RELATIONSHIPS varium to the species Homo anteces- OF HOMO ANTECESSOR sor, although this adult specimen can- not be directly compared to the Different evolutionary scenarios 66 immature TD6 hominins. can be considered to explain the ori- able, a fact that could weaken this The TD6 hominins represent the gins of the European Early Pleisto- scenario. However, it is necessary to earliest evidence of clear and unques- cene population. One is the possibility bear in mind that these hominins are tionable modern traits in the fossil that TD6 and the Dmanisi hominins one million years apart. This first sce- record. These hominins, together with are phylogenetically related. At the nario would explain the presence of the Ceprano calvarium, are older than Dmanisi site, located in the Republic Mode 1 in all of the European Early the Bodo cranium and more recent of Georgia, the entrance to Europe, and early Middle Pleistocene sites.72 than the Buia and Daka specimens. the earliest evidence of hominins out Moreover, in this evolutionary sce- Consequently, the appearance of of Africa has been recovered, dated nario Homo antecessor would repre- Homo antecessor appears to be the to the Pliocene-Pleistocene bound- sent a speciation event in Eurasia af- best candidate for the speciation event ary.4,66–69 Perhaps this first dispersal ter the first hominin dispersal out of that, around one million years ago, out of Africa, which may have oc- Africa. This species could have disap- preceded the origin of later hominin curred at the end of the Pliocene, also peared or been absorbed by the sub- lineages. Given this framework, sev- reached southwestern Europe, but sequent arrival of an “Acheulean” eral questions arise: Where did this this has yet to be determined. The old- population that originated in Africa. speciation event take place? What is est archeological evidence of the pres- In this case, we should consider that the origin of Homo antecessor? What ence of hominins in Europe comes the expression of “modern” traits in are the possible evolutionary scenar- from three Spanish localities: Sima the skull happened more than once, in 32 Bermu´dez de Castro et al. ARTICLES

both Africa and Europe, and in popu- lations that had been separated for almost one million years. In relation to this first scenario, it is known that before 1,200 kyr a series of dispersals started in Eurasia, mainly involving mammals of Asiatic origin and probably related to cli- matic change.73,74 More than 25 spe- cies of large mammals dispersed from Asia into western and central Europe in the next 500 kyr, many more than in any period of comparable length since the early Miocene. A second scenario postulates a sec- ond major dispersal of hominins out of Africa across the Levant toward southwestern Europe at the end of the Early Pleistocene, around one million years ago or earlier. In this context, it is important to remember that the main dispersals of mammals from Af- rica to Europe during the Pleistocene occurred around 1,200, 900, and 500 to 600 kyr.74–75 In this scenario, Homo antecessor could represent a specia- tion event that occurred either in Af- rica or Eurasia after the second major dispersal. If this event occurred in Af- rica, Homo antecessor would have per- sisted in Africa to originate the evolu- tionary lineage of Homo sapiens. If the species originated in Eurasia, or per- haps in the Near East, Homo anteces- sor must have gone back to the Afri- can continent to give rise to our species. This second scenario is strength- ened by the morphological similari- ties between the TD6 hominins and certain African hominins and homi- nins of Africa origin. Thus, the man- dibular specimen ATD6-5 displays a remarkable position of the mylohyoid groove, comparable only to that found in immature specimens of Homo er- gaster and, very rarely, in adult Homo sapiens (Fig. 3). Furthermore, as stated earlier, the TD6 hominins share three derived traits with modern hu- mans, Neanderthals, and African and European Middle Pleistocene homi- nins. Considering either of the two possibilities that might be expected in Figure 4. In this scheme, we assume that the Dmanisi hominins represent a distinct species, this second scenario, we would still Homo georgicus,102 and that this species shares a common ancestor with Homo ergaster. need to know why this expansion oc- A candidate for this common ancestor is Homo habilis. Although Homo erectus appears as curred with Mode 1 technology when a long-lasting lineage in China and Southeast Asia, the large variability of this species needs Mode 2 was already present in Africa to be revised. Theoretically, the distribution of the species Homo antecessor would include and the Near East. According to Southern Europe, the Near East, and Africa. OAD ϭ Out of Africa dispersal. suggestions made by Stringer and ARTICLES The Atapuerca Sites 33

Pleistocene population, represented by TD6 and Ceprano, and the Euro- pean Middle Pleistocene population. In other words, did Homo antecessor evolve in Europe into the Neanderthal lineage? One of the most striking Neander- thal features is midfacial progna- thism.79,80 In these hominins, the in- fraorbital bone plate is not orientated in the coronal plane, as it is in modern populations, but rather exhibits a coronal-sagital (or parasagittal) orien- tation, conforming to uniplanar sur- face with the lateral nasal wall. This surface lacks a canine fossa and max- illary flexion. The zygomatico-alveolar crest is straight and oblique with its

...anessential question is whether or not there is Figure 5. Partial view of Cranium 5 from Sima de los Huesos (Individual XXI). This specimen an ancestor-descendant exhibits midfacial prognathism. The infraorbital plate and the nasal wall do not form a uniplanar surface as they do in classic Neanderthals, but they meet at a wide angle. The relationship between the zygomaticoalveolar crest is gently curved instead of straight and oblique as in classic Neanderthals. European Early Pleistocene population, represented by TD6 and McKie,52 Rightmire,48 and Tatter- change with other people outside Eu- sall,46 the origin of the European Mid- rope, culminating in the “classic” Ceprano, and the dle Pleistocene population may be re- Neanderthals of the early Upper Pleis- European Middle lated to the dispersal toward Europe tocene. The appropriate name for this Pleistocene population. of an African Middle Pleistocene pop- lineage is Homo neanderthalensis if we ulation that probably resembled the acknowledge that the Neanderthals In other words, did Bodo specimen. In this way, Mode 2 do not represent a cladogenetic event Homo antecessor might have been carried to Europe by in Europe but, instead, are the result these new emigrants,22,65 resulting in of an evolutionary process of morpho- evolve in Europe into the replacement of the autochthonous logical “accretion” of the Neanderthal Neanderthal lineage? populations or, more likely, cross- features.36,45,77,78 For practical rea- breeding between them.76 sons, we can consider two chronospe- If this is correct, then it is necessary cies, Homo heidelbergensis and Homo to assume that another cladogenetic neanderthalensis in this European lin- event took place in Africa at the begin- eage.36 The Middle Pleistocene Afri- root low in the maxilla. Finally, the ning of the Middle Pleistocene, initi- can fossils could be grouped in Homo zygomatic bone is located at the M2 or 45 ating the geographic split between the rhodesiensis (see Stringer ). The Afri- M2–M3 level.80 Midfacial progna- European lineage, which then dis- can lineage followed a different trajec- thism, a derived trait of the Neander- persed out of Africa, and the African tory that culminated in the last specia- thal facial skeleton, was already lineage, which subsequently gave rise tion event, which gave rise to the present in its Middle Pleistocene an- to Homo sapiens. This cladogenetic species Homo sapiens (Fig. 4). cestors. According to Arsuaga and co- event could have been from the Afri- workers,36 Arago 21, Petralona, and can population of the species Homo HOMO ANTECESSOR AND THE Cranium 5 of Sima de los Huesos also antecessor, if we accept that this spe- EUROPEAN MIDDLE show midfacial prognathism (Fig. 5), cies is the common ancestor of the although differences from the classic Neanderthals and modern humans PLEISTOCENE POPULATION Neanderthal pattern are still distin- (Fig. 4). For climatic and geographical In both of the scenarios outlined, an guishable.79 reasons, the European lineage might essential question is whether or not The TD6 Hominid 3 face is categor- have evolved during the Middle Pleis- there is an ancestor-descendant rela- ically modern, bearing no resem- tocene almost without genetic ex- tionship between the European Early blance to the derived face of Neander- 34 Bermu´dez de Castro et al. ARTICLES

and 2 deciduous teeth and the Sima de los Huesos sample, with 467 per- manent and 8 deciduous teeth. The relative size of the second pre- molar (P4) and the molars (M1–M3) is a remarkable feature characterizing the Sima de los Huesos sample. The mean mesiodistal and buccolingual diameters of the crowns are similar to those in modern populations.85 Con- sidering the reduced size of these teeth in other Middle Pleistocene fos- sils such as those from Steinheim, Pontnewydd, and Mauer, as well as some of the Arago specimens, the gen- eral trend toward posterior tooth re- duction (except the first premolar, P3) in the European Middle Pleistocene is clear. This could represent a case of parallelism between the Middle Pleis- tocene populations and the lineage leading to modern populations.85 In contrast, the mesiodistal and bucco- Figure 6. Scatter diagram for the first and second principal components of dental variables: lingual dimensions of the TD6 poste- mesiodistal and buccolingual diameters of the mandibular I2-M2. Homo sapiens: Aborigi- rior teeth are large and comparable to nals from Gran Canaria, Canary Islands and individuals II, XII, and XXIII from the Atapuerca- those of the African and Asian Early Sima de los Huesos sample. (2): Individuals from the Neanderthal sample: Arcy II, Genay, Le and Middle Pleistocene specimens.47 Moustier, Ehringsdorf N, Spy II, Krapina D, Krapina E, Krapina H, Krapina L, and Valdegoba. As shown in Table 1, some of the di- mensions of the Gran Dolina-TD6 posterior teeth are beyond the Sima thals. ATD6-58 does not share any similar to those of modern humans de los Huesos range of variation. This common trait with these hominins ei- and lack the typical Neanderthal is true of the buccolingual dimension ther.59 However, Arsuaga and col- sharp lower margin formed by the lat- of the maxillary C mandibular and leagues59 believe that the Neanderthal eral crest.59 maxillary P3, and maxillary P4 and face could be derived from a face like Metric and shape features of the M1; the mesiodistal and buccolingual that of the TD6 hominin. According to Early Pleistocene mandible specimen dimensions of mandibular P4, M1, these authors, specimens from Sima from TD6 show that ATD6-5 had a and M2; and the mesiodistal dimen- de los Huesos (AT-404) and Steinheim generalized morphology largely sion of maxillary M2. However, it is point to that possibility,59 showing an shared with both African and Euro- important to note that some speci- intermediate morphology between the pean Early and Middle Pleistocene mens from Arago, such as Arago 13, generalized midface79 observed in cer- samples.82 However, distinctive Afri- tain hominins and modern popula- can traits such as corpus robustness TABLE 2. Principal Component tions and the derived midface of Ne- and strong alveolar prominence are Analysis of the Mandibular Dental anderthals. They also point to the fact absent in the Gran Dolina specimen. Variables that the AT-404 and Steinheim speci- At the same time, none of the apomor- Factor 1 Factor 2 mens are clearly derived toward the phic features that characterize Middle MD 0.853 Ϫ0.257 I2 Neanderthal direction. and early Upper Pleistocene Euro- BL 0.805 Ϫ0.424 The internal nasal cavity of pean hominins can be recognized in MD 0.912 Ϫ0.222 C ATD6-69 lacks the three Neanderthal ATD6-5. BL 0.901 Ϫ0.246 apomorphies described by Schwartz Study of the size, proportions, and MD 0.936 Ϫ0.007 P3 Ϫ and Tattersall81: development of an morphology of the TD6 and Sima de BL 0.902 0.239 MD 0.842 0.340 internal nasal margin bearing a well- los Huesos dental samples also pro- P4 BL 0.906 Ϫ0.003 developed and vertically oriented me- vide important data. Due to their MD 0.798 0.460 M1 dial projection, swelling of the poste- highly conserved genetic component, BL 0.728 0.483 rior-lateral wall of the nasal cavity as a teeth are considered a valuable and MD 0.884 0.131 M2 result of a medially expanded maxil- reliable source of characters for phy- BL 0.897 0.199 lary sinus, and lack of an ossified roof logenetic analysis.83,84 The sample for % of variance: 74.9 8.6 over the lacrimal groove. Further- this analysis comprises the TD6 hyp- Cumulative 74.9 83.5 variance: more, nasal crests of ATD6-69 are odigm, composed of 28 permanent ARTICLES The Atapuerca Sites 35

TABLE 3. Comparison of the State of Dental Features in the Gran Dolina-TD6 and Sima de los Huesos Hominins From the Sierra de Atapuerca Dental Traits TD6 SH Shovel-shaped upper incisors Present Present Relative buccolingual dimension Intermediate Broad of the mandibular incisors with regard to the posterior teeth dimensions Relative buccolingual dimension Intermediate Broad of the maxillary incisors with regard to the posterior teeth dimensions Cingulum in mandibular canines Present Absent and premolars Crown shape of the mandibular Strongly asymmetrical Symmetrical or moderately asymmetrical third premolar (P3) Relative buccolingual dimension Broad Broad/narrow of the mandibular P3 with regard to the mesiodistal dimension Talonid of the mandibular P3 Well developed Small or absent Mandibular premolar root 2 roots: MB ϩ DLa 1 Root morphology Mandibular P3/P4 size sequence P3 Ͼ P4 P3 Ͼ P4 for the crown area Mandibular M1/M2 size sequence M1 Ͻ M2 M1 Ͼ M2 for the crown areab Maxillary M1/M2 size sequence for M1 Ͻ M2 M1 Ͼ M2 the crown area Hypoconulid in the mandibular M1 Present and well developed Frequently absent in M2, and less so in M1 and M2b Relative buccolingual dimension Broad Broad of the mandibular M1 with regard to the mesiodistal dimension Taurodontismc Hypotaurodontism Hypo- to hypertaurodontism a The TD6 premolars have two roots; the distolingual root is shorter than the plate-like mesiobuccal root. The dominant buccal component and the shorter and narrower mesial components of the mesiobuccal root have independent root canals. b The Montmaurin mandible also exhibits the M1 Ͼ M2 size sequence. No hypoconulid is present in the M2 of this specimen or in the Arago 5 (M2) and Arago 6 (M2) specimens (personal observation of the originals by first author). c Classification of Shaw (1928).

have posterior teeth that are as large the size of the anterior and posterior show the clear differences between as or even larger than those of TD6. dentitions. Finally, in the Sima de los the TD6 and Sima de los Huesos sam- The anterior teeth (incisors, ca- Huesos hominins and most Neander- ples. The two samples share some nines, and the P3) from Sima de los thals, anterior teeth are clearly larger traits, but these traits do not necessar- Huesos are relatively large in compar- than posterior teeth. Figure 6 and Ta- ily imply a phylogenetic relationship ison to the P4 and molars. The size ble 2 show the results of an analysis of between the TD6 and Sima de los imbalance of I1-P3 versus P4-M3 is an principal components (factors 1 and Huesos populations. For example, important trait that can be used to 2) illustrating this size relationship shovel-shape, a plesiomorphic trait establish affinities and phylogenetic between anterior and posterior denti- for the Homo clade, is present in all relationships among hominins.38,44 As tions. It is important to highlight the Homo species, including some Homo far as the mandibular dentition is con- fact that the size and shape of the sapiens populations. The P3 dominat- cerned, some Homo specimens such dentition of the Mauer specimen (the ing P4 (P3 Ͼ P4) sequence is also as Dmanisi, OH7, or Zhoukoudian holotype of Homo heidelbergensis shared by the African Early and Mid- (mean values of this sample) show Schoetensack, 1908) are very similar dle Pleistocene hominins and the Ne- predominance of the posterior denti- to those of the Neanderthal and Sima anderthals. Finally, the relatively tion over the anterior teeth. Hominid de los Huesos samples.43,44 broad M1, common in TD6 and the 1 from TD6 and other Homo speci- With regard to the dental morphol- Sima de los Huesos hominins, is also mens such as Mauer and Tighenif 3 ogy and interdental indices (Table 3), present in African and Asian Middle show a balanced relationship between we selected a total of 14 features that Pleistocene hominins. 36 Bermu´dez de Castro et al. ARTICLES

Box 1. The Origin of the Sima de los Huesos Hominin Assemblage

Including all the skeletal elements, the Sima de los Huesos hominin sam- ple currently comprises more than 4,000 fossil remains. The minimum number of individuals was assessed through analysis of the maxilla, man- dibles, and isolated teeth. The Sima de los Huesos hypodigm includes more than fifty remains of maxillas and mandibles. Some of these bones are nearly complete; others are less so. Moreover, the current sample in- cludes a total of 479 teeth, 109 in situ and 370 isolated. The MNI evaluation has continued from the first excava- tion seasons.86–88 At this moment, we have determined a MNI of 28. Data obtained from the Sima de los Huesos hominins suggest that the time and pattern of dental develop- ment in the population represented by these hominins were similar to those in modern human popula- tions.89 Thus, we have used modern standards of human dental develop- ment to assess the relative mineral- ization stage of developing teeth in Age-at-death distribution of the 28 individuals identified in the Atapuerca-Sima de los the immature individuals and to esti- Huesos fossil hominin sample. mate their age at death. According to these standards, the third molars adults under the age of 30 years al- When this mortality distribution is (M3) of the hominins appear system- though, as tooth wear increases, its compared with theoretical models atically advanced in their formation as accuracy decreases. Nevertheless, based on demographic parameters compared to second molars (M2), only 3 individuals in the Sima de los estimated for Middle Pleistocene from 1.5 years in individual XVIII to 3.4 Huesos sample are over 30 years old, populations,94 we find that the pecu- years in individual XXV. This observa- so that the lack of precision at this liar Sima de los Huesos distribution tion implies that in these Middle Pleis- stage does not really influence our fits neither an attritional profile nor a tocene populations M3s had their mortality distribution assessment. catastrophic one. The main reason is gingival eruption approximately at the Moreover, we have quantified the that this sample almost completely age of 15 years, whereas the occlusal tooth-wear rate of lower incisors in lacks infants and children, and has an eruption occurred at about the age of immature individuals,92 which allows abnormally high percentage of ado- 16 years.90 us higher reliability and precision up lescents and prime-age adults. Also, In order to estimate the age at to the age of about 35 years. Con- the number of adults over the age of death of the Sima de los Huesos cerning sex, the metrical and mor- 20 years is lower than expected in adults we have applied the tooth- phological variability of the Sima de these models. wear-based method developed by los Huesos mandibles,93 and the ex- The testimonial presence of only Miles91 to the canines, premolars, tremes of variability of dental size88 one individual under the age of 10 and molars. This method takes as ref- suggest that 12 individuals are fe- years in the Sima de los Huesos site erence a group of individuals with es- males and 8 are males, while sex de- could be explained by the action of timated sex and incompletely devel- termination for 8 individuals is incon- taphonomic agents. The fragile and oped dentitions. The degree of wear clusive. delicate remains of infants and chil- on a particular tooth is calculated in a Figure 1 illustrates the age-at- dren are more severely affected by qualitative way and applied to adult death distribution for the Sima de los the action of biostratinomic and fos- specimens. This method has the ad- Huesos hominin sample. The most sildiagenetic agents than are bones vantage of obtaining an internal vari- noteworthy results are the presence from adolescents and adults.95 An- able for the population, in this case of a single individual under the age of drews and Ferna´ ndez-Jalvo96 have the wear rate, which is supposed to 10, represented by a deciduous ca- observed the presence of carnivore be similar for all individuals belonging nine; the high percentage of those marks of a big felid, probably Pan- to that population. (See Bermu´ dez de under the age of 20 years (64.3%); thera leo fossilis, and small scaven- Castro and Nicola´s87 for a discussion and the low percentage of individuals gers, probably Vulpes vulpes on more of this method). In our opinion, this who died after the age of 35 years than 50% of the human remains at method offers reasonable results for (10.7%). Sima de los Huesos. These authors ARTICLES The Atapuerca Sites 37

Box 1. The Origin of the Sima de los Huesos Hominin Assemblage (continued)

suggested that there was an initial anthropic accumulation of human corpses and that later the action of these animals eliminated all vestiges of the individuals younger than 10 years. However, very delicate bones have been recovered at the site, in- cluding small ear bones, as well as eight perfectly preserved deciduous teeth. This suggests extraordinary preservation conditions at the site. Consequently, it seems difficult to ac- cept the idea that almost all evidence of infants, children, and juveniles dis- appeared in the manner suggested. The presence of a high percentage of individuals under the age of 20 years is not expected in a mortality distribution of attritional type, where all individuals who died across a long period for diverse reasons are repre- sented. In a distribution of this kind, we should expect a high number of individuals close to the age of the maximum longevity of that popula- tion.97,98 In all populations, it is nor- mal to find a certain number of ado- lescents who have died of different causes, generally accidental death or first births. However, adolescents and young adults represent the sec- tor of the population that is most re- sistant to illness, which is a major cause of death for infants, children, and elderly members of the population. Frontal surface view of the handaxe found at Sima de los Huesos (Atapuerca Hill). Arsuaga and coworkers14 also con- sidered an anthropic origin for the ac- the first evidence of lithic industry in through flat, invasive extractions cumulations, postulating that they this site.20 The tool is made of good- around both of its surfaces. The were the result of a kind of mortuary quality, reddish to light-brown veined second phase was implemented by practice because of the large mini- quartzite, a raw material not com- shaping the edges of the biface to mum number of individuals. In a later monly found among the thousand achieve a convex distal conforma- work, Bocquet-Appel and Arsuaga99 stone tools recovered so far from the tion and a straight, sharp perimetral discarded the hypothesis that the site Pleistocene sites of Atapuerca. It has edge (Fig. 2). Traceology studies re- was a primitive cemetery, suggesting an amygdaloid shape, and one of its veal that the handaxe does not instead that the mortality distribution sides is flat while the other is convex. show use-wear traces. The finding could be the result of a catastrophe, It seems to have been made by of this unique stone tool together although they did not specify the ori- means of soft hammer percussion af- with the corpses of 28 individuals is gin of the accumulation. ter an initial reduction sequence of difficult to explain as a natural ac- The recent finding of a handaxe of two main phases. The first phase cumulation, that occurred without exceptional characteristics provides was devoted to forming the volume, human intervention.

The Arago hominins display a set of mandible. In this specimen, the crown into two components, mesiobuccal and dental traits that deserves special men- of the P3 is symmetrical and lacks a buccolingual, each with a single canal tion. Most Arago permanent teeth are cingulum and talonid. However, the (observable on CT scans). The crown of large, especially those of the Arago 13 apical fourth part of the root is divided the P4 exhibits a well-developed tal- 38 Bermu´dez de Castro et al. ARTICLES

Box 2. Human Cannibalism in the Aurora Stratum

One of the most interesting results of study of the Aurora stratum of the TD6 level has been the conclusion that the hominin assemblage origi- nated through the practice of canni- balism.100 It thus represents the old- est evidence of cannibalism recorded so far in hominin evolution. The 30-cm deep Aurora stratum contained a large number of human and nonhuman remains, and stone tools. The distribution of the human remains, excavated in 1994 and 1995, seems to be random in the 7 m2 area. There is not a clear pattern in the distribution of the different human skeletal parts, which are mixed with the faunal remains and stone tools. Furthermore, a random arrangement characterizes the distribution of the human and nonhuman fossil remains. Most of these remains show human- induced damage. Tool-induced sur- face modifications in the sample in- clude frequent cutmarks; scraping marks resulting from the removal of periosteum and muscle by scraping the bone surface; and percussion marks, which indicate the use of a stone hammer to smash the bones (Fig. 1). Adhered bone flakes are also frequent in the human and nonhuman remains. Such flakes are produced by striking bones with artifacts. Peeling is especially frequent in the remains of humans and small animals (roe deer, wild boars, and fallow deer). Peeling is defined as a roughened surface with parallel grooves or fi- brous texture produced by bending the fresh bones between the hands. All these butchering techniques were aimed at meat and marrow ex- traction. The presence of human re- mains in the assemblage suggests cannibalism for nutritional purposes. The species diversity recorded in the Aurora stratum is the richest found at a: Scanning electron microscope image of the immature clavicle ATD6-55 exhibiting any level in the Sierra de Atapuerca parallel cutmarks and a transversal fracture made when the bone was still fresh. b: sites. The temperate climate inferred Fragment of human temporal ATD6-16 showing numerous more-or-less parallel cut- from the fossil record (pollen and marks affecting the area where the sternocleidomastoid muscle is attached. c: The mammal community) for TD6, as well face ATD6-69 shows an impact produced with a stone tool near the infraorbital border as the abundance of hunting available (white arrow), as well as some slicing and sawing marks near the zigomaticoalveolar crest (black arrow). to hominins, make it improbable that humans ate other humans as a sur- ement representation in the Aurora marrow, suggests transport selection vival strategy. Rather, it seems that stratum suggest that the small ani- by hominins. Pending future excava- the TD6 hominins consumed other mals, including humans, were trans- tions over the whole TD6 level, the members of their species as part of ported complete into the cave.101 In Aurora stratum can be interpreted as their regular diet (dietary or gastro- contrast, the anatomical representa- a consumption site, whether it was a nomic cannibalism). tion of large animals, which is biased preferential central place or an occa- On the other hand, the skeletal-el- in favor of elements rich in fat and sional refuge. ARTICLES The Atapuerca Sites 39 onid, while the apical third of the root is ified the evolutionary landscape of the entiated during the Middle and early also divided in two components, mesio- genus Homo around one million years Upper Pleistocene. buccal and distolingual, as in the TD6 ago.7,48 This speciation event implied At the point of origin of these two sample. Also, the mesiobuccal compo- the origin of the hominin population lineages, we should, according to pro- nent has two-rooted canals. Hence, the that derived toward the “sapiens” pat- tagonists of the previously mentioned root morphology of this tooth is similar tern but retained plesiomorphic traits speciation event, expect an ancestral to that of the corresponding tooth of of its ancestral species Homo ergaster species from the Early Pleistocene Hominid 1 from TD6. On the other (or Homo erectus, if we accept the that fulfills the requirements of com- hand, Arago 13 and Arago 21 show a scheme of those who consider Homo bining plesiomorphic Homo ergaster/ clear M1 Ͻ M2 size sequence; the M2 ergaster to be the African form of a Homo erectus traits with derived traits and M3 of Arago 13 are hypotaurodont polytypic species distributed through- toward the “modern” pattern. Surpris- and mesotaurodont, respectively. Arago out Africa and Eurasia). The “sapiens” ingly, the first evidence of such mor- 13 shows a combination of the Gran pattern is characterized by a substan- phology was discovered outside of Af- Dolina and Sima de los Huesos dental tial increase in the cranial capacity rica. The Gran Dolina site in the traits (see Table 1). with subsequent modifications of the Sierra de Atapuerca and the Ceprano Since the 1997 publication regard- cranial vault and the appearance of site103 have provided fossils of a new ing the species Homo antecessor and certain modern traits in the facial species, Homo antecessor, which may its possible phylogenetic position,47 skeleton. According to anagenetic and represent the common ancestor of Ne- there have been new findings in Africa gradualist vision of human evolution, anderthals and modern populations. and Eurasia. Moreover, the question the presence of this hominin popula- Different scenarios have been pro- of the persistence of Mode 1 technol- tion was established in the Middle posed to complete the puzzle of the ogy in Eurasia or, if preferred, the late Pleistocene of Africa, Asia, and Eu- available fossil record. However, there arrival of Mode 2 to this continent, rope. In the last decade of the twenti- are still missing pieces waiting to be has been a source of debate in the eth century, along with the move to- uncovered. These pieces undoubtedly scientific community. Given this con- ward a cladogenetic understanding of would allow a more precise approach text, we find it appropriate to review human evolution, these hominins to the evolutionary history of the ge- the Atapuerca evidence. The study of have been grouped as Homo heidelber- nus Homo and the origin of our spe- the skull, mandibles, and dental re- gensis. cies. mains of TD6 has not revealed any This model is not totally satisfac- Neanderthal apomorphic trait. More- tory, especially to those who see con- ACKNOWLEDGMENTS over, the size and shape differences sistent and clear differences among We thank Professor Fleagle for his between the TD6 and Sima de los the specimens assigned to Homo hei- kind invitation to contribute a paper Huesos specimens, as well as between delbergensis, differences which seem TD6 and other specimens from the on the Sierra de Atapuerca sites and sufficient for distinguishing two or European Middle Pleistocene, are re- its contribution to the knowledge of more lineages within the group.36 The markable. Hence, the hypothesis of an human evolution. We are also grateful excavations in the Pleistocene sites of ancestral-descendant sequence of to the referees who, through their Sierra de Atapuerca have yielded sig- populations without rupture of the re- valuable comments, have helped us nificant data to contribute to this de- productive continuity between the improve the paper. This research was bate. First, the study of the extraordi- late early Pleistocene and the Middle supported by funding from the Direc- nary human fossil assemblage Pleistocene in Europe does not seem cio´n General de Investigacio´n of the recovered in the Sima de los Huesos clear. However, some of the Arago Spanish M.E.C., Project No BXX2000- site has undoubtedly shown that Eu- specimens might represent cross- 1258C03-01, the CSIC “Unidades Aso- rope was the home of the local evolu- breeding between the two popula- ciadas” Program, Fundacio´n Atapu- tion of a lineage that subsequently tions. erca, Fundacio´n Duques de Soria, and gave rise to the so-called “classic” Ne- Fundacio´n Caja Madrid. Field-work anderthals. This lineage started at CONCLUSIONS support came from Consejerı´a de Cul- least half a million years ago, proba- tura y Turismo of the Junta de Castilla The scattered nature of the fossil bly originating in a hominin dispersal y Leo´n and Fundacio´n Atapuerca. record has long undermined studies out of Africa that brought the Mode 2 of human evolution in the period be- to Europe. The most appropriate tween 1,200 and 500 kyr. 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