The costal skeleton of Homo antecessor: preliminary results

Journal of Human Evolution 59 (2010) 620e640 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol 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 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 b a r t i c l e i n f o a b s t r a c t Article history: Received 23 February 2010 Accepted 14 July 2010 The Lower Pleistocene TD6 level at the Gran Dolina site in the Sierra de Atapuerca (Burgos, Spain) has yielded nine ribs that represent a minimum of three individuals of the species, Homo antecessor. We 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 with other fossil hominins and with modern comparative samples. The costal elements recovered to date from the TD6 level at Gran Dolina can neither confirm nor reject the hypothesis that H. antecessor had a large thorax, similar to that of Neandertals. However, the fragmentary evidence of the H. antecessor thoracic skeleton is not inconsistent with this suggestion based on other skeletal elements, such as 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. Keywords: Ribs TD6 Lower Pleistocene Gran Dolina-TD6 Thorax Introduction The recent discovery of a human mandible dated to c. 1.1e1.2 Ma at the Sima del Elefante site (Sierra de Atapuerca, Burgos, Spain) has cemented the new paradigm of a long human occupation of Europe (Carbonell et al., 2008). Within this paradigm shift, another site from the Sierra de Atapuerca, Gran Dolina, has played a key role and the recovery of human remains from the TD6 level has been instrumental in this process. The first human remains from Gran Dolina-TD6 level were recovered in 1994, in a stratigraphic test pit of about 7 m2 (Carbonell et al., 1995; for a complete and detailed history of the findings see Carbonell et al., 1999a; Bermúdez de Castro et al., 2006, 2008). Thirty human fossils were found * Corresponding author. E-mail address: [email protected] (A. Gómez-Olivencia). 0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.07.023 together with abundant lithics and faunal remains. In the 1995 field season, this site yielded an additional 60 new human fossils as well as more lithic and faunal remains. This increase in the hypodigm revealed a unique combination of morphological traits that led Bermúdez de Castro et al. (1997) to propose a new species for this human fossil assemblage, Homo antecessor. The TD6 level is 2e2.5 m thick and is composed of clastic flows that coarsens upwards with very little clay matrix (Parés and PérezGonzález, 1999). The human remains from TD6 were first thought to derive from a single horizon within the TD6 level (the “Aurora Stratum”). However, new analysis and excavations have revealed that they derive from two (Canals et al., 2003) or even three 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 modifications are those produced by other humans in the form of A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 Figure 1. ATD6-251 rib in situ during excavation. Note the diagenetic breakages (arrows). Photo courtesy of Javier Trueba (Madrid Scientific Films). cut marks, percussion pits, etc. The pattern of these modifications is similar to that of other faunal remains at the site and indicates that these humans were processed for meat by a similar butchering process (Fernández-Jalvo et al., 1996, 1999; Díez et al., 1999). Numerous publications have been devoted to the study of the TD6 human fossil remains. The cranial, mandibular and dental remains have been studied by Arsuaga et al. (1999b, 2001), Bermúdez de Castro et al. (1999a,b, 2006, 2008), Rosas and Bermúdez de Castro (1999), Bermúdez de Castro and Sarmiento (2001), Carbonell et al. (2005). The postcranial remains have been studied by Carretero et al. (1999, 2001) and Lorenzo et al. (1999). The faunal remains found in the TD6 level encompass large herbivores (Made, 1999, 2001), carnivores (García and Arsuaga, 1999), birds (Sánchez-Marco, 1999), micromammals (Cuenca-Bescós et al., 1999; Cuenca-Bescós, 2002; López-Antoñanzas and Cuenca-Bescós, 2002), and small amphibians and reptiles (Blain et al., 2009). The lithic remains are attributed to the Oldowan tradition (Carbonell et al., 1999b) and were used for butchery and wood-working (Márquez et al., 2001). The magnetostratigraphic study of the Gran Dolina sequence has located the Matuyama Chron Boundary in level TD7, indicating that the TD6 level is older than 780 ka (Parés and Pérez-González, 1995, 1999). Uranium series and electronic spin resonance (ESR) techniques yielded a date of between 780 and 857 ka (Falguères et al., 1999, 2001). The paleoenvironmental data from pollen and from quantitative studies of amphibians and squamates (scaled reptiles) show that the upper part of the TD6 level was deposited during a humid and relatively warm period (García-Antón, 1995; Blain et al., 2009) that Bermúdez de Castro et al. (2008) relate to marine isotope stage (MIS) 19 or 21. However, new thermoluminescence (TL) and infrared-stimulated-luminescence (IRSL) dating 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 humid and warm interglacial period (Berger et al., 2008). The phylogenetic position of Homo antecessor1 continues to be debated, and conflicting hypotheses have been suggested since their discovery. Here, we will briefly summarize the most important publications (in our view) regarding this matter. Bermúdez de Castro 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 this species (Manzi et al., 2001). 621 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 chronological 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 lithic technology (see also Carbonell et al., 1999c). The morphology 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 continuity between them. However, the absence of Neandertal derived traits in the mandible of H. antecessor suggests the opposite (Carbonell et al., 2005). For these authors, H. antecessor might be more closely related to the Chinese populations of the late Lower and early Middle Pleistocene, represented at the sites of Nanjing and Zhoukoudian (Carbonell et al., 2005). At the same time, direct comparison of the dentition and mandibular remains of TD6 with those of Tighennif (Algeria) reveal important differences between these hominins (Bermúdez de Castro et al., 2007). Martinón-Torres et al. (2007) have recently defined a Eurasian dental pattern that differs from African hominins, and proposed that Asia may have played a major role in the hominin colonization of Europe. The debate regarding evolutionary continuity between H. antecessor and the Neandertal evolutionary lineage (H. heidelbergensiseH. neanderthalensis) was still open in the description of the most recently found fossils from Gran DolinaTD6 (Bermúdez de Castro et al., 2008; Gómez-Robles, 2010). More recently, Dennell et al. (2010, submitted for publication) have proposed that H. antecessor is not the common ancestor of H. sapiens and H. neanderthalensis. Rather, the similarities between H. antecessor and Neandertals would derive from a common ancestor. More specifically, these authors propose that there was a central area of dispersals of Eurasia (CADE), located in southwest Asia from which different populations would have entered Europe. One of these hominin dispersal events from the CADE to Europe led to a speciation event by 1.2 Ma, giving rise to H. antecessor. Subsequent dispersal event of H. heidelbergensis, could have replaced (or may have interbred) with some remnant populations of H. antecessor. Background and objectives Bermúdez de Castro et al. (1997) cite the presence of eight human ribs among the remains recovered in the 1995 field season. In this inventory, these authors provided the side of all of the costal remains but only the positions of the first (ATD6-108) and second (ATD6-79) ribs were anatomically determined. The postcranial 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 2 The latest dating of the Sima de los Huesos human fossils yielded an average 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 ATD6-39 ATD6-66 ATD6-79 ATD6-85 ATD6-88 ATD6-89þ206 ATD6-97 ATD6-108 ATD6-251 Side L L R R R L L R R Initial anatomical positiona Revised anatomical positionb 10 (9?) 3e4 2 9 (8e10) 4e5 7 (6?) 10 (11?) 1 10 (9-11) 10 3e4 2 9 (8e10) 4e5 7 1 Surface modificationsc Anatomical region Head C Neck Tubercle Shaft Posterior angle Shaft Sternal end Cutmarks Percussion pits C C N/A C C C C N/A C C C N/A C C C C N/A C C C X X P Cd P C C P C C e C N/A P P P C C P C Figures Peeling X X C e P C e e X 9 8 6 and 7 13 8 9 9 3 and 4 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 position was only determined for the first and second ribs. All of the costal remains were illustrated in a figure in cranial view but no metrical study was performed at that time (Carretero et al., 1999). The present contribution presents a more complete and detailed analysis of these costal remains. Work to homogenize the exposed 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 remains, including a rib (ATD6-97, found in 2004,) which is described here for the first time. The specific objectives of this paper are to provide an up-to-date inventory and morphological description of the human costal remains of the TD6 level, housed at the Centro Nacional de Investigación sobre la Evolución Humana (CENIEH). This includes determination of the anatomical position and age at death for each of the specimens, calculating the minimum number of individuals (MNI) represented within the sample, carrying out a comparative metric analysis of the adult or near adult remains and discussing the possible implications of the results. Materials This study includes the eight ribs recovered in the 1995 field season (illustrated in Carretero et al., 1999) and one rib (ATD6-97) recovered in the 2004 field season at Gran Dolina-TD6 level (Sierra 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 M? 1R M M 1L 1-10 (R and L) Krapina (n ¼ 5)f La Chapelle-aux-Saintsg Shanidar 3h ? M M Tabun C1i F 1R (n ¼ 3), 1L (n ¼ 2) 10 (R and L) 3R, 4R, 5R, 5L, 6R, 7R, 8R, 8L, 9R, 9L, 10R 2L, 6R, 6L,7R, 7L, 8R, 8L, 9R, 9L, 10L H. heidelbergensis (Sima de los Huesos) Co1(1L)c H. neanderthalensis Amud 1d Kebara 2d Fossil H. sapiens Ohalo 2d Recent H. sapiens EuroAmerican (n ¼ 26) j EuroAmerican (n ¼ 6)k EuroAmerican (n ¼ 35)j Gómez-Olivencia, 2009 175 166 e 162 166 Endo and Kimura, 1970 Arensburg, 1991; Gómez-Olivencia et al., 2009b Radov ci c et al., 1988 Boule, 1911e1913 Franciscus and Churchill, 2002 154 McCown and Keith, 1939 Hershkovitz et al., 1995 M 1R 173 M M F 1-10 (R); 4L 1-10 (R); 4L 1-10 (R); 4L 169.9  8.1 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). 160.7  6.0 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 623 Table 3 Measurement definitions. Variable Description 0a 0b 0c PrL PrExA PrExAVT 0d 1a PrInA TVC 1b HVC Preserved length Preserved external arc Preserved external arc ventral to the tubercle Preserved internal arc Tuberculo-ventral chorda Head-ventral chord 2a TVA Tuberculo-ventral arca 2b HVA Head-ventral arca 3 TVS 4a HCCD 5a TNL Tuberculo-ventral subtense Head cranio-caudal diameter Total neck length 6 NMnCCD 7 NTh Neck minimum craniocaudal diameter Neck thickness 8 ATH Articular tubercle heightb 9 ATW Articular tubercle widthb 10b TID2 11b PAC2 Tubercle-iliocostal line distance 2c Posterior angle chord 2 12b PAS2 Posterior angle subtense 2 13 PA Posterior angle 14 THD 15 DSMxD 16 DSMnD 17 SMxD Tubercle horizontal diameter Shaft maximum diameter at dorsal end Shaft minimum diameter at dorsal end Shaft maximum diameter at posterior angleb 18 SMnD Shaft minimum diameter at posterior angleb 19 MMxD Mid-shaft maximum diameterb 20 MMnD Mid-shaft minimum diameterb 23 SEMxD 24 SEMnD Sternal end maximum diameterd Sternal end minimum diameterd Maximum straight length of the rib fragment. Ribs 1e12. Maximum external arc length of the rib fragment. Ribs 1e12. Maximum external arc length of the rib fragment ventral from the lateral end of the articular surface of the tubercle. Ribs one to nine. Maximum internal arc length of the rib fragment. Ribs 1e12. Straight line distance between the dorsal-most margin of the articular tubercle to the ventral-most point of the sternal end of the rib. Ribs 1e9. 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. 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. 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. Perpendicular distance from TVC to the lateral-most extent of the shaft of the rib. Ribs 2e9. Maximum diameter in approximate cranio-caudal direction of the articular surface of the head. Ribs 1e12. Straight line distance between the lateral (sternal)-most margin of the articular tubercle to the medial(vertebral)-most point of the head. Ribs 1e9. Minimum reading of the cranio-caudal dimension of the neck, measured perpendicular to the long axis of the neck. Ribs 1e10. Measured at the mid part of the neck. Minimum diameter from internal to external surface of the rib. Ribs 1e10. Maximum cranio-caudal diameter of the articular tubercle with the rib positioned in approximate anatomical position. Ribs 1e9. Maximum width of the articular tubercle with the rib positioned in approximate anatomical position. Ribs 1e9. Straight line distance from the medial (vertebral) end of the articular tubercle to the furthest extent of the iliocostal line. Ribs 3e9. 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. 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. Angle between the TID2 and the line of the same distance used to determine the PAC2 measurement. Ribs 3e9. Maximum diameter from the internal surface of the rib to the further extent of the articular tubercle. Ribs 1 to 2. Measured between the tubercle and the posterior angle of the rib. Ribs 3e12. Measured between the tubercle and the posterior angle of the rib. Ribs 3e12. Measured at the posterior angle of the ribs. In all cases, the calipers are oriented for 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. Measured at the posterior angle of the ribs. In all cases, the calipers are oriented for 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. Measured at the mid-shaft, maximum diameter (from internal to external surface in 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. Measured at the mid-shaft, minimum diameter (approx. cranio-caudal in ribs 1 to 2 and 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. Measured at the sternal end. Maximum diameter. In ribs 1 to 2, is approximately horizontal. Ribs 1e12. Measured at the sternal end. Minimum diameter. In ribs 1 to 2, is approximately 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 abovementioned criteria, as well as complete rib sets from the osteological 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) first rib. Ribs ossify from a primary center of ossification and there may be three secondary centers of ossification: the head, the tubercle and the nonarticular tubercle. The presence of an articular tubercle depends on the articulation of the ribs with the transverse processes of the vertebra and therefore, lower ribs lack this tubercle (Scheuer and Black, 2000). We have quantified the maturation stage of the TD6 ribs using the scoring system developed by Ríos and Cardoso (2009). The epiphyses are scored following a three-stage scale: (1) no union; (2) partial union; (3) completed union. From these scorings, it is possible to provide an age range (see Ríos and Cardoso, 2009: their tables 6e8), taking into consideration three factors. First, there are significant sex differences in rib maturation: females generally show advanced union of all three epiphyses when compared with males (Ríos and Cardoso, 2009). Second, since the TD6 hominins had a shorter period of dental growth (Ramírez Rozzi and Bermúdez de Castro, 2004) and by inference, somatic development (Smith, 1991), we could be slightly overestimating the ages at death (see Dean and Smith (2009) for age disjunction between dental and skeletal ages for KNM-WT 15000). Third, if we assume that these rib remains are derived from the ten individuals For comparative purposes, we have chosen a EuroAmerican sample (Hamann-Todd collection), representing a population that inhabited similar latitudes to those of the Sierra de Atapuerca, and that had a stature similar to that estimated for H. antecessor (between 170.9 and 174.5 cm, depending on the bone used to perform the estimation; see Carretero et al., 1999; Lorenzo et al., 1999). The comparative fossil human sample represents three different species of Homo. We have studied the original specimens of Ohalo 2 (Upper Paleolithic H. sapiens), the Neandertal specimens of Amud 1, La Chapelle-aux-Saints, Kebara 2, Krapina, Shanidar 3, Tabun C1 and a cast of KNM-WT 15000 (Homo ergaster) (See Table 2 for details). Methods Determination of side and anatomical position Siding of ribs as well as sequencing of “atypical” ribs (ribs 1, 2, 10e12) is straightforward. However, the sequencing of “typical” Table 4 Epiphyseal scoring and age at death assessment of the TD6 ribs. Label ATD6-39 ATD6-66 ATD6-79 ATD6-85 ATD6-88 ATD6-89þ206 ATD6-97 ATD6-108 ATD6-251 Side L L R R R L L R R Revised anatomical position 10 3e4 2 9 (8e10) 4e5 7 1 Epiphyseal scoringa Age-at-death Head epiphysis Articular tubercle epiphysis Nonarticular tubercle epiphysis e e e e 3 e e e e 3 3 3 e 3 3 X 3 e X 3? 3 e 3 3 X 3 e Adolescenteyoung Young adult Adolescenteyoung Adolescenteyoung Young adult Adolescenteyoung Subadult Adolescenteyoung Subadult adult adult adult? adult adult 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). 1 ¼ 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. represented by the dental remains in TD6 level, we would have a maximum age at death for the costal elements of 18 years (Hominid 4) or “young adult” (Hominid 10) (Bermúdez de Castro et al., 2006, 2008). However, some of the ribs (ATD6-85, ATD6-97 and ATD6-251) do not preserve the anatomical regions necessary to evaluate the fusion of the head, articular and nonarticular tubercles. In these cases, we provide rough age at death estimates based on surface porosity and muscular scar rugosity (see below). Osteometrics and statistical analysis Metric analysis of the H. antecessor ribs allows us to corroborate and refine the anatomical positions made previously based on morphological considerations and compare the metric dimensions in the TD6 specimens with other fossil and recent humans. We used standard anthropometric techniques and instruments to take all measurements (Table 3; Fig. 2) (see also Franciscus and Churchill, 2002: their Fig. 3; Owers and Pastor, 2005: their Fig. 1). Univariate comparative analysis was performed on all of the variables measured using z-scores. Z-score values beyond 1.96 and 2.576 SD from the mean would be significant at p < 0.05 and p < 0.01 respectively (Sokal and Rohlf, 1981). We have also used bivariate plots to better characterize the most complete ribs. The curvature of the rib has been studied by analyzing the relationships between the arc variables (TVA and HVA) and the chord variables (TVC and HVC), and the relationship between the tuberculo-ventral chord (TVC) and the tuberculo-ventral subtense (TVS) (see Table 3 for measurement definitions). High values of the arc variables relative to chord variables indicate curved ribs. High values of tuberculo-ventral subtense (TVS) relative to tuberculo-ventral chord (TVC) would also indicate curved ribs. Anatomical position was assessed by analyzing the relationship between the tubercleiliocostal line distance 2 (TID2) and tuberculo-ventral arc (TVA). We are aware of the limitations of the metrical study performed on these isolated ribs. The postcranial remains of H. antecessor are TD6 costal remains e minimum number of individuals (MNI) There are ten labelled fragments that represent nine ribs attributed to H. antecessor (see below and Table 1). In Table 1, we include two columns for the anatomical determination of the ribs. The first column shows the results of the morphological study. The second column shows the conjoined results of the morphological and the metrical studies. In this table, we have included the surface modifications recorded by Fernández-Jalvo et al. (1999). The results of the age at death study are summarized in Table 4 and discussed in the description of each of the ribs (see below). All the ribs are represented in cranial and caudal views in the figures. Based on size and age at death compatibilities, ATD6-66 and ATD6-88 likely belong to the same individual. At the same time, based on size, age at death and coherent degree of development of the insertion for the serrati muscles, ATD6-108 (1R) and ATD6-79 (2R) likely belong to the same individual. Regarding the MNI represented in the TD6 sample, there are three ribs that are likely tenth ribs: ATD6-39 (adolescenteyoung adult), ATD6-97 (younger immature) and ATD6-251 (older immatureeadolescent). ATD6-39 and ATD6-97 are both from the left side but show different age at death, thus representing different individuals. ATD6-251 is from the right side and represents an immature individual. However, it would be an older individual than ATD6-97 and thus likely represents a third individual (Table 4). The remaining ribs could represent the same individual as ATD6-39, so they do not represent additional individuals. Based on this analysis, a minimum of three individuals (MNI ¼ 3) are represented among the TD6 costal remains. ATD6-108 (right first rib) (Fig. 3) ATD6-108 is a first rib from the right side that preserves approximately half of the neck (11.4 mm), the tubercle and the shaft of the rib including the sternal end (Fig. 3). However, the shaft of 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 groove for the subclavian artery and the brachial plexus is not present, but the dorsal-most half of the sternal end is preserved. This fossil was recovered in five fragments, four of which articulate well with one another. The fifth fragment represents the neck and half of the articular tubercle. A slight separation is visible in the cranial aspect, but this fragment refits perfectly with the rest of the rib on its caudal aspect. The three fragments that correspond to the ventral half of the rib are somehow cracked into minor pieces. While ATD6-108 does not preserve the head, the articular tubercle is completely fused and shows a slight osteophytic rim on its caudal border (maximum development of 0.5 mm). Following Ríos and Cardoso (2009), this gives us a minimum age of 14 years at the time of death, indicating that this specimen represents an adolescent or young adult. In its overall dimensions, this rib is larger than both Kebara 2 and the mean values of our modern adult comparative sample (Table 6). Ventral to the articular tubercle and parallel to the lateral border of the shaft, ATD6-108 shows a very well-developed ridge with a rough surface that represents the insertion point of the M. serratus anterior muscle. The dimensions of this ridge are ca. 31 mm in length, a mediolateral width of 5.8 mm and a maximum craniocaudal thickness of 7.6 mm. The considerable development of this ridge is related to a great development of M. serratus anterior. The first rib of KNM-WT 15000 shows a slight roughness in the same place, but neither KNM-WT 15000 nor Kebara 2 show this ridge (see Fig. 4). Finally, the scalenus tubercle, the insertion point to the M. scalenus anterior muscle, is present in ATD6-108 but is not as protruding as in the Kebara 2 Neandertal. Metrically, ATD6-108 displays a significantly smaller minimum diameter of the sternal end (SEMnD) compared with the modern male comparative sample (Tables 5 and 6). The curvature of this rib is similar to that of the H. heidelbergensis first rib from the Sima de los Huesos (Co1(1L)), but higher than the male Neandertal of Kebara 2 and within the lower limits of the modern human comparative samples (see Fig. 5). ATD6-79 (right second rib) (Fig. 6) ATD6-79 is a second rib from the right side that preserves approximately half of the length of the neck (9.8 mm), the tubercle and most of the shaft (Fig. 4). This rib consists of one large fragment that preserves the neck, the tubercle and a large part of the shaft, including the very well-developed attachment for the M. serratus anterior and 12 smaller fragments that represent a portion of the shaft that displays post mortem crushing in the cranio-caudal direction. This rib does not preserve the head. However the articular and nonarticular tubercles are completely fused. Following Ríos and Cardoso (2009), this suggests a minimum age of 12 years at the time of death. Based on size, age at death and coherent degree of development of the insertion for the serrati muscles, ATD6-108 (1R) and ATD6-79 (2R) are likely to belong to the same individual. This association would rise the minimum age at death of ATD6-79 to 14 years, suggesting that this rib belonged to an adolescent or young adult. The overall dimensions of this rib are similar in size to the mean values of our modern adult comparative samples. We have estimated the tuberculo-ventral chord (TVC) of this specimen as longer than 130 mm, through direct comparison with the R2 of the Kebara 2 Neandertal individual (Table 5, Fig. 7). This minimum value is similar to the modern male comparative sample and one standard deviation above our modern female comparative sample (Table 7). Metrically, ATD6-79 stands out for its significantly large tubercle horizontal diameter (THD) and mid-shaft maximum 627 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 Table 5 Raw dimensions (mm) of the Gran Dolina-TD6 ribs.a Variable 0a 0b 0c 0d 1a 1b 2a 2b 3 4a 5a 6 7 8 9 10b 11b 12b 13 14 15 16 17 18 19 20 23 24 a b Preserved length (PrL) Preserved external arc (PrExA) Preserved external arc ventral to the tubercle (PrExAVT) Preserved internal arc (PrInA) Tuberculo-ventral chord (TVC) Head-ventral chord (HVC) Tuberculo-ventral arc (TVA) Head-ventral arc (HVA) Tuberculo-ventral subtense (TVS) Head cranio-caudal diameter (HCCD) Total neck length (TNL) Neck minimum cranio-caudal diameter (NMnCCD) Neck thickness (NTh) Articular tubercle height (ATH) Articular tubercle width (ATW) Tubercle-iliocostal line distance 2 (TID2) Posterior angle chord 2 (PAC2) Posterior angle subtense 2 (PAS2) Posterior angle (PA) Tubercle horizontal diameter (THD) Shaft maximum diameter at dorsal end (DSMxD) Shaft minimum diameter at dorsal end (DSMnD) Shaft maximum diameter at posterior angle (SMxD) Shaft minimum diameter at posterior angle (SMnD) Mid-shaft maximum diameter (MMxD) Mid-shaft minimum diameter (MMnD) Sternal end maximum diameter (SEMxD) Sternal end minimum diameter (SEMnD) 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 78.1 85.0 55.0 48.2 53.0 49.0 147.0 (>130.0) e 88.0 34.0 e e e e e 123.5 182.0 162.0 (90.0) e (107.0) e 17.9 15.4 3.3b 156.0 182.0 e 171.0 225.0 215.0 167.0 209.0 e >245.0 e (190.0) (155.0e160.0) (192.0e198.0) (172.0e175.0) (237.0e240.0) e e (273.0) 9.1 32.7 7.1 4.3 7.0 10.3 224.0 e 275.0 e 68.0 189.0 182.0 182.0 7.8 8.4 16.4 4.1 6.4 8.6 35.3 7.0 (52.0) 95.0 (21.2) (129.4) e 7.4 e 6.9 e 6.8 8.0 7.7 8.1 9.7 9.7 10.7 7.9 7.3 8.5 12.8 8.5b 5.9b 11.4 6.3 (18.7) 8.3 e e 9.3 7.1 8.6 6.3 17.5 16.2 11.1 16.5 7.4 8.3 5.7 7.4 (14.7) (7.0) 15.3 7.6 15.4 9.5 6.6 14.5 6.7 Values in parentheses are estimated. Measured in cranio-caudal direction. diameter (MMxD). In both of these dimensions, ATD6-79 is significantly larger than our modern female sample, while compared with males only the THD is significantly different. The large dimension of MMxD is related to the well-developed insertion for the M. serratus anterior muscle, which rotates the scapula for abduction and flexion of the arm and protracts the scapula (Stone and Stone, 1999). Second ribs from the Sima de los Huesos and the Neandertal individual of Tabun C1 show a similar pattern, while Kebara 2 shows a cranio-caudally low and mediolaterally wide shaft (Gómez-Olivencia et al., 2009b). ATD6-66 (left third or forth rib) and ATD6-88 (right forth or fifth rib) (Fig. 8) Based on size and age at death compatibilities, it is likely that ATD6-66 and ATD6-88 belonged to the same individual. ATD6-66 partially preserves both articular and nonarticular tubercles as well as the posterior angle, while ATD6-88 preserves the head, neck, both articular and nonarticular tubercles, the posterior angle and approximately 25 mm of the shaft (Fig. 8). This latter specimen consists of two fragments that rejoin at the posterior angle. It has lost a slight bone chip (2.3  4.3 mm) on the caudal aspect of the fracture line. In addition, slight exposure (4.9  4.4 mm) of the trabecular bone is visible in the cranial aspect of the union between the head and the neck. ATD6-66 is from the left side and ATD6-88 is from the right side. While they are very similar, ATD6-88 has a longer posterior angle and a slightly larger space between the posterior angle and the tubercle (larger TID2 value). This suggests that ATD6-66 is a more cranial rib than ATD6-88. ATD6-88 is a third, forth or fifth rib based on the length and narrow aspect of the neck and the small distance between the tubercle and the iliocostal line. However, the vertical orientation of the surface of the shaft between the tubercle and the posterior angle points towards this rib being a forth or fifth element (see below). Thus ATD6-66 likely represents a left third or forth rib and ATD6-88 likely represents a right forth or fifth rib. In ATD6-88, the articular and nonarticular tubercles are completely fused. In addition, the epiphysis of its head is fused, although the epiphysis does not cover the whole metaphyseal surface and the metaphyseal line is still present. This suggests a minimum age of 18 years at the time of death (Ríos and Cardoso, 2009). However, the presence of a metaphyseal line is not uncommon even in middle-aged adult modern human individuals (Ríos and Cardoso, 2009). Both articular and nonarticular tubercles of ATD6-66 are fused, and the age at death of this specimen is consistent with that of ATD6-88. Thus, these two specimens represent a young adult individual. The metric dimensions of ATD6-88 and ATD6-66 are provided in Tables 5 and 8. The z-score analysis of these individuals has been conducted together due to their similar anatomical position and the fact that they likely belonged to the same individual. The tuberculo-iliocostalis distance 2 (TID2) in ATD6-88 is above the range of the third ribs of our modern male comparative sample and larger than the third rib of Kebara 2, which supports the diagnosis of this specimen as a forth or fifth rib. These ribs are notable for showing a dorsal end of the shaft that is weakly developed in the cranio-caudal direction and well-developed mediolaterally (Tables 9 and 10). Variable ATD6-108 EuroAmerican males (1R) EuroAmerican females (1R) Amud 1 Kebara 2 Z-score Z-score 1L 1R 1a TVC (90.0) (0.98) 2a TVA (107.0) (0.29) 6 NMNCCD 14 1.14 THD 17.9 0.50 19 MMxD 15.4 1.54 20 MMnDb 3.3 1.37 24 SEMnDb 5.9 L2.31* a b 84.68  5.42 (74.8e94.5) n ¼ 30 104.24  9.35 (85.0e126.0) n ¼ 30 4.98  0.59 (3.9e6.1) n ¼ 33 17.08  1.63 (12.9e19.8 n ¼ 33 19.55  2.70 (14.4e23.9) n ¼ 32 4.21  0.67 (2.9e5.3) n ¼ 32 9.44  1.53 (7.3e12.7) n ¼ 30 (1.54) (1.10) 0.39 1.40 0.72 0.01 1.54 Summary statistics 79.96  6.50 (65.7e99.6) n ¼ 31 97.77  8.36 (79.0e121.0) n ¼ 31 4.06  0.61 (2.8e5.4) n ¼ 32 15.36  1.82 (11.8e18.7) n ¼ 32 16.85  2.02 (12.8e20.9) n ¼ 33 3.30  0.50 (2.2e4.8) n ¼ 33 7.57  1.09 (5.5e9.6) n ¼ 31 1L 85.7 82.7 99.0 (96.0) Krapina 117.2 Krapina 117.3 Krapina 118.2 Krapina 117.1 Krapina 118.4 1R 1R 1R 1L 1L 15.4 4.7 >19.0 19.8 19.4 17.1 (16.5) 15.2 (20.7) 20.5 14.0 13.8 13.2 15.6 3.5 4.3 4.0 3.4 4.2 3.3 3.5 8.9 8.4 9.3 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. Measured in cranio-caudal direction. Figure 6. ATD6-79 (2R) in cranial (a) and caudal (b) views. Scale bar ¼ 5 cm. ATD6-89þ206 (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 well together, although some bone chips have been lost in some of the fracture lines. The general aspect and the degree of torsion of the shaft and sternal end suggest that ATD6-89þ206 is a rib from the cranial part of the rib cage (third to a seventh rib). The distance between the tubercle and the iliocostal line reduces the possibilities to a sixth or seventh rib. The external aspect of the shaft at the posterior angle is more consistent with a sixth rib while the orientation of the sternal end of the shaft is more similar to a seventh rib rather than to a sixth. This rib does not preserve the head. However, the articular and nonarticular tubercles are completely fused, suggesting a minimum age of 11 years (Ríos and Cardoso, 2009). The general size of this rib Figure 7. Cranial view of the second rib of (a) Kebara 2, (b) Tabun C1 (mirrored image), and (c) ATD6-79. Scale bar ¼ 5 cm. A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 4.3 Summary statistics 628 Table 6 Z-score valuesa 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. 629 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 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 (>130.0) EuroAmerican males (2R) EuroAmerican females (2R) Kebara 2 Z-scores Summary statistics Z-scores Summary statistics 2R (>0.06) 129.44  9.16 (110.7e148.0) n ¼ 27 12.12  1.59 (8.5e15.2) n ¼ 30 15.87  1.90 (11.6e20.0) n ¼ 29 6.18  1.45 (3.7e9.3) n ¼ 29 (>1.01) 122.31  7.60 (106.4e136.5) n ¼ 27 10.07  1.42 (6.6e12.3) n ¼ 32 13.70  1.63 (10.6e17.3) n ¼ 32 5.30  0.97 (3.2e7.4) n ¼ 32 137,2 1a TVC 14 THD 16.4 2.68**z 19 MMxD 12.8 1.61 20 MMnDb 8.5 1.60 4.47**z 0.55 3.30**z Tabun C1 2L 2L 14,7 17,2 8,7 4,8 4,8 7,6 14,3 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 z 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 samples and we consider that this rib belonged to an adolescent or young adult individual. In general dimensions (TVC and TVA), ATD6-89þ206 is similar to the seventh rib of the Tabun C1 female Neandertal and smaller than the male Neandertal individuals (Tables 5, 11 and 12). If this rib belonged to a male individual, it would only stand out by its significantly small values in the shaft maximum diameter at dorsal end (DSMxD). If this was a seventh rib belonging to a female individual, it would stand out for having a cranio-caudally low and mediolaterally thick dorsal end of the shaft as well as a large maximum diameter of the sternal end. Finally, this specimen also shows a moderately large distance between the tubercle and the iliocostal line (TID2), which is 1.52 SD above our modern female comparative sample (Table 12). To better assess the anatomical position of this rib, we have performed a bivariate study between the tubercle-iliocostal line distance 2 (TID2) and tuberculo-ventral arc (TVA). Modern and fossil seventh ribs show larger TID2 than sixth ribs, while they show similar values of TVA. ATD6-89þ206 is close to the male centroid of the seventh rib and to the seventh rib of the Neandertal Tabun C1 (Fig. 10), and thus we consider it more likely it to be a seventh rib. The curvature of this rib has been assessed by analyzing the relationships between the tuberculo-ventral subtense (TVS) and the tuberculo-ventral chord (TVC), and the relationship between the tuberculo-ventral chord (TVC) and the tuberculo-ventral arc (TVA) (Figs. 11 and 12). ATD6-89þ209 shows a curvature similar to modern adult seventh ribs. Unfortunately, the two Neandertal individuals that preserve the seventh ribs (i.e., Tabun C1 and Kebara 2) show evidence of taphonomic distortion (Gómez-Olivencia et al., 2009b) and cannot be compared metrically with ATD6-89þ206. ATD6-85 (right eighth to tenth ribs) (Fig. 13) ATD6-85 is from the right side and is comprised of nine fragments that preserve nearly all the shaft, from a point located dorsal to the posterior angle to a cranio-caudal narrowing of the shaft located close to the sternal end (Fig. 13). In these fractures, this specimen has lost small bone chips; the largest (10.7  5.5 mm) being the one located in the cranial aspect of the rib shaft, at the posterior angle. ATD6-85 most likely represents a ninth rib. However, due to its incompleteness the possibility that it represents an eighth or a tenth rib cannot be ruled out. The ventral-most preserved part of the rib shaft is more vertical in ATD6-39 (see below) than in ATD6-85. Additionally, the costal groove is more marked and longer in this rib that in ATD6-39. These two features make it more likely that this rib is a ninth rather than a tenth rib. The presence of a cranio-caudal narrowing in the ventral (sternal) third of the rib shaft is also more consistent with ATD6-85 being a ninth rib rather than an eighth rib. 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) Figure 8. Cranial and caudal views of (a, d) ATD6-88, and (b, c)ATD6-66. Scale bar ¼ 5 cm. 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 been some minor bone lost. We have assessed ATD6-39 as a tenth 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 4a 5a 6 7 10b 15 16 17 18 ATD6-88 HCCD TNL NMnCCD NTh TID2 DSMxD DSMnD SMxD SMnD 9.1 32.7 7.1 4.1 35.3 6.9 8.0 9.7 7.9 EuroAmerican males (Z-scores) EuroAmerican females (Z-scores) 4R 5R 4R L2.46*z 0.79 1.70 0.98 0.00 L2.18* 0.16 0.74 0.55 L2.64**z 0.80 L2.29* 1.51 1.50 L2.56* 0.24 1.31 0.98 ATD6-66 5R 0.85 0.52 1.12 0.39 0.65 1.06 2.81**z 0.17 1.14 1.80z 0.58 1.92z 0.79 0.69 1.74 2.73**z 0.78 0.67 EuroAmerican males (Z-scores) EuroAmerican females (Z-scores) 3R 3R 6.8 7.7 9.7 7.3 1.86 0.13 0.50 1.03 4L L2.02*z 0.19 1.01 1.13 4L 1.43 1.95 0.45 0.53 1.58 1.80 0.06 0.31 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 z are outside the range of our modern comparison samples. the shaft and the cross-sectional morphology at the angle and midshaft. The presence of an articular tubercle in ATD6-39 allows the comparison of this rib with modern and fossil ribs. The large distance between the articular tubercle and the iliocostal line (TID2) indicates that this is a tenth rib (Fig. 14). This rib does not preserve the head. However, the articular tubercle is completely fused, suggesting a minimum age of 12 years at the time of death (Ríos and Cardoso, 2009). The general size of this rib is similar to the mean values of our modern adult comparative samples and we consider it to represent an adolescent or young adult. This rib shows less torsion in the shaft at the posterior angle. The functional significance of this remains unclear but we hypothesize that it could be related to a more horizontal disposition of the rib. Compared with our modern human comparative samples, ATD6-39 has a thick shaft and a large sternal end (Tables 5 and 15). Moreover, if this rib belonged to a female individual, it would stand out for its large general dimensions (TVA and TVC). Compared with Neandertals, ATD6-39 is similar to male individuals and larger than the Tabun C1 female. ATD6-39 stands out for its large sternal end, only comparable with that of La Chapelle-aux-Saints. However, the dimensions of TVA and TVC are slightly smaller than those in the right tenth rib from Kebara 2. In order to assess the curvature of this rib, we have performed a bivariate analysis between the TVC and the TVA (Fig. 15). ATD6-39 is within the upper limit of the 70% equiprobability ellipse for modern adult males due to its large TVA, which means that this rib is slightly more curved than the mean modern male sample. ATD6-97 (left tenth rib) (Fig. 9) ATD6-97 is from the left side and preserves a nearly complete shaft, lacking the head, part of the neck and the sternal end (Fig. 6). ATD6-97 is very fragmentary and the specimen has suffered taphonomic deformation in the middle of the shaft due to crushing. This specimen most likely represents a tenth rib. Morphologically, it is very similar to ATD6-251 and ATD6-39. In contrast with ATD6-39, this rib does not present an articular tubercle. The position of the 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 4a HCCD 5a TNL 6 NMnCCD 7 NTh 10b TID2 15 DSMxD 16 DSMnD 17 SMxD 18 SMnD EuroAmerican females 3R 4R 4L 5R 3R 4R 4L 5R 10.50  1.37 (7.7e13.5) n ¼ 26 34.24  1.79 (29.2e38.5) n ¼ 29 8.61  1.34 (6.3e11.2) n ¼ 29 4.95  0.83 (3.4e6.3) n ¼ 29 29.74  3.03 (22.7e33.8) n ¼ 29 8.71  1.03 (6.2e11.3) n ¼ 29 7.83  1.03 (5.4e10.4) n ¼ 29 10.26  1.14 (7.3e12.2) n ¼ 29 8.37  1.04 (6.1e10.4) n ¼ 28 11.85  1.12 (9.9e14.5) n ¼ 28 34.50  2.29 (29.4e38.4) n ¼ 28 10.02  1.72 (5.3e12.4) n ¼ 29 5.19  1.11 (3.8e9.9) n ¼ 29 35.29  2.91 (29.5e40.5) n ¼ 29 8.90  0.92 (6.9e11.3) n ¼ 29 7.78  1.42 (5.9e13.1) n ¼ 29 10.83  1.54 (7.6e13.8) n ¼ 29 8.74  1.52 (5.9e12.0) n ¼ 29 12.12  1.44 (9.3e15.8) n ¼ 26 34.34  2.36 (29.9e38.5) n ¼ 26 10.93  1.64 (7.1e13.4) n ¼ 26 5.17  0.61 (4.2e7.0) n ¼ 27 36.00  3.22 (29.8e41.1) n ¼ 27 8.83  1.00 (6.7e11.3) n ¼ 27 7.90  1.06 (6.3e9.8) n ¼ 27 11.04  1.32 (8.5e13.3) n ¼ 27 8.63  1.18 (6.4e10.8) n ¼ 27 13.49  1.66 (10.1e17.5) n ¼ 28 34.52  2.27 (29.7e37.8) n ¼ 29 12.01  2.14 (7.7e15.2) n ¼ 29 5.39  0.86 (3.8e7.3) n ¼ 29 40.69  3.58 (32.7e47.2) n ¼ 29 9.56  1.04 (6.9e12.0) n ¼ 29 7.76  0.99 (5.2e9.7) n ¼ 29 12.07  1.80 (8.6e14.8) n ¼ 29 9.17  1.30 (6.6e11.6) n ¼ 29 9.22  1.57 (7.0e12.8) n ¼ 27 31.29  2.09 (26.6e37.0) n ¼ 28 7.49  1.20 (5.4e10.6) n ¼ 29 4.24  0.73 (3.2e7.1) n ¼ 29 27.94  3.23 (22.0e36.0) n ¼ 29 8.02  0.85 (6.4e10.1) n ¼ 29 6.17  0.79 (4.8e8.2) n ¼ 29 9.27  0.97 (6.7e11.7) n ¼ 29 6.66  1.22 (4.6e9.1) n ¼ 29 10.28  1.39 (8.1e13.3) n ¼ 28 31.64  2.04 (27.1e35.2) n ¼ 29 8.56  1.31 (6.2e11.7) n ¼ 30 4.42  0.81 (3.2e7.6) n ¼ 30 33.23  3.18 (29.3e40.1) n ¼ 29 8.01  1.04 (6.2e10.1) n ¼ 30 5.98  0.72 (4.6e7.4) n ¼ 30 9.94  1.44 (7.3e12.7) n ¼ 30 6.91  0.87 (5.4e8.8) n ¼ 30 10.62  1.24 (9.1e13.0) n ¼ 22 31.58  2.28 (27.3e35.4) n ¼ 24 8.47  1.22 (6.5e10.5) n ¼ 23 4.42  0.55 (3.2e5.3) n ¼ 24 31.84  3.03 (26.6e36.9) n ¼ 24 8.19  0.88 (6.3e10.0) n ¼ 24 6.08  0.90 (4.2e7.8) n ¼ 24 9.78  1.29 (7.3e11.9) n ¼ 23 7.01  0.94 (5.1e9.1) n ¼ 24 11.17  1.15 (9.7e14.1) n ¼ 28 31.36  2.28 (26.1e35.9) n ¼ 29 10.63  1.84 (8.1e14.4) n ¼ 29 4.39  0.37 (3.6e5.1) n ¼ 29 37.29  2.90 (29.7e44.7) n ¼ 30 8.52  0.93 (6.9e10.9) n ¼ 29 5.98  0.74 (4.6e8.1) n ¼ 29 11.20  1.93 (8.5e14.9) n ¼ 28 7.24  0.97 (5.8e9.3) n ¼ 29 631 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 Table 10 Measurements (in mm) of the Neandertal comparative sample for ribs 3 to 5. Variable Kebara 2 3R 4a 5a 6 7 10b 15 16 17 18 HCCD TNL NMnCCD NTh TID2 DSMxD DSMnD SMxD SMnD 5.0 32.1 3L Kebara 2 3R 4R 4L Shanidar 3 Kebara 2 4R 5R Shanidar 3 5L 5R 5L 9.6 11.9 6.7 41.7 8.9 9.6 12.1 9.7 9.9 32.9 9.1 4.9 9.7 (15.5) 7.9 Shanidar 3 7.8 11.1 7.2 14.9 7.4 9.2 8.1 9.5 cross-section of the shaft at the posterior angle and at the mid-shaft and the overall size suggest that ATD6-97 is a tenth rib. In fact, the orientation of the iliocostal line in external view is similar to modern tenth ribs. Although it is less likely to represent an eleventh rib, we cannot rule out this possibility. This rib does not preserve the head, thus its age at death assessment should be regarded as tentative. The external surface of the rib shaft is porous and the porosity increases towards the sternal end, indicating that the growth process was still ongoing. Thus, this rib likely belonged to an immature individual, younger than ATD6-251 (see below). ATD6-251 (right tenth rib) (Fig. 13) ATD6-251 is from the right side and preserves a nearly complete 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 generally rejoin well with each other, but some taphonomic distortion of the specimen is present in the mid-shaft. There is slight bone loss at all the fracture points. This specimen most likely 44.8 8.7 8.2 16.7 7.6 11.7 8.0 (17.0) 9.6 9.4 (17.7) 9.4 represents a tenth rib. Morphologically, it is very similar to ATD639, but it does not present an articular tubercle. The position of the iliocostal line, the torsion of the shaft and the morphology of the cross-section at the mid-shaft and at the posterior angle indicate that this is a tenth rib, although the possibility that it represents an eleventh rib cannot be entirely ruled out. The articular tubercle is present in the 91% of the ninth ribs of a pooled sex sample of 98 modern human individuals. Thus, its absence in ATD6-251 rules out this specimen representing a ninth rib. The ventral third of the shaft shows a very porous surface, indicating that the growth process was still ongoing and this rib likely belonged to an immature individual. Discussion Anatomical position Metric analysis has been shown to be a useful and complementary 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 6R EuroAmerican females 7R Z-scores 1a TVC 224.0 0.54 2a TVA 275.0 0.54 3 TVS 68.0 0.03 10b TID2 (52.0) (1.00) 11b PAC2 95.0 1.19 12b PAS2 (21.2) (0.27) 13 PA (129.4) (0.29) 15 DSMxD 7.4 L2.58**z 16 DSMnD 8.1 0.32 17 SMxD 10.7 1.30 18 SMnD 8.5 0.75 19 MMxD 11.4 0.35 20 MMnD 6.3 0.95 23 SEMxD (18.7) (1.58) 24 SEMnD 8.3 0.40 Summary statistics 216.28  14.33 (184.5e235.5) n ¼ 26 283.69  16.10 (244.0e305.0) n ¼ 26 68.17  6.21 (55.1e79.6) n ¼ 26 47.32  4.67 (38.2e57.4) n ¼ 29 85.24  8.23 (70.1e103.2) n ¼ 29 20.51  2.59 (15.1e25.2) n ¼ 29 128.49  3.18 (119.7e133.3) n ¼ 29 10.14  1.06 (7.8e12.3) n ¼ 29 7.82  0.88 (5.9e9.3) n ¼ 29 13.35  2.04 (9.9e18.3) n ¼ 29 9.45  1.26 (7.1e12.1) n ¼ 29 12.00  1.71 (9.1e15.3) n ¼ 29 7.10  0.84 (5.7e8.7) n ¼ 29 16.03  1.69 (13.0e20.3) n ¼ 23 8.81  1.25 (7.2e11.3) n ¼ 24 6R Z-scores 0.05 0.56 0.71 (0.01) 0.28 ( 0.99) (0.74) L2.63**z 0.07 1.53 0.92 1.13 0.90 (1.03) 0.34 Summary statistics 223.27  14.87 (189.0e244.8) n ¼ 26 284.56  16.96 (244.0e315.0) n ¼ 26 63.42  6.42 (52.0e84.3) n ¼ 26 51.95  3.90 (42.9e58.0) n ¼ 29 92.96  7.37 (77.0e105.1) n ¼ 29 23.15  1.97 (18.7e26.9) n ¼ 29 126.93  3.34 (121.9e132.3) n ¼ 29 10.57  1.21 (8.8e13.4) n ¼ 29 8.04  0.85 (6.6e10.0) n ¼ 29 13.88  2.08 (9.0e18.3) n ¼ 29 9.64  1.24 (7.7e12.4) n ¼ 29 13.32  1.70 (10.3e17.0) n ¼ 29 7.13  0.92 (5.3e9.0) n ¼ 29 17.01  1.64 (14.5e20.8) n ¼ 25 8.74  1.31 (6.8e11.5) n ¼ 26 7R Z-scores 2.09*z 0.75 0.24 (3.19)**z 3.15**z (1.80) ( 0.32) 1.78 2.83** 0.96 1.09 0.27 0.97 (3.80)**z 1.05 Summary statistics Z-scores 1.46 198.52  12.20 (171.4e218.7) n ¼ 22 266.09  11.89 (242.0e283.0) n ¼ 22 66.69  5.47 (57.5e77.8) n ¼ 23 42.93  2.84 (37.4e47.9) n ¼ 30 78.01  5.39 (66.9e87.8) n ¼ 30 17.86  1.86 (14.4e21.0) n ¼ 30 130.81  4.42 (119.5e137.5) n ¼ 29 9.40  1.12 (7.5e12.5) n ¼ 30 6.21  0.67 (5.2e8.4) n ¼ 30 12.63  2.01 (9.3e17.6) n ¼ 30 7.47  0.95 (6.0e9.3) n ¼ 30 10.98  1.53 (8.3e14.3) n ¼ 30 5.39  0.94 (4.0e7.5) n ¼ 30 13.90  1.26 (11.2e15.5) n ¼ 22 7.44  0.82 (6.2e9.3) n ¼ 21 0.83 1.18 (1.52) 1.59 (0.48) (0.00) L2.49*z 3.30**z 1.34 1.21 0.45 1.11 (2.03)*z 1.22 Summary statistics 206.86  11.76 (179.4e231.0) n ¼ 29 264.55  12.52 (239.0e282.0) n ¼ 29 60.78  6.10 (52.6e74.6) n ¼ 29 47.03  3.28 (40.2e53.7) n ¼ 30 84.95  6.32 (72.1e98.8) n ¼ 30 20.07  2.39 (15.9e24.4) n ¼ 30 129.39  5.51 (116.1e137.8) n ¼ 29 9.67  0.91 (7.6e11.9) n ¼ 30 6.06  0.62 (4.8e7.1) n ¼ 30 12.97  1.69 (9.2e16.6) n ¼ 30 7.19  1.08 (5.3e9.2) n ¼ 30 12.08  1.52 (9.1e15.1) n ¼ 30 5.28  0.92 (3.7e7.2) n ¼ 30 14.59  2.02 (10.2e18.1) n ¼ 23 7.43  0.71 (6.2e8.7) n ¼ 27 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 z are outside the range of our modern comparison samples. Table 12 Measurements (in mm) of the Neandertal comparative sample for ribs 6 to 7. Variable Kebara 2 6R 1a 2a 3 10b 11b 12b 13 15 16 17 18 19 20 23 24 TVC TVA TVS TID2 PAC2 PAS2 PA DSMxD DSMnD SMxD SMnD MMxD MMnD SEMxD SEMnD 6L (18.2) 11.8 Shanidar 3 Tabun C1 6R 6R 6L 11.7 6.7 (12.7) 4.3 (185-190)a 290.0 (87.5)a 47.5 78.4 26.8 136.2 6.9 7.0 (11.3) 6.4 10.6 5.8 14.3 9.8 21.9 (10.0) Values in parentheses are estimated. a These measurements may be affected by taphonomical distortion. Kebara 2 7R 7L Shanidar 3 Tabun C1 7R 7R (340.0) 57.4 103.5 25.7 16.4 11.8 14.5 9.3 56.3 65.0 9.6 8.2 15.1 9.3 (12.5) 9.2 20.2 12.3 11.0 10.1 16.4 9.9 17.0 8.1 13.1 6.0 7L 213.0a 290.0 79.1a 52.7 92.3 25.4 137.2 7.2 7.1 (14.0) 8.1 13.7 8.1 16.6 9.3 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. (3.33)**z (0.45) 1.04 1.19 (2.43)*z (0.82) 0.73 1.84 (2.15)* ( 0.08) 0.04 15.42  1.76 (12.7e19.5) n ¼ 29 7.35  1.20 (5.0e9.5) n ¼ 29 14.85  1.97 (10.8e18.8) n ¼ 29 5.12  0.88 (3.7e7.4) n ¼ 29 1.18 (1.51) ( 0.32) 0.54 0.58 260.50  16.24 (225.0e285.0) n ¼ 23 16.33  2.01 (12.9e20.3) n ¼ 29 7.94  1.00 (5.5e9.9) n ¼ 29 15.28  1.79 (12.4e19.7) n ¼ 29 5.60  0.93 (3.9e7.3) n ¼ 29 (0.74) (7.0) MMnD 20 (0.03) MMxD 19 (14.7) 7.4 SMnD 18 1.09 17.5 SMxD 17 1.19 280.04  15.01 (255.0e307.5) n ¼ 25 15.01  2.09 (9.8e18.7) n ¼ 29 8.72  1.22 (5.9e11.9) n ¼ 29 14.64  1.93 (11.8e18.3) n ¼ 29 6.14  1.16 (3.8e9.0) n ¼ 29 >245.0 TVA 2a 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 z are outside the range of our modern comparison samples. (3.92)**z (0.76) 1.76 1.68 237.61  14.29 (208.0e261.0) n ¼ 23 14.79  2.29 (9.7e19.2) n ¼ 30 6.40  0.96 (4.5e8.7) n ¼ 30 14.01  1.55 (10.9e17.8) n ¼ 30 4.39  0.78 (3.2e6.9) n ¼ 30 256.00  13.49 (232.0e276.0) n ¼ 24 14.00  1.90 (10.1e17.5) n ¼ 30 6.59  1.12 (5.0e9.2) n ¼ 30 13.27  1.74 (8.6e16.1) n ¼ 30 4.55  1.01 (3.0e6.9) n ¼ 30 10R 9R Summary statistics Z-scores 8R 10R 9R Z-scores Summary statistics 8R Z-scores Summary statistics Z-scores Summary statistics EuroAmerican females EuroAmerican males ATD6-85 Variable Table 13 Z-score valuesa for ATD6-85 compared with modern human comparative samples and summary statistics of the modern male and female samples. Z-scores Summary statistics Z-scores Summary statistics 13.99  2.09 (9.7e17.4) n ¼ 30 5.68  0.98 (3.6e8.1) n ¼ 30 13.26  1.90 (9.7e19.1) n ¼ 30 3.80  0.82 (2.6e6.6) n ¼ 30 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 it represents a third rib. In addition, ATD6-39 has been confirmed as it being a tenth rib, and the possibility of representing a ninth rib 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. Thus, the combination of morphological and metric criteria can provide an accurate assessment of the anatomical position of isolated ribs. Thorax size of the TD6 hominins Larson (2007: 182) has hypothesized that “H. antecessor is unlikely to have had the cold climate adaptation of an enlarged chest as do later Neandertals”. This assertion was based on the absence of cold-adapted taxa among the ungulates of TD6 (van der Made, 1999, 2001) and the assumption that the large chest of Neandertals represents a cold adaptation. A recent reassessment of the costal remains from the Kebara 2 male Neandertal individual (Gómez-Olivencia et al., 2009b) has corroborated the hypothesis that H. neanderthalensis had a capacious thorax, as previously proposed by other authors (Franciscus and Churchill, 2002; Weinstein, 2008). Moreover, a shape difference in the thorax of Kebara 2 in comparison with modern humans was also demonstrated. While the uppermost and lowermost ribs of the Kebara 2 individual are similar to modern males, the mid-thorax ribs are significantly larger. Following Churchill (2006), a large chest would better supply the large oxygen demands of a relatively large body and high activity levels, and would have been advantageous in cold climates. It has been argued that this would have been the result of an exaptation rather than cold adaptation per se (Gómez-Olivencia et al., 2009b). Moreover, the large size of the Neandertal thorax was 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., 2009b). Up until the 2007 field season, the Sima de los Huesos Middle Pleistocene site has yielded a total of 503 costal fragments belonging to the species H. heidelbergensis, a taxon which has been argued to be ancestral to H. neanderthalensis (Arsuaga et al., 1993, 1997b). Ongoing efforts at reconstruction and rejoining of these costal fragments have yielded 400 remains belonging to 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 well as the other fragmentary remains suggests that the hominins from Sima de los Huesos also possessed a large thorax (GómezOlivencia, 2009; Gómez-Olivencia et al., 2009a), this observation cannot be confirmed until more complete mid-thoracic ribs are recovered or reconstructed in the future. Regarding the TD6 remains, the only complete mid-thoracic rib of H. antecessor is ATD6-89þ206 (left seventh rib). This specimen is 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 independent elements to assess its sex. The direct application of 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 diagnosis. ATD6-89þ206 belonged to a late adolescenteyoung adult individual. Among the 11 dentally-defined individuals represented in the TD6 level, only four correspond to adolescent or young adults: an adolescent male (Hominid 1: age at death 12.9 years), a young adult male (Hominid 10), an adolescenteyoung adult female (Hominid 7, age at death 16.6 years) and one young 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 8R 2a 17 18 19 20 TVA SMxD SMnD MMxD MMnD 16.8 10.1 (16.1) (8.3) Shanidar 3 8L (325.0) 15.8 10.0 8R Tabun C1 8L 8R Kebara 2 Shanidar 3 Tabun C1 8L 9R 9L 9R 9L 13.2 6.6 11.7 6.4 17.2 8.8 16.1 7.4 18.1 8.8 18.1 9.8 15.0 9.2 15.3 8.5 9R 9L (12.7) (6.0) (13.5) 7.3 13.5 6.0 269.0 16.9 9.8 16.3 8.2 18.4 9.3 (11.8) (5.4) (Carbonell et al., 2005; Bermúdez de Castro et al., 2006, 2008, 2010). Thus, even assuming that the rib remains recovered from TD6 belong to one of the individuals represented by the dental remains, we still cannot reliably infer the sex of this individual. We can, however, explore the implications of ATD6-89þ206 belonging to a male or a female individual. If this rib belonged to a male individual and if we assume that this rib is from an average individual (i.e., is not abnormally small or large), then the thorax size in H. antecessor would appear to be similar to H. sapiens. On the other hand, if ATD6-89þ206 belonged to a female individual, then H. antecessor would show a large thorax similar to that of H. neanderthalensis, which would be consistent with our hypothesis that the large size of the Neandertal thorax is linked to a primitive body bauplan consisting of wide and heavy bodies (GómezOlivencia et al., 2009b). Evidence for heavy-bodied hominins (i.e., large body mass) has been found in the Middle Pleistocene of Africa, Asia and Europe (Arsuaga et al., 1999a; Rosenberg et al., 2006; Trinkaus, 2009; Churchill et al., in press) and has been proposed for the Lower Pleistocene of Africa (KNM-WT 15000, see Grine et al., 1995). In addition, other skeletal elements, in particular the clavicles from the TD6 level at the Gran Dolina, can also provide some information about the thorax size of H. antecessor. Because the clavicle is functionally part of the shoulder, its length is related to the breadth of the upper torso and provides information on this aspect of the upper body trunk. The extreme length of Neandertal clavicles is related to their broad shoulders (Boule, 1911e1913; Heim, 1976; Trinkaus, 1983; Churchill, 1994a; Vandermeersch and Trinkaus, 1995). At the same time, Carretero et al. (1999) proposed that the long absolute length of the adult clavicle, ATD6-50, also strongly suggest H. antecessor, like the Neandertals, is characterized by a relatively long clavicle compared with H. sapiens. Moreover, the ratio of the medial length to the total length of the clavicle has been suggested as informative of the anteroposterior depth of the upper thorax (Vrba, 1979). Churchill (1994a,b) found support to this suggestion among modern humans. Based on the measurements of the ATD6-50 clavicle reported by Carretero et al. (1999), we can calculate its conoid index (Conoid length/Maximum length  100). This calculation results in an index of 79.3, similar to 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. 637 A. Gómez-Olivencia et al. / Journal of Human Evolution 59 (2010) 620e640 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 (10R) Tabun C1 Kebara 2 Z-scores Summary statistics Z-scores Summary statistics 10L 10R 188.92  14.42 (155.4e216.5) n ¼ 24 252.52  20.81 (208.0e284.0) n ¼ 24 9.56  0.86 (7.9e11.7) n ¼ 29 6.51  0.76 (5.4e8.3) n ¼ 29 15.42  1.76 (12.7e19.5) n ¼ 29 7.35  1.20 (5.0e9.5) n ¼ 29 14.85  1.97 (10.8e18.8) n ¼ 29 5.12  0.88 (3.7e7.4) n ¼ 29 10.94  1.38 (8.8e15.2) n ¼ 24 7.12  0.92 (5.2e8.6) n ¼ 24 (1.79) 170.74  10.77 (151.7e194.1) n ¼ 25 227.92  17.41 (186.0e260.0) n ¼ 25 8.54  0.84 (7.1e10.0) n ¼ 29 5.42  0.51 (4.4e6.3) n ¼ 29 13.99  2.09 (9.7e17.4) n ¼ 30 5.68  0.98 (3.6e8.1) n ¼ 30 13.26  1.90 (9.7e19.1) n ¼ 30 3.80  0.82 (2.6e6.6) n ¼ 30 9.12  1.11 (6.9e11.5) n ¼ 25 5.69  1.13 (1.7e7.0) n ¼ 25 1b ChCaV (190.0) (0.07) 2b ACaV (273.0) (0.98) 15 DiCrCdEDCu 9.3 0.30 16 GEDCu 8.6 2.76**z 17 DiCrCdAngP 18 GAngP 19 DiCrCdCuM 20 GCuM 7.6 2.83**z 23 SEMxD 15.4 3.22**z 24 SEMnD 9.5 2.58**z 16.2 0.44 8.3 0.79 15.3 0.23 (2.59)**z 0.90 6.25**z 1.06 2.68**z 1.07 4.65**z 5.64**z 3.38**z 10L La Chapelle-auxSaints Shanidar 3 10R 10R 10L (225.0) (285.0) 11.4 8.8 9.7 7.5 8.2 9.3 8.3 7.4 9.8 9.2 8.4 (16.5) 6.8 9.7 12.3 15.4 5.5 6.6 14.9 9.8 (16.0) 9.9 9.2 14 9.1 (16.0) (8.1) 8.2 10.8 7.5 >10.0 9.4 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 z are outside the range of our modern comparison samples. 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, ATD639 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 as suggested by the ATD6-79 rib. A second complete left clavicle (ATD6-37) representing a subadult individual is also present in the fossil sample from TD6 (Carretero et al., 1999). The maximum length of ATD6-37 (83.7 mm) suggests an age at death of between five and seven years old when compared with specimens of similar length from H. sapiens juveniles. However, when compared with the adult clavicular length for H. antecessor, based on the ATD6-50 specimen, an age at death of two to four years is suggested for ATD6-37. This indicates that this subadult H. antecessor individual is also characterized by a relatively long clavicle compared with modern human children of similar age (García-González et al., 2009). Relatively long clavicles have been also noted in the Neandertal children from Roc de Marsal 1 (Madre-Dupouy, 1992), Amud 7, Dederiyeh 1 and Teshik-Tash (García-González et al., 2009). Thus, the relatively long clavicle in both adult and subadult individuals of H. antecessor provides additional support for the hypothesis that, like the Neandertals, these hominins had a broader thorax than living humans. The costal elements recovered to date from the TD6 level at the Gran Dolina can neither confirm nor reject the hypothesis that H. antecessor had a large thorax similar to that of Neandertals. However, the fragmentary evidence of the H. antecessor thoracic skeleton is consistent with this suggestion based on other skeletal elements. Future discoveries of additional costal remains from the Gran Dolina may prove more informative and help elucidate the size and shape of the thorax of the first inhabitants of Europe. Acknowledgements We are grateful to the Atapuerca excavation team, especially the team involved in the test pit excavation at Gran Dolina during mid 1990s and the team involved in the excavation of the TD6 level during the last few years, for their dedication and effort. The restoration of these specimens has been performed by Lucía LópezPolín. We are also grateful to Philip Mennecier (Musée de l’Homme, Paris), Yohannes Haile-Selassie (Cleveland Natural History Museum), Chris Stringer and Rob Kruszynski (Natural History Museum, London), Yoel Rak (Department of Anatomy, Sackler School of Medicine, Tel Aviv University, Israel), Richard Potts (Smithsonian Institution-National Museum of Natural History, Washington D.C.), Jakov Radov ci c (Croatian Natural History Museum, Zagreb), Jean-Jacques Hublin (Department of Human Evolution, Max Planck Institute, Leipzig) for providing access to the important specimens under their care. We are also indebted to Aurélie Fort, Véronique Laborde, Liliana Huet, Lyman Jellema and Jennifer Clark for curatorial assistance. Further thanks go to our colleagues at the Centro UCM-ISCIII de Investigación sobre Evolución y Comportamiento Humanos, Laboratorio de Evolución Humana (LEH) of the Universidad de Burgos, the Centro Nacional de Investigación sobre la Evolución Humana (CENIEH, the Institut Catalá de Paleoecología Humana i Evolució Social (IPHES) and LCHES-University of Cambridge. Special thanks to Aimara for her comments, support and help with the figures. Thanks to R.G. Franciscus, K.L. Eaves-Johnson, J.C. Ohman, A. Bartsiokas, S.E. Churchill, J. Ríos, A. Gómez-Robles, M. Martinón, J. Rodríguez, L. Prado, A. Bonmatí, I. Martínez and J. Tardy for fruitful discussion. F. Gracia has kindly revised the English on a previous version. R. Quam has revised the English and provided helpful comments. We would like to thank D. Begun, an associate editor and two referees for helpful comments that have improved the manuscript. The first author has been partially supported by a grant from the Ministerio de Educación y Ciencia, a travel grant from Universidad de Burgos, and a postdoctoral fellowship of the Ministerio of Educación (Programa Nacional de Movilidad de Recursos Humanos del Plan Nacional de I-Dþi 2008-2011). This research was supported by the Ministerio de Ciencia e Innovación, Proyectos CGL2006-13532-C03-01/02/03 and CGL2009-12703-C03-01/02/03 and by Junta de Castilla y León Project BU00509. This research received support from the SYNTHESYS Project http://www. synthesys.info/, which is financed by European Community Research Infrastructure Action under the FP6 “Structuring the European Research Area” Programme. Funding for the fieldwork came from the Junta de Castilla y León and Fundación Atapuerca. Help in the field from the Grupo Espeleológico Edelweiss was essential. 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