The Costal Skeleton of Homo Antecessor: Preliminary Results

Journal of Human Evolution 59 (2010) 620e640

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Journal of Human Evolution

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The costal skeleton of Homo antecessor: preliminary results

Asier Gómez-Olivencia a,b,*, José Miguel Carretero a,c, Carlos Lorenzo a,d, Juan Luis Arsuaga a,e, José María Bermúdez de Castro f, Eudald Carbonell d,g a Centro UCM-ISCIII de Investigación sobre Evolución y Comportamiento Humanos, c/Sinesio Delgado, 4 (Pabellón 14), 28029 Madrid, Spain b Leverhulme Centre for Human Evolutionary Studies, Department of Biological Anthropology, University of Cambridge, Fitzwilliam Street, CB2 1QH Cambridge, UK c Laboratorio de Evolución Humana, Dpto, de Ciencias Históricas y Geografía, Universidad de Burgos, Ediﬁcio IþDþi, Plaza Misael de Bañuelos s/n, 09001 Burgos, Spain d IPHES, Institut Catalá de Paleoecología Humana i Evolució Social, Universitat Rovira i Virgili, Pça Imperial Tarraco,1, 43005 Tarragona, Spain e Departamento de Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain f Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo Sierra de Atapuerca s/n, 09002 Burgos, Spain g Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China article info abstract

Article history: The Lower Pleistocene TD6 level at the Gran Dolina site in the Sierra de Atapuerca (Burgos, Spain) has Received 23 February 2010 yielded nine ribs that represent a minimum of three individuals of the species, Homo antecessor.We Accepted 14 July 2010 present a detailed morphological and metric study of these costal elements, including the siding and anatomical position of all of the rib remains. The adult or nearly adult ribs are also metrically compared Keywords: with other fossil hominins and with modern comparative samples. The costal elements recovered to date Ribs from the TD6 level at Gran Dolina can neither conﬁrm nor reject the hypothesis that H. antecessor had TD6 a large thorax, similar to that of Neandertals. However, the fragmentary evidence of the H. antecessor Lower Pleistocene Gran Dolina-TD6 thoracic skeleton is not inconsistent with this suggestion based on other skeletal elements, such as Thorax clavicles. Resumen: En el nivel TD6 del Pleistoceno inferior del yacimiento de Gran Dolina, en la Sierra de Atapuerca (Burgos, España) se han recuperado nueve costillas que pertenecen a un mínimo de tres individuos de la especie Homo antecessor. Presentamos un detallado estudio métrico y morfológico incluyendo el lado y la determinación anatómica. Las costillas pertenecientes a individuos adultos o casi adultos también son comparadas métricamente a muestras modernas de comparación y otros homininos fósiles. Basándonos en el registro de costillas de Homo antecessor recuperado hasta el momento no podemos probar ni refutar la hipótesis de que esta especie presentaba un tórax grande similar al de los Neandertales. Sin embargo, el registro de costillas no es inconsistente con la hipótesis de un tórax grande como sugiere la gran longitud de sus clavículas. Ó 2010 Elsevier Ltd. All rights reserved.

Introduction together with abundant lithics and faunal remains. In the 1995 field season, this site yielded an additional 60 new human fossils as well The recent discovery of a human mandible dated to c. 1.1e1.2 Ma as more lithic and faunal remains. This increase in the hypodigm at the Sima del Elefante site (Sierra de Atapuerca, Burgos, Spain) has revealed a unique combination of morphological traits that led cemented the new paradigm of a long human occupation of Europe Bermúdez de Castro et al. (1997) to propose a new species for this (Carbonell et al., 2008). Within this paradigm shift, another site human fossil assemblage, Homo antecessor. from the Sierra de Atapuerca, Gran Dolina, has played a key role and The TD6 level is 2e2.5 m thick and is composed of clastic flows the recovery of human remains from the TD6 level has been that coarsens upwards with very little clay matrix (Parés and Pérez- instrumental in this process. The first human remains from Gran González, 1999). The human remains from TD6 were first thought Dolina-TD6 level were recovered in 1994, in a stratigraphic test pit to derive from a single horizon within the TD6 level (the “Aurora of about 7 m2 (Carbonell et al., 1995; for a complete and detailed Stratum”). However, new analysis and excavations have revealed history of the findings see Carbonell et al., 1999a; Bermúdez de that they derive from two (Canals et al., 2003) or even three Castro et al., 2006, 2008). Thirty human fossils were found different horizons within TD6 (Bermúdez de Castro et al., 2008). The human remains, including the ribs (Fig. 1) show diagenetic breakage due to sediment compression, but the most extensive * Corresponding author. modifications are those produced by other humans in the form of E-mail address: [email protected] (A. Gómez-Olivencia).

et al. (1997) initially proposed that H. antecessor represents the last common ancestor of Homo neanderthalensis and Homo sapiens (see also Arsuaga et al., 1999a,b). Subsequently, Bischoff et al. (2003) published new radiometric dates for the Sima de los Huesos (SH), a Middle Pleistocene site, which is 560 m from Gran Dolina and where abundant remains of Homo heidelbergensis have been recovered (Arsuaga et al., 1997a). The age range given by the UeTh series dating from an in situ speleothem (SRA-3), which seals the human-fossil bearing deposit of SH, was 400e600 ka.2 The chro- nological closeness between the fossil samples from SH and TD6, both from the Sierra de Atapuerca and the differences in the dentition between them led Bermúdez de Castro et al. (2003) to question the evolutionary continuity between these two hominin groups. They hypothesized the replacement of the human populations from Gran Dolina-TD6 and Ceprano, Italy, at around 500e600 ka ago by populations probably coming from Africa that used Mode 2 Figure 1. ATD6-251 rib in situ during excavation. Note the diagenetic breakages lithic technology (see also Carbonell et al., 1999c). The morphology (arrows). Photo courtesy of Javier Trueba (Madrid Scientific Films). of the upper first molar of H. antecessor is similar to that of H. heidelbergensis and H. neanderthalensis (Gómez-Robles et al., 2007; Gómez-Robles, 2010), suggesting the probability of evolutionary cut marks, percussion pits, etc. The pattern of these modifications is continuity between them. However, the absence of Neandertal similar to that of other faunal remains at the site and indicates that derived traits in the mandible of H. antecessor suggests the opposite these humans were processed for meat by a similar butchering (Carbonell et al., 2005). For these authors, H. antecessor might be process (Fernández-Jalvo et al., 1996, 1999; Díez et al., 1999). more closely related to the Chinese populations of the late Lower and Numerous publications have been devoted to the study of the TD6 early Middle Pleistocene, represented at the sites of Nanjing and human fossil remains. The cranial, mandibular and dental remains Zhoukoudian (Carbonell et al., 2005). have been studied by Arsuaga et al. (1999b, 2001), Bermúdez de At the same time, direct comparison of the dentition and Castro et al. (1999a,b, 2006, 2008), Rosas and Bermúdez de Castro mandibular remains of TD6 with those of Tighennif (Algeria) reveal (1999), Bermúdez de Castro and Sarmiento (2001), Carbonell important differences between these hominins (Bermúdez de et al. (2005). The postcranial remains have been studied by Castro et al., 2007). Martinón-Torres et al. (2007) have recently fi Carretero et al. (1999, 2001) and Lorenzo et al. (1999). de ned a Eurasian dental pattern that differs from African homi- The faunal remains found in the TD6 level encompass large nins, and proposed that Asia may have played a major role in the herbivores (Made, 1999, 2001), carnivores (García and Arsuaga, 1999), hominin colonization of Europe. The debate regarding evolutionary birds (Sánchez-Marco, 1999), micromammals (Cuenca-Bescós et al., continuity between H. antecessor and the Neandertal evolutionary e 1999; Cuenca-Bescós, 2002; López-Antoñanzas and Cuenca-Bescós, lineage (H. heidelbergensis H. neanderthalensis) was still open in 2002), and small amphibians and reptiles (Blain et al., 2009). The the description of the most recently found fossils from Gran Dolina- lithic remains are attributed to the Oldowan tradition (Carbonell et al., TD6 (Bermúdez de Castro et al., 2008; Gómez-Robles, 2010). 1999b) and were used for butchery and wood-working (Márquez et al., More recently, Dennell et al. (2010, submitted for publication) 2001). have proposed that H. antecessor is not the common ancestor of The magnetostratigraphic study of the Gran Dolina sequence H. sapiens and H. neanderthalensis. Rather, the similarities between has located the Matuyama Chron Boundary in level TD7, indicating H. antecessor and Neandertals would derive from a common fi that the TD6 level is older than 780 ka (Parés and Pérez-González, ancestor. More speci cally, these authors propose that there was 1995, 1999). Uranium series and electronic spin resonance (ESR) a central area of dispersals of Eurasia (CADE), located in southwest techniques yielded a date of between 780 and 857 ka (Falguères Asia from which different populations would have entered Europe. et al., 1999, 2001). The paleoenvironmental data from pollen and One of these hominin dispersal events from the CADE to Europe led from quantitative studies of amphibians and squamates (scaled to a speciation event by 1.2 Ma, giving rise to H. antecessor. Subse- reptiles) show that the upper part of the TD6 level was deposited quent dispersal event of H. heidelbergensis, could have replaced during a humid and relatively warm period (García-Antón, 1995; (or may have interbred) with some remnant populations of Blain et al., 2009) that Bermúdez de Castro et al. (2008) relate to H. antecessor. marine isotope stage (MIS) 19 or 21. However, new thermolumi- nescence (TL) and infrared-stimulated-luminescence (IRSL) dating Background and objectives suggest that the oldest human fossils from the TD6 level could be between 900 and 950 ka old and attributed to MIS 25, a relatively Bermúdez de Castro et al. (1997) cite the presence of eight humid and warm interglacial period (Berger et al., 2008). human ribs among the remains recovered in the 1995 field season. The phylogenetic position of Homo antecessor1 continues to be In this inventory, these authors provided the side of all of the costal debated, and conflicting hypotheses have been suggested since their remains but only the positions of the first (ATD6-108) and second discovery. Here, we will briefly summarize the most important (ATD6-79) ribs were anatomically determined. The postcranial publications (in our view) regarding this matter. Bermúdez de Castro remains recovered in the test pit during the 1994 and 1995 seasons were published in two different papers (Carretero et al., 1999; Lorenzo et al., 1999). Carretero et al. (1999) quote the presence of nine labelled fragments that constitute eight ribs; five from the 1 We refer here to the fossils from Gran Dolina-TD6. It should be noted that the human mandible (ATE9-1) from the nearby Sima del Elefante site, dated to approximately 1.1e1.2 Ma, has been provisionally assigned to Homo antecessor too. In addition, some authors have also attributed the calvaria from Ceprano, Italy, to 2 The latest dating of the Sima de los Huesos human fossils yielded an average this species (Manzi et al., 2001). age of 600 ka with a minimum age of 530ka (see Bischoff et al., 2007). 622 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

Table 1 Inventory of the Homo antecessor costal remains.

Label Side Initial Revised Anatomical region Surface modiﬁcationsc Figures anatomical anatomical Head Neck Tubercle Shaft Posterior Shaft Sternal Cut- Percussion Peeling positiona positionb angle end marks pits ATD6-39 L 10 (9?) 10 Cd CC CC X X 9 ATD6-66 L 3e43e4PCC 8 ATD6-79 R 2 2 P C N/A N/A P X 6 and 7 ATD6-85 R 9 (8e10) 9 (8e10) CC P X 13 ATD6-88 R 4e54e5CCCCCP 8 ATD6-89þ206 L 7 (6?) 7 CCC CC 9 ATD6-97 L 10 (11?) e CC C ee e 9 ATD6-108 R 1 1 P C N/A N/A P P 3 and 4 ATD6-251 R 10 (9-11) N/A C C CCX 13

C ¼ complete or largely preserved; P ¼ partially preserved; N/A ¼ not applicable a Based on morphological features. b Based on morphological and metrical features. c According to Fernández-Jalvo et al. (1999). Note that ATD6-97 was not included in their study. d The articular tubercle is present. right side and three from the left side. Again, the anatomical Investigación sobre la Evolución Humana (CENIEH). This includes position was only determined for the first and second ribs. All of the determination of the anatomical position and age at death for each costal remains were illustrated in a figure in cranial view but no of the specimens, calculating the minimum number of individuals metrical study was performed at that time (Carretero et al., 1999). (MNI) represented within the sample, carrying out a comparative The present contribution presents a more complete and detailed metric analysis of the adult or near adult remains and discussing analysis of these costal remains. Work to homogenize the exposed the possible implications of the results. section of the Gran Dolina site has provided the opportunity to excavate approximately 13 m2 of the Aurora Stratum (Bermúdez de Castro et al., 2008). These new excavations have yielded new fossil Materials remains, including a rib (ATD6-97, found in 2004,) which is described here for the first time. This study includes the eight ribs recovered in the 1995 field The specific objectives of this paper are to provide an up-to-date season (illustrated in Carretero et al., 1999) and one rib (ATD6-97) inventory and morphological description of the human costal recovered in the 2004 field season at Gran Dolina-TD6 level (Sierra remains of the TD6 level, housed at the Centro Nacional de de Atapuerca, Burgos, Spain) (Table 1).

Table 2 Comparative specimens and samples.

Specimen/Sample Sex Ribs measured and side Stature (in cm)a References H. ergaster KNM-WT 15000b M 1R and 1L 147 Jellema et al., 1993; Ohman et al., 2002 H. heidelbergensis (Sima de los Huesos) Co1(1L)c M? 1R Gómez-Olivencia, 2009 H. neanderthalensis Amud 1d M 1L 175 Endo and Kimura, 1970 Kebara 2d M 1-10 (R and L) 166 Arensburg, 1991; Gómez-Olivencia et al., 2009b Krapina (n ¼ 5)f ?1R(n ¼ 3), 1L (n ¼ 2) e Radovcic et al., 1988 La Chapelle-aux-Saintsg M 10 (R and L) 162 Boule, 1911e1913 Shanidar 3h M 3R, 4R, 5R, 5L, 6R, 7R, 166 Franciscus and Churchill, 2002 8R, 8L, 9R, 9L, 10R Tabun C1i F 2L, 6R, 6L,7R, 7L, 8R, 154 McCown and Keith, 1939 8L, 9R, 9L, 10L Fossil H. sapiens Ohalo 2d M 1R 173 Hershkovitz et al., 1995 Recent H. sapiens EuroAmerican (n ¼ 26) j M 1-10 (R); 4L 169.9 8.1 EuroAmerican (n ¼ 6)k M 1-10 (R); 4L EuroAmerican (n ¼ 35)j F 1-10 (R); 4L 160.7 6.0

All data collected on original specimens except KNM-WT 15000. a According to Ruff et al. (1997: their supplementary information), except KNM WT-15000. b KNM cast curated by the Max Planck Institute, Leipzig (Germany). c Field label: AT-2748þAT-3546þAT-3549. d Department of Anatomy and Anthropology, Tel Aviv University, Tel Aviv (Israel). f Croatian Natural History Museum, Zagreb (Croatia). g Musée de l’Homme, Paris (France). h Smithsonian Institution-National Museum of Natural History, Washington D.C. (USA). i Natural History Museum, London (United Kingdom). j Cleveland Museum of Natural History (Hamann-Todd Collection), Cleveland (Ohio, USA). k University of Iowa, Iowa City (Iowa, USA). A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 623

Table 3 Measurement deﬁnitions.

Variable Description 0a PrL Preserved length Maximum straight length of the rib fragment. Ribs 1e12. 0b PrExA Preserved external arc Maximum external arc length of the rib fragment. Ribs 1e12. 0c PrExAVT Preserved external arc Maximum external arc length of the rib fragment ventral from the lateral end of the ventral to the tubercle articular surface of the tubercle. Ribs one to nine. 0d PrInA Preserved internal arc Maximum internal arc length of the rib fragment. Ribs 1e12. 1a TVC Tuberculo-ventral Straight line distance between the dorsal-most margin of the articular tubercle to the chorda ventral-most point of the sternal end of the rib. Ribs 1e9. 1b HVC Head-ventral chord Straight line distance between the lateral (dorsal) margin of the articular surface of the head to the ventral-most point of the sternal end of the rib. Ribs 10e12. 2a TVA Tuberculo-ventral arca Arc length measured along the greater curvature of the rib from the lateral end of the articular surface of the tubercle to the sternal end of the rib. Ribs 1e9. 2b HVA Head-ventral arca Arc length measured along the greater curvature of the rib from the lateral (dorsal) margin of the articular surface of the head to the sternal end of the rib. Ribs 10e12. 3 TVS Tuberculo-ventral Perpendicular distance from TVC to the lateral-most extent of the shaft of the rib. Ribs 2e9. subtense 4a HCCD Head cranio-caudal Maximum diameter in approximate cranio-caudal direction of the articular surface diameter of the head. Ribs 1e12. 5a TNL Total neck length Straight line distance between the lateral (sternal)-most margin of the articular tubercle to the medial(vertebral)-most point of the head. Ribs 1e9. 6 NMnCCD Neck minimum cranio- Minimum reading of the cranio-caudal dimension of the neck, measured perpendicular caudal diameter to the long axis of the neck. Ribs 1e10. 7 NTh Neck thickness Measured at the mid part of the neck. Minimum diameter from internal to external surface of the rib. Ribs 1e10. 8 ATH Articular tubercle heightb Maximum cranio-caudal diameter of the articular tubercle with the rib positioned in approximate anatomical position. Ribs 1e9. 9 ATW Articular tubercle widthb Maximum width of the articular tubercle with the rib positioned in approximate anatomical position. Ribs 1e9. 10b TID2 Tubercle-iliocostal line Straight line distance from the medial (vertebral) end of the articular tubercle to the distance 2c furthest extent of the iliocostal line. Ribs 3e9. 11b PAC2 Posterior angle chord 2 Straight line distance from the dorsal end of the articular tubercle to a point on the inferior aspect of the shaft whose ventral linear distance from the iliocostal line is equidistant to the TID2. Ribs 3e9. 12b PAS2 Posterior angle subtense 2 The subtense from the inferior iliocostal point to the chord PAC2. The value for the subtense is derived geometrically from a right triangle whose base is ½ PAC2 and whose hypotenuse is TID2. Ribs 3e9. 13 PA Posterior angle Angle between the TID2 and the line of the same distance used to determine the PAC2 measurement. Ribs 3e9. 14 THD Tubercle horizontal Maximum diameter from the internal surface of the rib to the further extent of the diameter articular tubercle. Ribs 1 to 2. 15 DSMxD Shaft maximum diameter Measured between the tubercle and the posterior angle of the rib. Ribs 3e12. at dorsal end 16 DSMnD Shaft minimum diameter Measured between the tubercle and the posterior angle of the rib. Ribs 3e12. at dorsal end 17 SMxD Shaft maximum diameter Measured at the posterior angle of the ribs. In all cases, the calipers are oriented for at posterior angleb maximum reading, which is approximately cranio-caudal (for rib 12, the measurement is taken at the farthest extent of the Mm. erector spinae line). Ribs 3e12. 18 SMnD Shaft minimum diameter Measured at the posterior angle of the ribs. In all cases, the calipers are oriented for at posterior angleb minimum reading, which is approximately from the internal surface to the external surface of the rib (for rib 12, the measurement is taken at the farthest extent of the Mm. erector spinae line). Ribs 3e12. 19 MMxD Mid-shaft maximum Measured at the mid-shaft, maximum diameter (from internal to external surface in diameterb ribs 1e2 and approximately cranio-caudal direction in ribs 3e10, following the maximum dimension of the shaft). In rib 1, it is measured at the groove for the subclavian artery. In rib 2, it is measured at the insertion point of the M. scalenus. In rib 3, it is measured in the cranio-caudal narrowing approx. at mid-shaft. Ribs 1e10. 20 MMnD Mid-shaft minimum Measured at the mid-shaft, minimum diameter (approx. cranio-caudal in ribs 1 to 2 and diameterb from internal to external surface of the rib in ribs 3e12). In rib 1, is measured at the groove for the subclavian artery. In rib 2, is measured at the insertion point of the M. scalenus. In rib 3, it is measured in the cranio-caudal narrowing approximately at mid-shaft. Ribs 1e10. 23 SEMxD Sternal end maximum Measured at the sternal end. Maximum diameter. In ribs 1 to 2, is diameterd approximately horizontal. Ribs 1e12. 24 SEMnD Sternal end minimum Measured at the sternal end. Minimum diameter. In ribs 1 to 2, is approximately diameterd vertical. Ribs 1e12.

Numbering of the variables follows Gómez-Olivencia (2009). TNL, NMnCCD and TID2 variables are equivalent to HAFL, SCTCH and AFTAL variables from Owers and Pastor (2005). Our TID2 variable is similar to TID from Franciscus and Churchill (2002) except that TID2 is measured from the dorsal end of the articular tubercle. a McCown and Keith (1939). b Franciscus and Churchill (2002). c Gómez-Olivencia et al. (2009b). d Arensburg (1991). 624 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

mid-thoracic ribs (ribs 3e9) is more difficult. Franciscus and Churchill (2002) have provided a complete set of criteria to sequence mid-thoracic ribs based on both previous work (Dudar, 1993; Jellema et al., 1993; Mann, 1993), as well as on their own observations. Quantitative methods for rib seriation have also been proposed and tested (Hoppa and Saunders, 1998; Owers and Pastor, 2005). In addition, we have taken into consideration the fact that Neandertals show a different pattern in some of the morphological features (e.g., the distance between the tubercle and the iliocostalis line) used to sequence the ribs in modern humans and that they show a significant difference in thorax size and shape from H. sapiens (see Franciscus and Churchill, 2002; Gómez-Olivencia et al., 2009b). Several of the TD6 ribs are fragmentary and represent different individuals with distinct ages at death. We have used the above- mentioned criteria, as well as complete rib sets from the osteo- logical collections housed at the Laboratorio de Evolución Humana (University of Burgos, Spain) and high quality casts of the costal remains of the male Neandertal individual, Kebara 2, from the Musée de l’Homme (Musée National de Histoire Naturelle, Paris). Based on these criteria and the comparative material, we have determined a range of possible anatomical positions for each of the ribs. The metrical study was also used to refine the previously determined anatomical determination (see below).

Age at death determination Figure 2. Some of the dimensions used in the osteometric analysis, as defined in Table 3: (a) caudal view of a forth rib, (b) cranial views of a forth rib, (c) second rib, and (d) Ribs ossify from a primary center of ossification and there may fi rst rib. be three secondary centers of ossification: the head, the tubercle and the nonarticular tubercle. The presence of an articular tubercle For comparative purposes, we have chosen a EuroAmerican depends on the articulation of the ribs with the transverse sample (Hamann-Todd collection), representing a population that processes of the vertebra and therefore, lower ribs lack this tubercle inhabited similar latitudes to those of the Sierra de Atapuerca, and (Scheuer and Black, 2000). that had a stature similar to that estimated for H. antecessor (between We have quantified the maturation stage of the TD6 ribs using 170.9 and 174.5 cm, depending on the bone used to perform the the scoring system developed by Ríos and Cardoso (2009). The estimation; see Carretero et al., 1999; Lorenzo et al., 1999). epiphyses are scored following a three-stage scale: (1) no union; (2) The comparative fossil human sample represents three different partial union; (3) completed union. From these scorings, it is species of Homo. We have studied the original specimens of Ohalo 2 possible to provide an age range (see Ríos and Cardoso, 2009: their (Upper Paleolithic H. sapiens), the Neandertal specimens of Amud 1, tables 6e8), taking into consideration three factors. First, there are La Chapelle-aux-Saints, Kebara 2, Krapina, Shanidar 3, Tabun C1 and significant sex differences in rib maturation: females generally a cast of KNM-WT 15000 (Homo ergaster) (See Table 2 for details). show advanced union of all three epiphyses when compared with males (Ríos and Cardoso, 2009). Second, since the TD6 hominins Methods had a shorter period of dental growth (Ramírez Rozzi and Bermúdez de Castro, 2004) and by inference, somatic develop- Determination of side and anatomical position ment (Smith, 1991), we could be slightly overestimating the ages at death (see Dean and Smith (2009) for age disjunction between Siding of ribs as well as sequencing of “atypical” ribs (ribs 1, 2, dental and skeletal ages for KNM-WT 15000). Third, if we assume 10e12) is straightforward. However, the sequencing of “typical” that these rib remains are derived from the ten individuals

Table 4 Epiphyseal scoring and age at death assessment of the TD6 ribs.

Label Side Revised Epiphyseal scoringa Age-at-death anatomical Head Articular tubercle Nonarticular tubercle position epiphysis epiphysis epiphysis ATD6-39 L 10 e 3 X Adolescenteyoung adult ATD6-66 L 3e4 e 3 3? Young adult ATD6-79 R 2 e 3 3 Adolescenteyoung adult ATD6-85 R 9 (8e10) ee e Adolescenteyoung adult? ATD6-88 R 4e5 3 3 3 Young adult ATD6-89þ206 L 7 e 3 3 Adolescenteyoung adult ATD6-97 L e X X Subadult ATD6-108 R 1 e 3 3 Adolescenteyoung adult ATD6-251 R ee e Subadult

A “e” indicates that it has not been possible to score that anatomical part because it has not been preserved. An “X” indicates that that rib does not possess the mentioned feature. a Based on Ríos and Cardoso (2009).1¼ no union; 2 ¼ partial union; 3 ¼ completed union. A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 625

Figure 4. Lateral view of the ﬁrst ribs: (a) ATD6-108, (b) Kebara 2 (cast), and (c) a modern male. The arrow indicates the great development of the M. serratus anterior in the ﬁrst rib of Homo antecessor. Scale bar ¼ 5 cm.

still scarce. At this moment, it is not possible to study the costal remains relative to other skeletal parts as has been done with other fossil specimens (i.e., Shanidar 3, Kebara 2, see Franciscus and Churchill, 2002; Gómez-Olivencia et al., 2009b). A longer term goal would be the possibility of assigning these ribs to the dental individuals proposed by Bermúdez de Castro et al. (2006, 2008).

Results Figure 3. ATD6-108 (1R) in cranial (a) and caudal view (b). Scale bar ¼ 5 cm. TD6 costal remains e minimum number of individuals (MNI) represented by the dental remains in TD6 level, we would have a maximum age at death for the costal elements of 18 years There are ten labelled fragments that represent nine ribs (Hominid 4) or “young adult” (Hominid 10) (Bermúdez de Castro attributed to H. antecessor (see below and Table 1). In Table 1,we et al., 2006, 2008). However, some of the ribs (ATD6-85, ATD6-97 include two columns for the anatomical determination of the ribs. and ATD6-251) do not preserve the anatomical regions necessary to The first column shows the results of the morphological study. The evaluate the fusion of the head, articular and nonarticular tubercles. second column shows the conjoined results of the morphological In these cases, we provide rough age at death estimates based on and the metrical studies. In this table, we have included the surface surface porosity and muscular scar rugosity (see below). modifications recorded by Fernández-Jalvo et al. (1999). The results of the age at death study are summarized in Table 4 and discussed Osteometrics and statistical analysis in the description of each of the ribs (see below). All the ribs are represented in cranial and caudal views in the figures. Metric analysis of the H. antecessor ribs allows us to corroborate Based on size and age at death compatibilities, ATD6-66 and and refine the anatomical positions made previously based on ATD6-88 likely belong to the same individual. At the same time, morphological considerations and compare the metric dimensions based on size, age at death and coherent degree of development of in the TD6 specimens with other fossil and recent humans. We used the insertion for the serrati muscles, ATD6-108 (1R) and ATD6-79 standard anthropometric techniques and instruments to take all (2R) likely belong to the same individual. measurements (Table 3; Fig. 2) (see also Franciscus and Churchill, Regarding the MNI represented in the TD6 sample, there are 2002: their Fig. 3; Owers and Pastor, 2005: their Fig. 1). three ribs that are likely tenth ribs: ATD6-39 (adolescenteyoung Univariate comparative analysis was performed on all of the adult), ATD6-97 (younger immature) and ATD6-251 (older imma- variables measured using z-scores. Z-score values beyond 1.96 tureeadolescent). ATD6-39 and ATD6-97 are both from the left side and 2.576 SD from the mean would be significant at p < 0.05 and but show different age at death, thus representing different indi- p < 0.01 respectively (Sokal and Rohlf, 1981). We have also used viduals. ATD6-251 is from the right side and represents an imma- bivariate plots to better characterize the most complete ribs. The ture individual. However, it would be an older individual than curvature of the rib has been studied by analyzing the relationships ATD6-97 and thus likely represents a third individual (Table 4). The between the arc variables (TVA and HVA) and the chord variables remaining ribs could represent the same individual as ATD6-39, so (TVC and HVC), and the relationship between the tuberculo-ventral they do not represent additional individuals. Based on this analysis, chord (TVC) and the tuberculo-ventral subtense (TVS) (see Table 3 a minimum of three individuals (MNI ¼ 3) are represented among for measurement definitions). High values of the arc variables the TD6 costal remains. relative to chord variables indicate curved ribs. High values of tuberculo-ventral subtense (TVS) relative to tuberculo-ventral ATD6-108 (right first rib) (Fig. 3) chord (TVC) would also indicate curved ribs. Anatomical position was assessed by analyzing the relationship between the tubercle- ATD6-108 is a first rib from the right side that preserves iliocostal line distance 2 (TID2) and tuberculo-ventral arc (TVA). approximately half of the neck (11.4 mm), the tubercle and the shaft We are aware of the limitations of the metrical study performed of the rib including the sternal end (Fig. 3). However, the shaft of on these isolated ribs. The postcranial remains of H. antecessor are the rib has lost part of its internal surface, approximately from the 626 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

Figure 5. Curvature of the ﬁrst rib ATD6-108: tuberculo-ventral chord (TVC) (x) vs. tuberculo-ventral arc (TVA) (y). Individuals closer to the straight line (y ¼ x) would have less curved ﬁrst ribs. Dashed lines represent similar curvatures, i.e., ribs between the same two dashed lines have similar curvatures. The modern human comparative samples from the right side are represented by 95% equiprobability ellipses and show a high degree of overlap. Note that ATD6-108 is larger than the Neandertal male of Kebara 2. Regarding the curvature, ATD6-108 shows a curvature similar to modern samples and to Co1(1L) from Sima de los Huesos but is more curved than Kebara 2.

internal part of the articular tubercle to the scalenus tubercle. The is similar to that of the H. heidelbergensis first rib from the Sima de groove for the subclavian artery and the brachial plexus is not los Huesos (Co1(1L)), but higher than the male Neandertal of present, but the dorsal-most half of the sternal end is preserved. Kebara 2 and within the lower limits of the modern human This fossil was recovered in five fragments, four of which articulate comparative samples (see Fig. 5). well with one another. The fifth fragment represents the neck and half of the articular tubercle. A slight separation is visible in the ATD6-79 (right second rib) (Fig. 6) cranial aspect, but this fragment refits perfectly with the rest of the rib on its caudal aspect. The three fragments that correspond to ATD6-79 is a second rib from the right side that preserves the ventral half of the rib are somehow cracked into minor pieces. approximately half of the length of the neck (9.8 mm), the tubercle While ATD6-108 does not preserve the head, the articular and most of the shaft (Fig. 4). This rib consists of one large fragment tubercle is completely fused and shows a slight osteophytic rim on that preserves the neck, the tubercle and a large part of the shaft, its caudal border (maximum development of 0.5 mm). Following including the very well-developed attachment for the M. serratus Ríos and Cardoso (2009), this gives us a minimum age of 14 years at anterior and 12 smaller fragments that represent a portion of the the time of death, indicating that this specimen represents an shaft that displays post mortem crushing in the cranio-caudal adolescent or young adult. In its overall dimensions, this rib is direction. larger than both Kebara 2 and the mean values of our modern adult This rib does not preserve the head. However the articular and comparative sample (Table 6). nonarticular tubercles are completely fused. Following Ríos and Ventral to the articular tubercle and parallel to the lateral border Cardoso (2009), this suggests a minimum age of 12 years at the of the shaft, ATD6-108 shows a very well-developed ridge with time of death. Based on size, age at death and coherent degree of a rough surface that represents the insertion point of the M. serratus development of the insertion for the serrati muscles, ATD6-108 (1R) anterior muscle. The dimensions of this ridge are ca. 31 mm in and ATD6-79 (2R) are likely to belong to the same individual. This length, a mediolateral width of 5.8 mm and a maximum cranio- association would rise the minimum age at death of ATD6-79 to 14 caudal thickness of 7.6 mm. The considerable development of this years, suggesting that this rib belonged to an adolescent or young ridge is related to a great development of M. serratus anterior. The adult. The overall dimensions of this rib are similar in size to the first rib of KNM-WT 15000 shows a slight roughness in the same mean values of our modern adult comparative samples. place, but neither KNM-WT 15000 nor Kebara 2 show this ridge We have estimated the tuberculo-ventral chord (TVC) of this (see Fig. 4). Finally, the scalenus tubercle, the insertion point to the specimen as longer than 130 mm, through direct comparison with M. scalenus anterior muscle, is present in ATD6-108 but is not as the R2 of the Kebara 2 Neandertal individual (Table 5, Fig. 7). This protruding as in the Kebara 2 Neandertal. minimum value is similar to the modern male comparative sample Metrically, ATD6-108 displays a significantly smaller minimum and one standard deviation above our modern female comparative diameter of the sternal end (SEMnD) compared with the modern sample (Table 7). Metrically, ATD6-79 stands out for its significantly male comparative sample (Tables 5 and 6). The curvature of this rib large tubercle horizontal diameter (THD) and mid-shaft maximum A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 627

Table 5 Raw dimensions (mm) of the Gran Dolina-TD6 ribs.a

Variable ATD6-108 ATD6-79 ATD6-88 ATD6-66 ATD6-89þ206 ATD6-85 ATD6-39 ATD6-97 ATD6-251

1R 2R 4e5R 3e4L 7L 9 (8e10)R 10L 10 (11?)L 10R 0a Preserved length (PrL) 123.5 78.1 48.2 189.0 156.0 171.0 0b Preserved external arc (PrExA) 182.0 85.0 53.0 182.0 182.0 225.0 0c Preserved external arc ventral to 162.0 55.0 49.0 182.0 e the tubercle (PrExAVT) 0d Preserved internal arc (PrInA) 147.0 88.0 34.0 215.0 167.0 209.0 1a Tuberculo-ventral chord (TVC) (90.0) (>130.0) 224.0 1b Head-ventral chord (HVC) e eeee e (190.0) (155.0e160.0) (172.0e175.0) 2a Tuberculo-ventral arc (TVA) (107.0) 275.0 >245.0 (192.0e198.0) (237.0e240.0) 2b Head-ventral arc (HVA) e eeee e (273.0) 3 Tuberculo-ventral subtense (TVS) 68.0 4a Head cranio-caudal diameter (HCCD) 9.1 5a Total neck length (TNL) 32.7 6 Neck minimum cranio-caudal 4.3 7.1 diameter (NMnCCD) 7 Neck thickness (NTh) 4.1 8 Articular tubercle height (ATH) 7.0 7.8 6.4 7.0 9 Articular tubercle width (ATW) 10.3 8.4 8.6 10b Tubercle-iliocostal line distance 2 (TID2) 35.3 (52.0) 11b Posterior angle chord 2 (PAC2) 95.0 12b Posterior angle subtense 2 (PAS2) (21.2) 13 Posterior angle (PA) (129.4) 14 Tubercle horizontal diameter (THD) 17.9 16.4 eee e ee e 15 Shaft maximum diameter at 6.9 6.8 7.4 9.3 7.1 6.6 dorsal end (DSMxD) 16 Shaft minimum diameter at 8.0 7.7 8.1 8.6 6.3 dorsal end (DSMnD) 17 Shaft maximum diameter at posterior 9.7 9.7 10.7 17.5 16.2 11.1 16.5 angle (SMxD) 18 Shaft minimum diameter at posterior 7.9 7.3 8.5 7.4 8.3 5.7 7.4 angle (SMnD) 19 Mid-shaft maximum diameter (MMxD) 15.4 12.8 11.4 (14.7) 15.3 14.5 20 Mid-shaft minimum diameter (MMnD) 3.3b 8.5b 6.3 (7.0) 7.6 6.7 23 Sternal end maximum diameter (SEMxD) (18.7) 15.4 24 Sternal end minimum diameter (SEMnD) 5.9b 8.3 9.5

a Values in parentheses are estimated. b Measured in cranio-caudal direction. diameter (MMxD). In both of these dimensions, ATD6-79 is a more cranial rib than ATD6-88. ATD6-88 is a third, forth or fifth significantly larger than our modern female sample, while rib based on the length and narrow aspect of the neck and the compared with males only the THD is significantly different. The small distance between the tubercle and the iliocostal line. large dimension of MMxD is related to the well-developed inser- However, the vertical orientation of the surface of the shaft tion for the M. serratus anterior muscle, which rotates the scapula between the tubercle and the posterior angle points towards this for abduction and flexion of the arm and protracts the scapula rib being a forth or fifth element (see below). Thus ATD6-66 likely (Stone and Stone, 1999). Second ribs from the Sima de los Huesos represents a left third or forth rib and ATD6-88 likely represents and the Neandertal individual of Tabun C1 show a similar pattern, a right forth or fifth rib. while Kebara 2 shows a cranio-caudally low and mediolaterally In ATD6-88, the articular and nonarticular tubercles are completely wide shaft (Gómez-Olivencia et al., 2009b). fused. In addition, the epiphysis of its head is fused, although the epiphysis does not cover the whole metaphyseal surface and the ATD6-66 (left third or forth rib) and ATD6-88 (right forth or fifth rib) metaphyseal line is still present. This suggests a minimum age of 18 (Fig. 8) years at the time of death (Ríos and Cardoso, 2009). However, the presence of a metaphyseal line is not uncommon even in middle-aged Based on size and age at death compatibilities, it is likely that adult modern human individuals (Ríos and Cardoso, 2009). Both ATD6-66 and ATD6-88 belonged to the same individual. ATD6-66 articular and nonarticular tubercles of ATD6-66 are fused, and the age partially preserves both articular and nonarticular tubercles as well at death of this specimen is consistent with that of ATD6-88. Thus, as the posterior angle, while ATD6-88 preserves the head, neck, these two specimens represent a young adult individual. both articular and nonarticular tubercles, the posterior angle and The metric dimensions of ATD6-88 and ATD6-66 are provided approximately 25 mm of the shaft (Fig. 8). This latter specimen in Tables 5 and 8. The z-score analysis of these individuals has consists of two fragments that rejoin at the posterior angle. It has been conducted together due to their similar anatomical position lost a slight bone chip (2.3 4.3 mm) on the caudal aspect of the and the fact that they likely belonged to the same individual. The fracture line. In addition, slight exposure (4.9 4.4 mm) of the tuberculo-iliocostalis distance 2 (TID2) in ATD6-88 is above the trabecular bone is visible in the cranial aspect of the union between range of the third ribs of our modern male comparative sample the head and the neck. and larger than the third rib of Kebara 2, which supports the ATD6-66 is from the left side and ATD6-88 is from the right diagnosis of this specimen as a forth or fifth rib. These ribs are side. While they are very similar, ATD6-88 has a longer posterior notable for showing a dorsal end of the shaft that is weakly angle and a slightly larger space between the posterior angle and developed in the cranio-caudal direction and well-developed the tubercle (larger TID2 value). This suggests that ATD6-66 is mediolaterally (Tables 9 and 10). 628 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 3.4 15.6 1L 15.4 1L 4.0 15.2 13.2 1R 4.3 0.01. 13.8 (16.5) 1R < p cant at fi

Figure 6. ATD6-79 (2R) in cranial (a) and caudal (b) views. Scale bar ¼ 5 cm. are signi ** þ

4.7 ATD6-89 206 (left seventh rib) (Fig. 9)

ATD6-89þ206 is from the left side, nearly complete and lacks the head and neck (Fig. 9). It is comprised of six fragments that reﬁt 19.8 19.4 17.1 99.0 (96.0) 85.7 82.7 (20.7) 20.5 14.0 well together, although some bone chips have been lost in some of the fracture lines. The general aspect and the degree of torsion þ 8.9 8.4 9.3 4.2 3.3 3.5 3.5 of the shaft and sternal end suggest that ATD6-89 206 is a rib from 19.0

> the cranial part of the rib cage (third to a seventh rib). The distance between the tubercle and the iliocostal line reduces the possibili- 0.05. Values in bold letters and

< ties to a sixth or seventh rib. The external aspect of the shaft at the p posterior angle is more consistent with a sixth rib while the orientation of the sternal end of the shaft is more similar to 2.02 1.82 8.36 6.50 0.61 1.09 0.50 20.9) 18.7) 121.0) 99.6) cant at 5.4) 9.6) 4.8) a seventh rib rather than to a sixth. ﬁ e e e e 33 32 32 31 31 33 31 e e e ¼ ¼ ¼ ¼ ¼ ¼ ¼ This rib does not preserve the head. However, the articular and n (12.8 (11.8 n (2.8 n (79.0 n (5.5 n (2.2 n (65.7 n nonarticular tubercles are completely fused, suggesting a minimum are signi

* age of 11 years (Ríos and Cardoso, 2009). The general size of this rib 0.72 16.85 1.40 15.36 0.39 4.06 1.54 7.57 0.01 3.30 (1.10) 97.77 (1.54) 79.96 9.35 2.70 1.63 5.42 0.59 1.53 0.67 23.9) 19.8 126.0) 94.5) 6.1) 12.7) 5.3) e e e e 32 33 33 30 30 32 30 e e e ¼ ¼ ¼ ¼ ¼ ¼ ¼ (14.4 n (12.9 n (3.9 n (85.0 n (7.3 n (2.9 n 9.44 (74.8 n * 1.54 19.55 1.14 4.98 2.31 1.37 4.21 L Z-score Summary statistics Z-score Summary statistics 1L 1R 1L 1R 3.3 5.9 17.9 0.50 17.08 ATD6-108 EuroAmerican males (1R) EuroAmerican females (1R) Amud 1 Kebara 2 Krapina 117.2 Krapina 117.3 Krapina 118.2 Krapina 117.1 Krapina 118.4 for ATD6-108 (1R) compared with modern human comparative samples, summary statistics of the modern male and female samples and measurements (in mm) of the Neandertal comparative sample. b b a

Values in parentheses are estimated.Measured Values in in cranio-caudal bold direction. letters and with an Figure 7. Cranial view of the second rib of (a) Kebara 2, (b) Tabun C1 (mirrored image), 19 MMxD 15.4 14 THD 6 NMNCCD 4.3 2a TVA (107.0) (0.29) 104.24 24 SEMnD 20 MMnD Variable 1a TVC (90.0) (0.98) 84.68 a b

Table 6 Z-score values and (c) ATD6-79. Scale bar ¼ 5 cm. A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 629

Table 7 Z-score valuesa for ATD6-79 (2R) compared with modern human comparative samples, summary statistics of the modern male and female samples and measurements (in mm) of the Neandertal comparative sample.

Variable ATD6-79 EuroAmerican males (2R) EuroAmerican females (2R) Kebara 2 Tabun C1

Z-scores Summary statistics Z-scores Summary statistics 2R 2L 2L 1a TVC (>130.0) (>0.06) 129.44 9.16 (>1.01) 122.31 7.60 137,2 (110.7e148.0) (106.4e136.5) n ¼ 27 n ¼ 27 z z 14 THD 16.4 2.68** 12.12 1.59 4.47** 10.07 1.42 14,3 (8.5e15.2) (6.6e12.3) n ¼ 30 n ¼ 32 19 MMxD 12.8 1.61 15.87 1.90 0.55 13.70 1.63 14,7 17,2 8,7 (11.6e20.0) (10.6e17.3) n ¼ 29 n ¼ 32 z 20 MMnDb 8.5 1.60 6.18 1.45 3.30** 5.30 0.97 4,8 4,8 7,6 (3.7e9.3) (3.2e7.4) n ¼ 29 n ¼ 32

z a Values in parentheses are estimated. Values in bold letters and with an *are significant at p < 0.05. Values in bold letters and ** are significant at p < 0.01. Values with a are outside the range of our modern comparison samples. b Measured in cranio-caudal direction. is similar to the mean values of our modern adult comparative the tuberculo-ventral chord (TVC) and the tuberculo-ventral arc samples and we consider that this rib belonged to an adolescent or (TVA) (Figs. 11 and 12). ATD6-89þ209 shows a curvature similar to young adult individual. modern adult seventh ribs. Unfortunately, the two Neandertal In general dimensions (TVC and TVA), ATD6-89þ206 is similar individuals that preserve the seventh ribs (i.e., Tabun C1 and Kebara to the seventh rib of the Tabun C1 female Neandertal and smaller 2) show evidence of taphonomic distortion (Gómez-Olivencia et al., than the male Neandertal individuals (Tables 5, 11 and 12). If this rib 2009b) and cannot be compared metrically with ATD6-89þ206. belonged to a male individual, it would only stand out by its significantly small values in the shaft maximum diameter at dorsal ATD6-85 (right eighth to tenth ribs) (Fig. 13) end (DSMxD). If this was a seventh rib belonging to a female individual, it would stand out for having a cranio-caudally low and ATD6-85 is from the right side and is comprised of nine frag- mediolaterally thick dorsal end of the shaft as well as a large ments that preserve nearly all the shaft, from a point located dorsal maximum diameter of the sternal end. Finally, this specimen also to the posterior angle to a cranio-caudal narrowing of the shaft shows a moderately large distance between the tubercle and the located close to the sternal end (Fig. 13). In these fractures, this iliocostal line (TID2), which is 1.52 SD above our modern female specimen has lost small bone chips; the largest (10.7 5.5 mm) comparative sample (Table 12). being the one located in the cranial aspect of the rib shaft, at the To better assess the anatomical position of this rib, we have posterior angle. performed a bivariate study between the tubercle-iliocostal line ATD6-85 most likely represents a ninth rib. However, due to its distance 2 (TID2) and tuberculo-ventral arc (TVA). Modern and incompleteness the possibility that it represents an eighth or a tenth fossil seventh ribs show larger TID2 than sixth ribs, while they rib cannot be ruled out. The ventral-most preserved part of the rib show similar values of TVA. ATD6-89þ206 is close to the male shaft is more vertical in ATD6-39 (see below) than in ATD6-85. centroid of the seventh rib and to the seventh rib of the Neandertal Additionally, the costal groove is more marked and longer in this rib Tabun C1 (Fig. 10), and thus we consider it more likely it to be that in ATD6-39. These two features make it more likely that this rib a seventh rib. is a ninth rather than a tenth rib. The presence of a cranio-caudal The curvature of this rib has been assessed by analyzing the narrowing in the ventral (sternal) third of the rib shaft is also more relationships between the tuberculo-ventral subtense (TVS) and consistent with ATD6-85 being a ninth rib rather than an eighth rib. the tuberculo-ventral chord (TVC), and the relationship between The age at death assessment of this rib should be regarded as tentative since it lacks the head and the tubercles. ATD6-85 does not display the porosity present in ATD6-97 or ATD6-251. Additionally, it shows marked muscular insertions at the posterior angle for the iliocostalis and at the shaft for the intercostals. Thus, we infer that this rib likely belonged to an adolescent or young adult individual. ATD6-85 shows shaft dimensions intermediate in size between the Neandertal male individuals of Kebara 2 and Shanidar 3, and the Neandertal female individual, Tabun C1 (Tables 5, 13 and 14). Compared with our modern human comparative samples, it only stands out for being significantly thicker at the mid-shaft. The fragmentary nature of this specimen prevents further conclusions.

ATD6-39 (right tenth rib) (Fig. 9)

ATD6-39 is from the right side and preserves the articular tubercle and the complete shaft, including the sternal end (Fig. 9). It is comprised of 12 fragments that rejoin perfectly with one another. In some of these unions, especially in the caudal aspect there has Figure 8. Cranial and caudal views of (a, d) ATD6-88, and (b, c)ATD6-66. Scale been some minor bone lost. We have assessed ATD6-39 as a tenth bar ¼ 5 cm. rib (less likely a ninth rib) based on the general size, the torsion of 630 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

Table 8 Z-score valuesa for ATD6-88 and ATD6-66 compared with modern human comparative samples.

Variable ATD6-88 EuroAmerican males EuroAmerican females ATD6-66 EuroAmerican EuroAmerican (Z-scores) (Z-scores) males (Z-scores) females (Z-scores)

4R 5R 4R 5R 3R 4L 3R 4L z z z 4a HCCD 9.1 L2.46* L2.64** 0.85 1.80 5a TNL 32.7 0.79 0.80 0.52 0.58 z 6 NMnCCD 7.1 1.70 L2.29* 1.12 1.92 7 NTh 4.1 0.98 1.51 0.39 0.79 10b TID2 35.3 0.00 1.50 0.65 0.69 z 15 DSMxD 6.9 L2.18* L2.56* 1.06 1.74 6.8 1.86 L2.02* 1.43 1.58 z z 16 DSMnD 8.0 0.16 0.24 2.81** 2.73** 7.7 0.13 0.19 1.95 1.80 17 SMxD 9.7 0.74 1.31 0.17 0.78 9.7 0.50 1.01 0.45 0.06 18 SMnD 7.9 0.55 0.98 1.14 0.67 7.3 1.03 1.13 0.53 0.31

z a Values in parentheses are estimated. Values in bold letters and with an *are significant at p < 0.05. Values in bold letters and ** are significant at p < 0.01. Values with a are outside the range of our modern comparison samples. the shaft and the cross-sectional morphology at the angle and mid- only comparable with that of La Chapelle-aux-Saints. However, the shaft. The presence of an articular tubercle in ATD6-39 allows the dimensions of TVA and TVC are slightly smaller than those in the comparison of this rib with modern and fossil ribs. The large right tenth rib from Kebara 2. In order to assess the curvature of this distance between the articular tubercle and the iliocostal line rib, we have performed a bivariate analysis between the TVC and (TID2) indicates that this is a tenth rib (Fig. 14). This rib does not the TVA (Fig. 15). ATD6-39 is within the upper limit of the 70% preserve the head. However, the articular tubercle is completely equiprobability ellipse for modern adult males due to its large TVA, fused, suggesting a minimum age of 12 years at the time of death which means that this rib is slightly more curved than the mean (Ríos and Cardoso, 2009). The general size of this rib is similar to the modern male sample. mean values of our modern adult comparative samples and we consider it to represent an adolescent or young adult. This rib ATD6-97 (left tenth rib) (Fig. 9) shows less torsion in the shaft at the posterior angle. The functional significance of this remains unclear but we hypothesize that it ATD6-97 is from the left side and preserves a nearly complete could be related to a more horizontal disposition of the rib. shaft, lacking the head, part of the neck and the sternal end (Fig. 6). Compared with our modern human comparative samples, ATD6-97 is very fragmentary and the specimen has suffered taph- ATD6-39 has a thick shaft and a large sternal end (Tables 5 and 15). onomic deformation in the middle of the shaft due to crushing. This Moreover, if this rib belonged to a female individual, it would stand specimen most likely represents a tenth rib. Morphologically, it is out for its large general dimensions (TVA and TVC). Compared with very similar to ATD6-251 and ATD6-39. In contrast with ATD6-39, Neandertals, ATD6-39 is similar to male individuals and larger than this rib does not present an articular tubercle. The position of the the Tabun C1 female. ATD6-39 stands out for its large sternal end, iliocostal line, the torsion of the shaft, the morphology of the

Table 9 Summary statistics (mean, SD, range and samples sizes) for ribs 3 R, 4 R, 4 L and 5 R in the modern comparative samples.

Variable EuroAmerican males EuroAmerican females

3R 4R 4L 5R 3R 4R 4L 5R 4a HCCD 10.50 1.37 11.85 1.12 12.12 1.44 13.49 1.66 9.22 1.57 10.28 1.39 10.62 1.24 11.17 1.15 (7.7e13.5) (9.9e14.5) (9.3e15.8) (10.1e17.5) (7.0e12.8) (8.1e13.3) (9.1e13.0) (9.7e14.1) n ¼ 26 n ¼ 28 n ¼ 26 n ¼ 28 n ¼ 27 n ¼ 28 n ¼ 22 n ¼ 28 5a TNL 34.24 1.79 34.50 2.29 34.34 2.36 34.52 2.27 31.29 2.09 31.64 2.04 31.58 2.28 31.36 2.28 (29.2e38.5) (29.4e38.4) (29.9e38.5) (29.7e37.8) (26.6e37.0) (27.1e35.2) (27.3e35.4) (26.1e35.9) n ¼ 29 n ¼ 28 n ¼ 26 n ¼ 29 n ¼ 28 n ¼ 29 n ¼ 24 n ¼ 29 6 NMnCCD 8.61 1.34 10.02 1.72 10.93 1.64 12.01 2.14 7.49 1.20 8.56 1.31 8.47 1.22 10.63 1.84 (6.3e11.2) (5.3e12.4) (7.1e13.4) (7.7e15.2) (5.4e10.6) (6.2e11.7) (6.5e10.5) (8.1e14.4) n ¼ 29 n ¼ 29 n ¼ 26 n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 23 n ¼ 29 7 NTh 4.95 0.83 5.19 1.11 5.17 0.61 5.39 0.86 4.24 0.73 4.42 0.81 4.42 0.55 4.39 0.37 (3.4e6.3) (3.8e9.9) (4.2e7.0) (3.8e7.3) (3.2e7.1) (3.2e7.6) (3.2e5.3) (3.6e5.1) n ¼ 29 n ¼ 29 n ¼ 27 n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 24 n ¼ 29 10b TID2 29.74 3.03 35.29 2.91 36.00 3.22 40.69 3.58 27.94 3.23 33.23 3.18 31.84 3.03 37.29 2.90 (22.7e33.8) (29.5e40.5) (29.8e41.1) (32.7e47.2) (22.0e36.0) (29.3e40.1) (26.6e36.9) (29.7e44.7) n ¼ 29 n ¼ 29 n ¼ 27 n ¼ 29 n ¼ 29 n ¼ 29 n ¼ 24 n ¼ 30 15 DSMxD 8.71 1.03 8.90 0.92 8.83 1.00 9.56 1.04 8.02 0.85 8.01 1.04 8.19 0.88 8.52 0.93 (6.2e11.3) (6.9e11.3) (6.7e11.3) (6.9e12.0) (6.4e10.1) (6.2e10.1) (6.3e10.0) (6.9e10.9) n ¼ 29 n ¼ 29 n ¼ 27 n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 24 n ¼ 29 16 DSMnD 7.83 1.03 7.78 1.42 7.90 1.06 7.76 0.99 6.17 0.79 5.98 0.72 6.08 0.90 5.98 0.74 (5.4e10.4) (5.9e13.1) (6.3e9.8) (5.2e9.7) (4.8e8.2) (4.6e7.4) (4.2e7.8) (4.6e8.1) n ¼ 29 n ¼ 29 n ¼ 27 n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 24 n ¼ 29 17 SMxD 10.26 1.14 10.83 1.54 11.04 1.32 12.07 1.80 9.27 0.97 9.94 1.44 9.78 1.29 11.20 1.93 (7.3e12.2) (7.6e13.8) (8.5e13.3) (8.6e14.8) (6.7e11.7) (7.3e12.7) (7.3e11.9) (8.5e14.9) n ¼ 29 n ¼ 29 n ¼ 27 n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 23 n ¼ 28 18 SMnD 8.37 1.04 8.74 1.52 8.63 1.18 9.17 1.30 6.66 1.22 6.91 0.87 7.01 0.94 7.24 0.97 (6.1e10.4) (5.9e12.0) (6.4e10.8) (6.6e11.6) (4.6e9.1) (5.4e8.8) (5.1e9.1) (5.8e9.3) n ¼ 28 n ¼ 29 n ¼ 27 n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 24 n ¼ 29 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 631

Table 10 Measurements (in mm) of the Neandertal comparative sample for ribs 3 to 5.

Variable Kebara 2 Shanidar 3 Kebara 2 Shanidar 3 Kebara 2 Shanidar 3

3R 3L 3R 4R 4L 4R 5R 5L 5R 5L 4a HCCD 9.9 5a TNL 32.9 6 NMnCCD 9.1 11.9 7 NTh 5.0 4.9 6.7 10b TID2 32.1 44.8 41.7 15 DSMxD 11.1 9.2 8.7 11.7 9.4 8.9 16 DSMnD 9.7 7.2 8.1 8.2 8.0 9.6 17 SMxD (15.5) 14.9 16.7 (17.0) (17.7) 12.1 18 SMnD 7.9 7.8 7.4 9.5 7.6 9.6 9.4 9.6 9.7 cross-section of the shaft at the posterior angle and at the mid-shaft represents a tenth rib. Morphologically, it is very similar to ATD6- and the overall size suggest that ATD6-97 is a tenth rib. In fact, the 39, but it does not present an articular tubercle. The position of the orientation of the iliocostal line in external view is similar to iliocostal line, the torsion of the shaft and the morphology of the modern tenth ribs. Although it is less likely to represent an eleventh cross-section at the mid-shaft and at the posterior angle indicate rib, we cannot rule out this possibility. This rib does not preserve that this is a tenth rib, although the possibility that it represents an the head, thus its age at death assessment should be regarded as eleventh rib cannot be entirely ruled out. The articular tubercle is tentative. The external surface of the rib shaft is porous and the present in the 91% of the ninth ribs of a pooled sex sample of 98 porosity increases towards the sternal end, indicating that the modern human individuals. Thus, its absence in ATD6-251 rules out growth process was still ongoing. Thus, this rib likely belonged to this specimen representing a ninth rib. The ventral third of the shaft an immature individual, younger than ATD6-251 (see below). shows a very porous surface, indicating that the growth process was still ongoing and this rib likely belonged to an immature individual. ATD6-251 (right tenth rib) (Fig. 13)

ATD6-251 is from the right side and preserves a nearly complete Discussion shaft, from the point equivalent to the tubercle in other ribs to the sternal end (Fig. 13). This rib is broken in six fragments that Anatomical position generally rejoin well with each other, but some taphonomic distortion of the specimen is present in the mid-shaft. There is Metric analysis has been shown to be a useful and comple- slight bone loss at all the fracture points. This specimen most likely mentary approach to morphological criteria for reﬁning the

Figure 9. Caudal and cranial views of (a, f) ATD6-89þ206, (b, e) ATD6-39, and (c, d) ATD6-97. Scale bar ¼ 5 cm. 632 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

Table 11 Z-score values for ATD6-89þ206 compared with modern human comparative samples and summary statistics of the modern male and female samples.a

Variables ATD6-89þ206 EuroAmerican males EuroAmerican females

6R 7R 6R 7R

Z-scores Summary statistics Z-scores Summary statistics Z-scores Summary statistics Z-scores Summary statistics z 1a TVC 224.0 0.54 216.28 14.33 0.05 223.27 14.87 2.09* 198.52 12.20 1.46 206.86 11.76 (184.5e235.5) (189.0e244.8) (171.4e218.7) (179.4e231.0) n ¼ 26 n ¼ 26 n ¼ 22 n ¼ 29 2a TVA 275.0 0.54 283.69 16.10 0.56 284.56 16.96 0.75 266.09 11.89 0.83 264.55 12.52 (244.0e305.0) (244.0e315.0) (242.0e283.0) (239.0e282.0) n ¼ 26 n ¼ 26 n ¼ 22 n ¼ 29 3 TVS 68.0 0.03 68.17 6.21 0.71 63.42 6.42 0.24 66.69 5.47 1.18 60.78 6.10 (55.1e79.6) (52.0e84.3) (57.5e77.8) (52.6e74.6) n ¼ 26 n ¼ 26 n ¼ 23 n ¼ 29 z 10b TID2 (52.0) (1.00) 47.32 4.67 (0.01) 51.95 3.90 (3.19)** 42.93 2.84 (1.52) 47.03 3.28 (38.2e57.4) (42.9e58.0) (37.4e47.9) (40.2e53.7) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 z 11b PAC2 95.0 1.19 85.24 8.23 0.28 92.96 7.37 3.15** 78.01 5.39 1.59 84.95 6.32 (70.1e103.2) (77.0e105.1) (66.9e87.8) (72.1e98.8) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 12b PAS2 (21.2) (0.27) 20.51 2.59 (0.99) 23.15 1.97 (1.80) 17.86 1.86 (0.48) 20.07 2.39 (15.1e25.2) (18.7e26.9) (14.4e21.0) (15.9e24.4) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 13 PA (129.4) (0.29) 128.49 3.18 (0.74) 126.93 3.34 (0.32) 130.81 4.42 (0.00) 129.39 5.51 (119.7e133.3) (121.9e132.3) (119.5e137.5) (116.1e137.8) n ¼ 29 n ¼ 29 n ¼ 29 n ¼ 29 z z z 15 DSMxD 7.4 L2.58** 10.14 1.06 L2.63** 10.57 1.21 1.78 9.40 1.12 L2.49* 9.67 0.91 (7.8e12.3) (8.8e13.4) (7.5e12.5) (7.6e11.9) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 z 16 DSMnD 8.1 0.32 7.82 0.88 0.07 8.04 0.85 2.83** 6.21 0.67 3.30** 6.06 0.62 (5.9e9.3) (6.6e10.0) (5.2e8.4) (4.8e7.1) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 17 SMxD 10.7 1.30 13.35 2.04 1.53 13.88 2.08 0.96 12.63 2.01 1.34 12.97 1.69 (9.9e18.3) (9.0e18.3) (9.3e17.6) (9.2e16.6) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 18 SMnD 8.5 0.75 9.45 1.26 0.92 9.64 1.24 1.09 7.47 0.95 1.21 7.19 1.08 (7.1e12.1) (7.7e12.4) (6.0e9.3) (5.3e9.2) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 19 MMxD 11.4 0.35 12.00 1.71 1.13 13.32 1.70 0.27 10.98 1.53 0.45 12.08 1.52 (9.1e15.3) (10.3e17.0) (8.3e14.3) (9.1e15.1) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 20 MMnD 6.3 0.95 7.10 0.84 0.90 7.13 0.92 0.97 5.39 0.94 1.11 5.28 0.92 (5.7e8.7) (5.3e9.0) (4.0e7.5) (3.7e7.2) n ¼ 29 n ¼ 29 n ¼ 30 n ¼ 30 z z 23 SEMxD (18.7) (1.58) 16.03 1.69 (1.03) 17.01 1.64 (3.80)** 13.90 1.26 (2.03)* 14.59 2.02 (13.0e20.3) (14.5e20.8) (11.2e15.5) (10.2e18.1) n ¼ 23 n ¼ 25 n ¼ 22 n ¼ 23 24 SEMnD 8.3 0.40 8.81 1.25 0.34 8.74 1.31 1.05 7.44 0.82 1.22 7.43 0.71 (7.2e11.3) (6.8e11.5) (6.2e9.3) (6.2e8.7) n ¼ 24 n ¼ 26 n ¼ 21 n ¼ 27

Table 12 Measurements (in mm) of the Neandertal comparative sample for ribs 6 to 7.

Variable Kebara 2 Shanidar 3 Tabun C1 Kebara 2 Shanidar 3 Tabun C1

6R 6L 6R 6R 6L 7R 7L 7R 7R 7L 1a TVC (185-190)a 213.0a 2a TVA 290.0 (340.0) 290.0 3 TVS (87.5)a 79.1a 10b TID2 47.5 57.4 56.3 65.0 52.7 11b PAC2 78.4 103.5 92.3 12b PAS2 26.8 25.7 25.4 13 PA 136.2 137.2 15 DSMxD 6.9 9.6 11.0 7.2 16 DSMnD 7.0 8.2 10.1 7.1 17 SMxD (18.2) 14.3 11.7 (11.3) 16.4 15.1 16.4 (14.0) 18 SMnD 11.8 9.8 6.7 6.4 11.8 9.3 9.9 8.1 19 MMxD (12.7) 10.6 14.5 (12.5) 17.0 13.1 13.7 20 MMnD 4.3 5.8 9.3 9.2 8.1 6.0 8.1 23 SEMxD 21.9 20.2 16.6 24 SEMnD (10.0) 12.3 9.3

Values in parentheses are estimated. a These measurements may be affected by taphonomical distortion. A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 633

Figure 10. Tuberculo-ventral arc (TVA) (x) vs. tubercle-iliocostal line distance 2 (TID2) (y) in the sixth and seventh ribs. The modern human comparative samples are represented by 70% equiprobability ellipses and show a high degree of overlap. Neandertals show larger dimensions for the TVA and TID2 than the modern human comparative samples of the same sex and anatomical position. ATD6-89þ206 is similar in dimensions to the modern male seventh rib sample and to the seventh rib of the Tabun C1 female Neandertal. Note that both Tabun C1 and Kebara 2 show larger values for TVA than modern females and males respectively, and thus are displaced to the right of the plot.

Figure 11. Curvature of the ATD6-89þ206 rib: tuberculo-ventral subtense (TVS) (x) vs. tuberculo-ventral chord (TVC) (y). The modern human comparative samples are represented by 70% equiprobability ellipses and show a high degree of overlap. ATD6-89þ206 is similar in size to our modern male sample, but using these variables it could represent either a sixth or a seventh rib. 634 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

Figure 12. Curvature of the ATD6-89þ206 rib: tuberculo-ventral chord (TVC) (x) vs. tuberculo-ventral arc (TVA) (y). The modern human comparative samples are represented by 70% equiprobability ellipses and show a high degree of overlap. ATD6-89þ206 is similar in size to our male sample but using these variables it is more likely to be a seventh rib.

Figure 13. Cranial and caudal views of (a, d) ATD6-85, and (b, c) and ATD6-251. Scale bar ¼ 5 cm. A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 635

anatomical position of some of the Gran Dolina ribs (Table 1). In the case of the specimen ATD6-88, it has been possible to discount that 2.09 1.90 0.98 0.82 ﬁ 17.4) 8.1) 6.6) 19.1) it represents a third rib. In addition, ATD6-39 has been con rmed as 30 30 30 30 e e e e ¼ ¼ ¼ ¼ it being a tenth rib, and the possibility of representing a ninth rib (9.7 n (3.6 n (2.6 n 3.80 (9.7 n statistics was ruled out. Finally, in the case of ATD6-89þ206, the metric study suggests that it is most likely a seventh rib rather than a sixth rib. z

** Thus, the combination of morphological and metric criteria can provide an accurate assessment of the anatomical position of 1.68 13.99 1.76 5.68 (3.92) (0.76) 13.26 10R Z-scores Summary isolated ribs.

Thorax size of the TD6 hominins 14.29 2.29 1.55 261.0) 0.96 0.78 17.8) 19.2) 8.7) 6.9) e “ 30 30 30 23 30 e e e Larson (2007: 182) has hypothesized that H. antecessor is ¼ ¼ ¼ ¼ ¼ are outside the range of our modern unlikely to have had the cold climate adaptation of an enlarged (9.7 n (4.5 n (3.2 n 237.61 (208.0 e n 4.39 n 14.01 (10.9 statistics z chest as do later Neandertals”. This assertion was based on the

z absence of cold-adapted taxa among the ungulates of TD6 (van der ** Made, 1999, 2001) and the assumption that the large chest of 1.19 14.79 1.04 6.40 (0.45) (3.33) 9R Z-scores Summary Neandertals represents a cold adaptation. A recent reassessment of the costal remains from the Kebara 2 male Neandertal individual

0.01. Values with a (Gómez-Olivencia et al., 2009b) has corroborated the hypothesis <

13.49 that H. neanderthalensis had a capacious thorax, as previously p 1.74 1.90 276.0) 1.12 1.01 17.5) e proposed by other authors (Franciscus and Churchill, 2002; 16.1) 9.2) 6.9) e 30 30 30 30 24 e e e Weinstein, 2008). Moreover, a shape difference in the thorax of ¼ ¼ ¼ ¼ ¼ cant at n (8.6 (10.1 n (5.0 n (3.0 n ﬁ 256.00 (232.0 n 4.55 statistics Kebara 2 in comparison with modern humans was also demon- strated. While the uppermost and lowermost ribs of the Kebara 2 z * individual are similar to modern males, the mid-thorax ribs are are signi ﬁ ** signi cantly larger. Following Churchill (2006), a large chest would 1.84 14.00 0.73 6.59 (0.82) 13.27 (2.43) EuroAmerican females 8R Z-scores Summary better supply the large oxygen demands of a relatively large body and high activity levels, and would have been advantageous in cold 1.97 1.76 climates. It has been argued that this would have been the result of 0.88 1.20 18.8) 19.5) 7.4) 9.5) e e an exaptation rather than cold adaptation per se (Gómez-Olivencia 29 29 29 29 e e ¼ ¼ ¼ ¼ et al., 2009b). Moreover, the large size of the Neandertal thorax was (10.8 n (12.7 n (3.7 n (5.0 n 5.12 statistics argued to represent one manifestation of a primitive body bauplan,

* consisting of wide and heavy bodies inherited from their Middle Pleistocene ancestors (Arsuaga et al., 1999a; Gómez-Olivencia et al., 0.08) 14.85 1.18 15.42 0.04 7.35 (2.15)

2009b). 0.05. Values in bold letters and ( 10R Z-scores Summary

< Up until the 2007 ﬁeld season, the Sima de los Huesos Middle p Pleistocene site has yielded a total of 503 costal fragments belonging to the species H. heidelbergensis, a taxon which has been 16.24 1.79 2.01 cant at 285.0) 0.93 1.00 ﬁ 19.7) 20.3) argued to be ancestral to H. neanderthalensis (Arsuaga et al., 1993, e 7.3) 9.9) e e 29 29 29 29 23 e e 1997b). Ongoing efforts at reconstruction and rejoining of these ¼ ¼ ¼ ¼ ¼ (12.4 n (12.9 n (3.9 (5.5 n n 260.50 (225.0 n statistics costal fragments have yielded 400 remains belonging to are signi

* a minimum of 114 ribs, but only two of them (a ﬁrst and an eleventh rib) are complete. Although the size of these complete specimens as 0.32) 15.28 0.58 16.33 0.54 7.94 well as the other fragmentary remains suggests that the hominins (1.51) 5.60 ( 9R Z-scores Summary from Sima de los Huesos also possessed a large thorax (Gómez- Olivencia, 2009; Gómez-Olivencia et al., 2009a), this observation cannot be conﬁrmed until more complete mid-thoracic ribs are 15.01 1.93 2.09 recovered or reconstructed in the future. 307.5) 1.22 1.16 18.3) e 18.7) 11.9) 9.0) e Regarding the TD6 remains, the only complete mid-thoracic rib 29 29 29 29 25 e e e ¼ ¼ ¼ ¼ ¼ of H. antecessor is ATD6-89þ206 (left seventh rib). This specimen is (11.8 n (9.8 n (5.9 n (3.8 n statistics n (255.0 280.04 similar in size to our modern male comparative sample and among the fossil specimens most closely resembles the female Neandertal individual, Tabun C1, in size. Being an isolated element, we have no

1.09 8.72 independent elements to assess its sex. The direct application of 8R Z-scores Summary discriminant analysis based on modern comparative samples (which relies on the unproven assumption that the TD6 hominins show a modern thorax size and shape) would suggest a male sex

245.0 þ e > diagnosis. ATD6-89 206 belonged to a late adolescent young adult individual. Among the 11 dentally-deﬁned individuals rep- for ATD6-85 compared with modern human comparative samples and summary statistics of the modern male and female samples.

a resented in the TD6 level, only four correspond to adolescent or young adults: an adolescent male (Hominid 1: age at death 12.9 SMnD 7.4 years), a young adult male (Hominid 10), an adolescenteyoung

Values in parentheses are estimated. Values in bold letters and with an adult female (Hominid 7, age at death 16.6 years) and one young 18 19 MMxD (14.7) (0.03) 14.64 17 SMxD 17.5 1.19 15.01 Variable ATD6-85 EuroAmerican males 20 MMnD (7.0) (0.74) 6.14 2a TVA a comparison samples. Table 13 Z-score values adult of undetermined sex (Hominid 4, age at death 18 years) 636 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

Table 14 Measurements (in mm) of the Neandertal comparative sample for ribs 8e9.

Variable Kebara 2 Shanidar 3 Tabun C1 Kebara 2 Shanidar 3 Tabun C1

8R 8L 8R 8L 8R 8L 9R 9L 9R 9L 9R 9L 2a TVA (325.0) 269.0 17 SMxD 16.8 15.8 16.9 18.4 13.2 17.2 18.1 18.1 15.0 (13.5) 18 SMnD 10.1 10.0 9.8 9.3 6.6 8.8 8.8 9.8 9.2 7.3 19 MMxD (16.1) 16.3 (11.8) 11.7 16.1 15.3 (12.7) 13.5 20 MMnD (8.3) 8.2 (5.4) 6.4 7.4 8.5 (6.0) 6.0

(Carbonell et al., 2005; Bermúdez de Castro et al., 2006, 2008, In addition, other skeletal elements, in particular the clavicles 2010). Thus, even assuming that the rib remains recovered from from the TD6 level at the Gran Dolina, can also provide some TD6 belong to one of the individuals represented by the dental information about the thorax size of H. antecessor. Because the remains, we still cannot reliably infer the sex of this individual. clavicle is functionally part of the shoulder, its length is related to We can, however, explore the implications of ATD6-89þ206 the breadth of the upper torso and provides information on this belonging to a male or a female individual. If this rib belonged to aspect of the upper body trunk. The extreme length of Neandertal a male individual and if we assume that this rib is from an average clavicles is related to their broad shoulders (Boule, 1911e1913; individual (i.e., is not abnormally small or large), then the thorax Heim, 1976; Trinkaus, 1983; Churchill, 1994a; Vandermeersch and size in H. antecessor would appear to be similar to H. sapiens. On the Trinkaus, 1995). At the same time, Carretero et al. (1999) other hand, if ATD6-89þ206 belonged to a female individual, then proposed that the long absolute length of the adult clavicle, H. antecessor would show a large thorax similar to that of H. ATD6-50, also strongly suggest H. antecessor, like the Neandertals, is neanderthalensis, which would be consistent with our hypothesis characterized by a relatively long clavicle compared with H. sapiens. that the large size of the Neandertal thorax is linked to a primitive Moreover, the ratio of the medial length to the total length of the body bauplan consisting of wide and heavy bodies (Gómez- clavicle has been suggested as informative of the anteroposterior Olivencia et al., 2009b). Evidence for heavy-bodied hominins (i.e., depth of the upper thorax (Vrba, 1979). Churchill (1994a,b) found large body mass) has been found in the Middle Pleistocene of support to this suggestion among modern humans. Based on the Africa, Asia and Europe (Arsuaga et al., 1999a; Rosenberg et al., measurements of the ATD6-50 clavicle reported by Carretero et al. 2006; Trinkaus, 2009; Churchill et al., in press) and has been (1999), we can calculate its conoid index (Conoid length/Maximum proposed for the Lower Pleistocene of Africa (KNM-WT 15000, see length 100). This calculation results in an index of 79.3, similar to Grine et al., 1995). that reported by Churchill (1994a) for the deep chested Aleutian

Figure 14. Tuberculo-ventral arc (TVA) (x) vs. tubercle-iliocostal line distance 2 (TID2) (y). The Kebara 2 ninth rib is incomplete. Its TVA was estimated through regression analysis based on our modern male comparative samples using the complete eighth and tenth ribs, which have yields two different estimates. In addition, the TID2 from both sides was used, resulting in a total of four estimates. Kebara 2 follows the modern human pattern for the ninth rib, but is larger. On the contrary, ATD6-39 shows a large tubercle-iliocostal line distance, more compatible with a tenth rib rather than a ninth rib. A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 637

Table 15 Z-score valuesa for ATD6-39 compared with modern human comparative samples and summary statistics of the modern male and female samples.

Variable ATD6-39 EuroAmerican males (10R) EuroAmerican females Tabun C1 Kebara 2 La Chapelle-aux- Shanidar 3 (10R) Saints

Z-scores Summary Z-scores Summary 10L 10R 10L 10R 10L 10R statistics statistics 1b ChCaV (190.0) (0.07) 188.92 14.42 (1.79) 170.74 10.77 (225.0) (155.4e216.5) (151.7e194.1) n ¼ 24 n ¼ 25 z 2b ACaV (273.0) (0.98) 252.52 20.81 (2.59)** 227.92 17.41 (285.0) (208.0e284.0) (186.0e260.0) n ¼ 24 n ¼ 25 15 DiCrCdEDCu 9.3 0.30 9.56 0.86 0.90 8.54 0.84 8.8 9.7 7.5 8.2 9.3 (7.9e11.7) (7.1e10.0) n ¼ 29 n ¼ 29 z z 16 GEDCu 8.6 2.76** 6.51 0.76 6.25** 5.42 0.51 8.3 7.4 9.8 9.2 8.4 (5.4e8.3) (4.4e6.3) n ¼ 29 n ¼ 29 17 DiCrCdAngP 16.2 0.44 15.42 1.76 1.06 13.99 2.09 11.4 (16.5) 14.9 (16.0) 14 (12.7e19.5) (9.7e17.4) n ¼ 29 n ¼ 30 z 18 GAngP 8.3 0.79 7.35 1.20 2.68** 5.68 0.98 6.8 9.7 9.8 9.9 9.2 9.1 (5.0e9.5) (3.6e8.1) n ¼ 29 n ¼ 30 19 DiCrCdCuM 15.3 0.23 14.85 1.97 1.07 13.26 1.90 12.3 15.4 (16.0) (10.8e18.8) (9.7e19.1) n ¼ 29 n ¼ 30 z z 20 GCuM 7.6 2.83** 5.12 0.88 4.65** 3.80 0.82 5.5 6.6 (8.1) 8.2 (3.7e7.4) (2.6e6.6) n ¼ 29 n ¼ 30 z z 23 SEMxD 15.4 3.22** 10.94 1.38 5.64** 9.12 1.11 10.8 (8.8e15.2) (6.9e11.5) n ¼ 24 n ¼ 25 z z 24 SEMnD 9.5 2.58** 7.12 0.92 3.38** 5.69 1.13 7.5 >10.0 9.4 (5.2e8.6) (1.7e7.0) n ¼ 24 n ¼ 25

Figure 15. Curvature of the ATD6-39 rib: chord variables (x) vs. arc variables (y) for the ninth and tenth ribs. The modern human comparative samples are represented by 70% equiprobability ellipses and show a high degree of overlap. If ATD6-39 was a ninth rib, it would be located in the overlapping zone between the males and females. However, ATD6- 39 is a tenth rib (see text) and thus, is in the upper limits of the male comparative sample, indicating that this rib is relatively curved. 638 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640

Islanders. This is consistent with an anteroposteriorly large thorax Educación (Programa Nacional de Movilidad de Recursos Humanos as suggested by the ATD6-79 rib. del Plan Nacional de I-Dþi 2008-2011). This research was sup- A second complete left clavicle (ATD6-37) representing ported by the Ministerio de Ciencia e Innovación, Proyectos a subadult individual is also present in the fossil sample from TD6 CGL2006-13532-C03-01/02/03 and CGL2009-12703-C03-01/02/03 (Carretero et al., 1999). The maximum length of ATD6-37 (83.7 mm) and by Junta de Castilla y León Project BU00509. This research suggests an age at death of between five and seven years old when received support from the SYNTHESYS Project http://www. compared with specimens of similar length from H. sapiens juve- synthesys.info/, which is financed by European Community niles. However, when compared with the adult clavicular length for Research Infrastructure Action under the FP6 “Structuring the H. antecessor, based on the ATD6-50 specimen, an age at death of European Research Area” Programme. Funding for the fieldwork two to four years is suggested for ATD6-37. This indicates that this came from the Junta de Castilla y León and Fundación Atapuerca. subadult H. antecessor individual is also characterized by a rela- Help in the field from the Grupo Espeleológico Edelweiss was tively long clavicle compared with modern human children of essential. The first author (AGO) would like to thank his family for similar age (García-González et al., 2009). Relatively long clavicles all their support. have been also noted in the Neandertal children from Roc de Marsal 1(Madre-Dupouy, 1992), Amud 7, Dederiyeh 1 and Teshik-Tash References (García-González et al., 2009). Thus, the relatively long clavicle in both adult and subadult individuals of H. antecessor provides Arensburg, B., 1991. The vertebral column, thoracic cage and hyoid bone. In: Bar- additional support for the hypothesis that, like the Neandertals, Yosef, O., Vandermeersch, B. (Eds.), Le squelette moustérien de Kébara 2. Éditions du CNRS, Paris, pp. 113e147. these hominins had a broader thorax than living humans. Arsuaga, J.L., Martínez, I., Gracia, A., Carretero, J.M., Carbonell, E., 1993. Three new The costal elements recovered to date from the TD6 level at the human skulls from the Sima de los Huesos Middle Pleistocene site in Sierra de Gran Dolina can neither confirm nor reject the hypothesis that Atapuerca, Spain. Nature 362, 534e537. Arsuaga, J.L., Martínez, I., Gracia, A., Carretero, J.M., Lorenzo, C., Garcia, N., H. antecessor had a large thorax similar to that of Neandertals. Ortega, A.I., 1997a. Sima de los Huesos (Sierra de Atapuerca, Spain). The site. However, the fragmentary evidence of the H. antecessor thoracic J. Hum. Evol. 33, 109e127. skeleton is consistent with this suggestion based on other skeletal Arsuaga, J.L., Martínez, I., Gracia, A., Lorenzo, C., 1997b. The Sima de los Huesos crania e elements. Future discoveries of additional costal remains from the (Sierra de Atapuerca, Spain). A comparative study. J. Hum. Evol. 33, 219 281. Arsuaga, J.L., Lorenzo, C., Carretero, J.M., Gracia, A., Martínez, I., García, N., Bermúdez Gran Dolina may prove more informative and help elucidate the de Castro, J.M., Carbonell, E., 1999a. A complete human pelvis from the Middle size and shape of the thorax of the first inhabitants of Europe. Pleistocene of Spain. Nature 399, 255e258. Arsuaga, J.L., Martínez, I., Lorenzo, C., Gracia, A., Muñoz, A., Alonso, O., Gallego, J., 1999b. The human cranial remains from Gran Dolina Lower Pleistocene site Acknowledgements (Sierra de Atapuerca, Spain). J. Hum. Evol. 37, 431e457. Arsuaga, J.L., Martínez, I., Gracia, A., 2001. Analyse phylogénétique des Hominidés We are grateful to the Atapuerca excavation team, especially the de la Sierra de Atapuerca (Sima de los Huesos et Gran Dolina TD-6): l’évidence crânienne. L’Anthropologie 105, 161e178. team involved in the test pit excavation at Gran Dolina during mid Berger, G.W., Pérez-González, A., Carbonell, E., Arsuaga, J.L., Bermúdez de 1990s and the team involved in the excavation of the TD6 level Castro, J.M., Ku, T.-L., 2008. Luminescence chronology of cave sediments at the during the last few years, for their dedication and effort. The Atapuerca paleoanthropological site, Spain. J. Hum. Evol. 55, 300e311. Bermúdez de Castro, J.M., Arsuaga, J.L., Carbonell, E., Rosas, A., Martínez, I., restoration of these specimens has been performed by Lucía López- Mosquera, M., 1997. A hominid from the Lower Pleistocene of Atapuerca, Spain: Polín. We are also grateful to Philip Mennecier (Musée de l’Homme, possible ancestor to Neandertals and modern humans. Science 276, 1392e1395. Paris), Yohannes Haile-Selassie (Cleveland Natural History Bermúdez de Castro, J.M., Rosas, A., Nicolás, M.E., 1999a. Dental remains from Atapuerca-TD6 (Gran Dolina site, Burgos, Spain). J. Hum. Evol. 37, 523e566. Museum), Chris Stringer and Rob Kruszynski (Natural History Bermúdez de Castro, J.M., Rosas, A., Nicolás, M.E., Rodríguez, J., Carbonell, E., Museum, London), Yoel Rak (Department of Anatomy, Sackler Arsuaga, J.L., 1999b. A modern human pattern of dental development in Lower School of Medicine, Tel Aviv University, Israel), Richard Potts Pleistocene hominids from Atapuerca-TD6 (Spain). Proc. Natl. Acad. Sci. U S A e (Smithsonian Institution-National Museum of Natural History, 96, 4210 4213. Bermúdez de Castro, J.M., Sarmiento, S., 2001. Analyse morphométrique comparée Washington D.C.), Jakov Radovcic (Croatian Natural History des dents humaines de Gran Dolina (TD6) et de Sima de los Huesos d’Atapuerca. Museum, Zagreb), Jean-Jacques Hublin (Department of Human L’Anthropologie 105, 203e222. Evolution, Max Planck Institute, Leipzig) for providing access to the Bermúdez de Castro, J.M., Martinón-Torres, M., Sarmiento, S., Lozano, M., 2003. Gran Dolina-TD6 versus Sima de los Huesos dental samples from Atapuerca: important specimens under their care. We are also indebted to evidence of discontinuity in the European Pleistocene population? J. Archaeol. Aurélie Fort, Véronique Laborde, Liliana Huet, Lyman Jellema and Sci. 30, 1421e1428. Jennifer Clark for curatorial assistance. Bermúdez de Castro, J.M., Carbonell, E., Gómez, A., Mateos, A., Martinón-Torres, M., Muela, A., Rodríguez, J., Sarmiento, S., Varela, S., 2006. Paleodemografía del Further thanks go to our colleagues at the Centro UCM-ISCIII de hipodigma de fósiles de homininos del nivel TD6 de Gran Dolina (Sierra de Investigación sobre Evolución y Comportamiento Humanos, Labo- Atapuerca, Burgos): estudio preliminar. Estudios Geológicos 62, 145e154. ratorio de Evolución Humana (LEH) of the Universidad de Burgos, Bermúdez de Castro, J.M., Martinón-Torres, M., Gómez-Robles, A., Prado, L., Sarmiento, S., 2007. Comparative analysis of the Gran Dolina-TD6 (Spain) and Tighennif (Algeria) the Centro Nacional de Investigación sobre la Evolución Humana hominin mandibles. Bull. Mém. Soc. d’Anthropol. Paris 19, 149e167. (CENIEH, the Institut Catalá de Paleoecología Humana i Evolució Bermúdez de Castro, J.M., Martinún-Torres, M., Prado, L., Gómez-Robles, A., Rosell, J., Social (IPHES) and LCHES-University of Cambridge. Special thanks López-Polín, L., Arsuaga, J.L., Carbonell, E., 2010. New immature hominin fossil fi from European Lower Pleistocene shows the earliest evidence of a modern to Aimara for her comments, support and help with the gures. human dental development pattern. Proc. Nat. Acad. Sci. U.S.A. 107, Thanks to R.G. Franciscus, K.L. Eaves-Johnson, J.C. Ohman, A. Bart- 11739e11744. siokas, S.E. Churchill, J. Ríos, A. Gómez-Robles, M. Martinón, J. Bermúdez de Castro, J.M., Pérez-González, A., Martinón-Torres, M., Gómez-Robles, A., Rodríguez, L. Prado, A. Bonmatí, I. Martínez and J. Tardy for fruitful Rosell, J., Prado, L., Sarmiento, S., Carbonell, E., 2008. A new early Pleistocene hominin mandible from Atapuerca-TD6, Spain. J. Hum. Evol. 55, 729e735. discussion. F. Gracia has kindly revised the English on a previous Bischoff, J.L., Shamp, D.D., Aramburu, A., Arsuaga, J.L., Carbonell, E., Bermúdez de version. R. Quam has revised the English and provided helpful Castro, J.M., 2003. The Sima de los Huesos hominids date to beyond U/Th > comments. 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