The Neandertals of northeastern Iberia: new remains from the Cova del Gegant (Sitges, Barcelona).

Journal of Human Evolution xxx (2015) 1e16

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The Neandertals of northeastern Iberia: New remains from the Cova del Gegant (Sitges, Barcelona) Rolf Quam a, b, c, *, Montserrat Sanz d, Joan Daura d, Kate Robson Brown e, lez f, Laura Rodríguez f, g, Heidi Dawson e, Rosa Flor Rodríguez d, Rebeca García-Gonza d mez , Lucía Villaescusa d, Angel Rubio d, h, Almudena Yagüe d, Sandra Go b ~o Zilha ~o i, j, Juan Luis Arsuaga b, k María Cruz Ortega Martínez , Josep Maria Fullola i, Joa a

Department of Anthropology, Binghamton University (SUNY), Binghamton, NY 13902-6000, USA n sobre la Evolucio n y Comportamiento Humanos, Avda. Monforte de Lemos, 5, 28029 Madrid, Spain Centro UCM-ISCIII de Investigacio c Division of Anthropology, American Museum of Natural History, Central Park West at 79th St., New York, NY 10024-5192, USA d riques, Dept. Prehisto ria, H. Antiga i Arqueologia, Facultat de Geografia i Histo ria, Grup de Recerca del Quaternari-Seminari d'Estudis i Recerques Prehisto Universitat de Barcelona, C/Montalegre, 6, 08001 Barcelona, Spain e Department of Archaeology and Anthropology, University of Bristol, 43 Woodland Road, Bristol BS8 1UU, UK f ricas y Geografía, Universidad de Burgos, Facultad de Humanidades y Educacio n, 09001 Burgos, Spain Departamento de Ciencias Histo g n sobre la Evolucio n Humana (CENIEH), Paseo Sierra de Atapuerca s/n, 09002 Burgos, Spain Centro Nacional de Investigacio h Laboratorio de Antropología, Depto de Medicina Legal, Toxicología y Antropología Física, Facultad de Medicina, Universidad de Granada, Av de Madrid, 11, 18012 Granada, Spain i riques, Dept. Prehisto ria, H. Antiga i Arqueologia, Facultat de Geografia i Histo ria, Universitat de Barcelona, Seminari d'Estudis i Recerques Prehisto C/Montalegre, 6, 08001 Barcelona, Spain j Catalana de Recerca i Estudis Avançats (ICREA), Passeig Lluís Companys, 23, 08010 Barcelona, Spain Institucio k gicas, Universidad Complutense de Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain Departamento de Paleontología, Facultad de Ciencias Geolo b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 21 June 2014 Accepted 5 February 2015 Available online xxx

The present study describes a new juvenile hominin mandible and teeth and a new juvenile humerus from level V of the GP2 gallery of Cova del Gegant (Spain). The mandible (Gegant-5) preserves a portion of the right mandibular corpus from the M1 distally to the socket for the dc mesially, and the age at death is estimated as 4.5e5.0 years. Gegant-5 shows a single mental foramen located under the dm1/ dm2 interdental septum, a relatively posterior placement compared with recent hominins of a similar developmental age. The mental foramen in Gegant-5 is also placed within the lower half of the mandibular corpus, as in the previously described late adolescent/adult mandible (Gegant-1) from this same Middle Paleolithic site. The Gegant-5 canine shows pronounced marginal ridges, a distal accessory ridge, and a pronounced distolingual tubercle. The P3 shows a lingually-displaced protoconid cusp tip and a distal accessory ridge. The P4 shows a slightly asymmetrical crown outline, a continuous transverse crest, a mesially placed metaconid cusp tip, a slight distal accessory ridge, and an accessory lingual cusp. The M1 shows a Y5 pattern of cusp contact and a well-developed and deep anterior fovea bounded posteriorly by a continuous midtrigonid crest. Gegant-4 is the distal portion of a left humerus from a juvenile estimated to be between 5 and 7 years old at death. The specimen shows thick cortical bone. Although fragmentary, the constellation of morphological and metric features indicates Neandertal affinities for these specimens. Their spatial proximity at the site and similar ages at death suggest these remains may represent a single individual. The addition of these new specimens brings the total number of Neandertal remains from the Cova del Gegant to five, and this site documents the clearest evidence for Neandertal fossils associated with Middle Paleolithic stone tools in this region of the Iberian Peninsula. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Homo neanderthalensis Tooth Mandible Humerus Upper Pleistocene Iberian Peninsula

* Corresponding author. E-mail address: [email protected] (R. Quam). http://dx.doi.org/10.1016/j.jhevol.2015.02.002 0047-2484/© 2015 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Quam, R., et al., The Neandertals of northeastern Iberia: New remains from the Cova del Gegant (Sitges, Barcelona), Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.02.002

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R. Quam et al. / Journal of Human Evolution xxx (2015) 1e16

Introduction During the last two decades, numerous archaeological sites in the northeast (NE) of the Iberian Peninsula have documented Neandertal occupations at rock shelters, open-air sites, and caves during Marine Isotope Stages (MIS) 5e3. Recent research at Abric Romaní (Vallverdú et al., 2005; Camps and Higham, 2012), Roca dels Bous (Martínez Moreno et al., 2010), and Cova Gran de Santa Linya (Mora et al., 2011) has contributed to debates on the Middle to Upper Paleolithic transition focusing on radiocarbon dating (Camps and Higham, 2012; Maroto et al., 2012; Vaquero and Carbonell, baut et al., 2012) and its variability 2012), lithic technology (Thie (Mora et al., 2008), and stratigraphic sequences (Martínez Moreno et al., 2010). However, Neandertal fossils remain scant, especially when compared to the southern Mediterranean coast (Arsuaga et al., 1989, 2001, 2007, 2012; Garralda, 2005; Walker et al., 2008, 2010, 2011a, 2011b, 2012). The relative rarity of hominin remains can be explained by (i) the small number of archaeological sites excavated, (ii) site function, (iii) the low intensity of occupations, (iv) behavioral patterns, and/or (v) sampling bias. Hitherto, Neandertal remains from this northeastern area were limited to the Cova de Mollet isolated tooth, the Banyoles mandible, and the Cova del Gegant mandible and isolated tooth. Although the stratigraphic provenance of the hominin molar from Cova Mollet is uncertain (Maroto et al., 1987; Cortada and Maroto, 1990), a recent study, based on the degree of fossilization and the sediment adhering to the tooth, places it in Layer 5 from the site, which possibly dates to MIS 7 (ca. 215 ka; Maroto et al., 2012). The most accepted date for the Banyoles mandible is ca. 45 ka obtained for and Bischoff (1991), but there is the encasing travertine by Julia ongoing disagreement as to both its true chronological ascription (Grün et al., 2006) and its taxonomic status (Alc azar de Vel azco et al., 2011). At Cova del Gegant (Fig. 1), the Neandertal fossils came from sediments that also contained Mousterian stone tools and Pleistocene faunal remains (Daura et al., 2005; Rodríguez et al., 2011). The Cova del Gegant specimens were recovered during a thorough revision of the faunal material excavated in the gallery closer ric Municipal de to the sea (GL1; Fig. 1) in the 1950s (Arxiu Histo Sitges, AHSI) and in the 1970s (Paleontological Collections, Natural History Museum of Barcelona, MGB). These remains correspond to an adolescent/adult hominin mandible (Gegant-1; Daura et al., 2005, 2010; Arsuaga et al., 2011) and an isolated lower lateral incisor (Gegant-2; Rodríguez et al., 2011; Sanz, 2013). Martínez Moreno (1990) mentions a central incisor germ (Gegant-3) from a different gallery (GL2; Fig. 1), but this specimen remains unpublished. Although fragmentary, all of the hominin fossils were suggested to show Neandertal affinities. Their approximate provenience within the site is fairly clear, and considerable effort has been made to provide a precise chronological control for the associated deposits in order to place these specimens within an appropriate paleontological context (Daura et al., 2010; Daura and Sanz, 2011e2012). Here, we present the anatomical description and comparative study of two new Neandertal remains discovered during the 2009 and 2010 field seasons: a partial humerus (Gegant4) and a juvenile mandible (Gegant-5) from a different area of the site (GP2; Fig. 1). Both fossils were recovered during the ongoing archeological excavation of the site, and their stratigraphic provenance is known. The Cova del Gegant site The Cova del Gegant (Sitges, Barcelona) is located on the seaward edge of the Garraf Massif (Fig. 1), some 40 km south of Barcelona (1460 27.3300 E, 41130 24.7500 N). This massif, one of the

most important karstic systems of NE Iberia, is composed of Jurassic and Cretaceous limestone and dolomite. The site is currently accessible both from the sea and through a natural vertical shaft. It consists of a principal chamber (GP), now eroded by wave action, and its inner part (GP1 and GP2), where a small conduit (GLT) leads to the adjacent Cova Llarga. Two galleries branch off of the right side of GP, one more interiorly (GL2) and the other nearer to the sea (GL1). At least eight site formation episodes from the Upper Pleistocene (Episodes 0e3) to the Holocene (Episodes 4e7) have been recognized in the Cova del Gegant stratigraphic sequence, alternating between continental sediment deposition and periods of marine erosion followed by the accumulation of beach deposits (Daura et al., 2010). This framework makes it possible to establish correlations between the deposits that yielded the Neandertal remains and those located elsewhere in the cave (Table 1). The Gegant-1 mandible and the Gegant-2 incisor come from the same gallery (GL1) and likely derive from the same layer (XV). Thus, they may have been in close spatial proximity (Daura and Sanz, 2011e2012), and correspond to Episode 2 or 3. The archaeological sequence in this part of the site has been dated to between 49.4 ± 1.8 ka and 60.0 ± 3.9 ka (two and one sigma errors, respectively; Daura et al., 2010). The Gegant-2 incisor falls within this time range, while the Gegant-1 mandible has been directly dated by U-series to 52.3 ± 2.3 ka (2 sigma error). The Neandertal remains described here (Gegant-4 and Gegant5) were recovered in layer V of the GP2 gallery, which contains intact deposits in the rear part of the main conduit. This layer overlies the rocky floor of the cave, and it is possible that it once filled most of the principal chamber (GP); it consists of dark brown to black lutites and sands with faunal remains, a few stone tools, and a large number of coprolites. In the chronostratigraphic framework proposed for Cova del Gegant (Daura et al., 2010), these new hominin remains belong to Episode 1. The Gegant-3 central incisor germ also likely comes from this same level and episode but in GL2. A small sample was removed from the Gegant-4 humerus for DNA analysis and radiocarbon dating at Oxford (P-27870), but no results were obtained due to low collagen yield. Nevertheless, Episode 1 at the site has been dated to 55.7 ± 4.8 ka by the Optically Stimulated Luminescence (OSL) technique (Daura et al., 2010), suggesting that all the hominin remains from the Cova del Gegant are roughly similar in chronology. Although there is clear evidence of hominin activity at the site in the form of hearths (GP2) (Sanz, 2013), hominin presence was likely short-term and sporadic, as evidenced by the small number of stone tools (GP2, GL1, and GL2) and the low level of anthropic impact (e.g., cut marks and burning) on the faunal remains. In addition, no evidence of on-site stone tool production has been documented, and the tool assemblage is entirely composed of finished tools that were transported to and discarded at the cave. It is plausible that hominin activity would have been primarily concentrated at the entrance, which has been heavily modified by marine erosion. In contrast to the limited evidence for hominin activity, the presence of hyena remains, partly digested bones, and coprolites suggest that the site primarily functioned as a hyena den. The damage and breakage patterns in the faunal remains are in keeping with those described in fossil hyena assemblages. Long bones have been turned into cylinders as a result of ravaging, with diaphyses being more abundant than epiphyses. At Cova del Gegant, carnivores are plausibly the main agents responsible for the accumulation of ungulate remains (Mora, 1988; Daura, 2008; Daura and Sanz, 2011e2012; Sanz, 2013; Samper Carro and Martínez Moreno, 2014).



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Figure 1. Location of the Cova del Gegant, including panoramic views of Cova del Gegant and other caves from Punta de les Coves in 1928 (1) and in 2012 (2). Site plan of the Cova del Gegant (3) indicating the position of the different galleries discussed in the text and the location of the Neandertal remains. Schematic reconstruction (4) of stratigraphic profiles in different sectors of the cave with radiometric dates and the position of the Neandertal remains indicated.

Materials and methods Preservation and description of the Cova del Gegant fossils The Gegant-5 mandibular specimen (Fig. 2) preserves a portion of the right corpus from the M1 distally to the socket for the dc mesially. The alveolar margin is better preserved than the basal

margin along its length, but few morphological details of the external or internal corpus can be discerned and reliable corpus dimensions can be recorded only at the level of the mental foramen. The dm2 and M1 are fully erupted and in situ in their alveolar sockets. The latter is well preserved, but the crown of the dm2 is nearly entirely missing, with only a small portion of the enamel preserved distally, in contact with the mesial face of the M1. The

Table 1 Human fossils from the Cova del Gegant. Specimen

Field label

Season

Gegant-1 Gegant-2 Gegant-3 Gegant-4 Gegant-5

AHSI 567 MGB V2828 UAB CG85-GB UB CG09-H23-Vf-2311 UB CG10-H24-Vf-3131

1954 1974e1975 1985 2009 2010

a

Provenience Layer Layer Layer Layer Layer

XVa (GL1)a XVa (GL1)a V (GL2) V (GP2) V (GP2)

Age at death

Preservation

Source

Adolescent/Adult 8e10 years Subadult 5e7 years 4.5e5.0 years

Edentulous mandibular corpus Lower lateral incisor Central incisor (Germ) Fragmentary left distal humerus Fragmentary mandible and left C1-M1

Daura et al. (2005) Rodríguez et al. (2011) Martínez-Moreno (1990) Present study Present study

Tentatively assigned stratigraphic level.


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Comparative morphology

Figure 2. The Gegant-5 mandible with the dm2 and M1 in place in their alveolar sockets. Note the canine still housed in its crypt within the mandibular corpus. Scale bar ¼ 3 cm.

remaining teeth (C1eP4) are still housed in their crypts within the mandibular corpus. They were removed for study during cleaning and restoration of the specimen. Gegant-4 is the distal fragment of a left humerus (Fig. 3), with a maximum preserved length of 82 mm. Proximally, the fragment extends well into the diaphysis and includes the nutrient foramen, which is directed distally. Diaphyseal surfaces are well preserved, and the lateral supracondylar ridge is marked. No deltoid tuberosity is visible, and the distal section of the radial groove is lightly marked. The distal epiphysis (capitulum, trochlea, and medial and lateral epicondyles) is not present. The distal posterior bone surface is largely intact, and the rounded cross-section of the lateral border suggests that, at least in this region, only the superficial bony tissue has been lost. The medial border is quite strongly projecting medially, and the epicondyle may have been unfused. The distal anterior bone surface has suffered more damage, possibly caused by scavengers, resulting in most of the coronoid fossa being lost.

The morphology and metric characteristics of the Gegant-5 mandible and teeth are compared with middle and upper Pleistocene members of the Neandertal lineage and Homo sapiens. The mandibular dimensions have been compared with juvenile Neandertal and H. sapiens individuals measured by the authors or compiled from the literature. The dental dimensions and morphology are compared mainly with the large sample of teeth from the middle Pleistocene site of the Sima de los Huesos (SH) in the Sierra de Atapuerca in northern Spain, Upper Pleistocene Neandertals from Europe and southwest Asia, and recent H. sapiens. Description of the dental morphology generally follows those features defined by the Arizona State University Dental Anthropology System (ASUDAS; Turner et al., 1991). In addition, a few features not included in the ASUDAS, but defined more recently, are also n-Torres et al., 2012). The considered (Bailey, 2002, 2006; Martino main metric dimensions of the crown and roots were recorded to the nearest 0.1 mm using sliding calipers. In addition, the areas of the individual molar cusps and the crown area were measured from scaled occlusal photographs following previously defined techniques (Wood and Abbott, 1983; Wood et al., 1983; Bailey, 2004). High resolution serial CT scan images were used to create virtual 2D and 3D representations of the Gegant-4 humerus. The Gegant-4 specimen was CT scanned using a Skyscan 1172 system located at the University of Bristol, set at 74 kV and 133 mA with an Al/Cu filter to provide images with an isometric voxel resolution of 35 mm. Analysis of the resulting reconstructed image files was achieved using the software CTAn (Version 1.9.2.5, Skyscan, Kontich, Belgium) and Avizo v.6. Cross-sectional geometry of the diaphysis was analyzed at the approximately 35% location (measured from the distal end), in a slice at a right-angle to the bone's long axis. The following values were measured: periosteal perimeter (PP), total area (TA), cortical bone area (CA), % cortical area (%CA), and mean cortical thickness (CTh). TA was measured by selecting the entire slice as the region of interest. CA measurements were repeated three times and the mean calculated to account for any minor discrepancies when selecting the region of interest. CTh was calculated as the mean of cortical thickness taken in the medial, lateral, anterior, and posterior sections of the bone. The crosssectional properties in the Gegant-4 specimen were compared with samples of Pleistocene European fossils and recent hominis to place the specimen within a broader comparative context. Age at death estimation

Figure 3. The Gegant-4 humerus in medial (left), anterior (center), posterior (right), and inferior (lower) views. Scale bar ¼ 2 cm.

Despite some initial controversy, many studies have shown that Neandertals and modern humans differ in some aspects of their dental anatomy that are crucial to determining a dental age at death. Among the most important differences are those regarding the relative dental developmental sequence (Tompkins, 1996a; Bayle et al., 2009), the distribution of perikymata on the crown surface (Guatelli-Steinberg et al., 2007; Guatelli-Steinberg and Reid, 2008), and cuspal enamel thickness (Olejniczak et al., 2008) and extension rate (Smith et al., 2007a). Thus, dental age at death estimates in Neandertals should generally not be based on modern human standards (Smith et al., 2010). Similarly, there is growing evidence that the tempo and mode of skeletal ontogeny have varied in hominin evolution, which suggests that it may not always be possible to extrapolate directly from a modern human reference to a Neandertal (Smith and Tompkins, 1995). The debate as to whether Neandertal maturational schedules proceeded faster, slower, or at a similar pace to modern humans is ongoing, and it is possible that hominin life history evolution was, and may continue to be, a modular process (Heim,



1982; Tompkins and Trinkaus, 1987; Madre-Dupouy, 1992; Tillier, 1999; Leigh and Blomquist, 2007; Cowgill, 2010). Dental developmental sequence To assess the dental developmental pattern of the Gegant-5 mandible, high resolution serial CT scan images were used to create virtual 3D representations of the individual teeth. The specimen was CT scanned using a YXLON Compact (YXLON International X-Ray GmbH, Hamburg, Germany) industrial multi-slice computed-tomography (CT) scanner, located at the Universidad de Burgos in Spain. The mandible was aligned along the long axis of the right mandible corpus. Scanner energy was set at 160 kV and 4 mA and the field of view was 69.9 mm. Individual slices were obtained as a 1024 1024 matrix of 32 bit Float format for processing. The final pixel size was 0.051 mm with an inter-slice distance of 0.2 mm. The Mimics™ (Materialise, Belgium) software program was used to visualize the CT images and make the virtual reconstructions. We have used semiautomatic segmentation in order to define Hounsfield values for the dentine, enamel, bone, and air. To assess the degree of similarity or difference between the dental developmental sequence in the Gegant mandible and that of modern humans, we have relied on a Bayesian approach (Braga and Heuze, 2007), which provides a probability that the development pattern in the Gegant individual could be found within a modern human population. The developmental stages of the Gegant permanent dentition were scored following the systems developed by Moorrees et al. (1963) and Demirjian et al. (1973), while the dm2 was scored based on the system established by Liversidge and Molleson (2004). Although dental development is under tight genetic control, some variability in both tooth formation and eruption is present (Tompkins, 1996b). In light of this, the Demirjian dental developmental sequence obtained for the Gegant-5 permanent mandibular teeth was also compared to a pooled sample of modern human children of both sexes and diverse geographic and temporal periods (n ¼ 100). This pooled sample was drawn from three sources. A subset was chosen from each source based on having at least one tooth that showed the same score as that seen in at least one tooth from the Gegant-5 mandible. The first subset was derived from the data included in the Electronic Encyclopedia on MaxilloFacial, Dental and Skeletal Development CD-ROM (Demirjian, 1996). These data come from a longitudinal study of Montreal French-Canadian children conducted in the 1960s and 1970s. A subset of girls (n ¼ 40) and boys (n ¼ 40) aged from 6 to 10 years was selected. The second subset consists of cross-sectional standardized orthopantomographs of ten living girls of known chronological age ranging between 3 and 8 years old from Burgos (Spain). The last subset is a sample of ten children from a Medieval archaeological population excavated from the Dominican n-Alvarez, Monastery of San Pablo (Ada 2003) that are now housed at the Laboratory of Human Evolution at the Universidad de Burgos. CT image data for these ten individuals were obtained with similar parameters as those for the Gegant mandible, except for a larger field of view (111.1e187.5 mm) to encompass the entire mandible. Virtual reconstruction of the individual teeth was performed in the same way as in the Gegant mandible. The development of the dm2 was not included in the comparative analysis due to lack of data. Crown formation time Crown formation time was calculated only for the C1 and P3. The P4 was still housed within the body of the mandible when the analyses were performed, and the M1 shows some slight wear on the mesiobuccal cusp, which makes it difficult to measure the cuspal enamel thickness and number of perikymata. Crown formation time in the C1 and P3 was calculated as the time to form both cuspal enamel plus the lateral or imbricational enamel. Cuspal enamel thickness can be measured on CT scans as the

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distance from the dentine horn tip to the position of the first formed perikymata. However, it was not possible to observe the first perikymata in the CT scan. For this reason, the position of this perikymata was established by visual comparison of the CT image and the SEM image. After taking this into account, the enamel formation time was estimated by two different means, based on the thickness. First, a minimum cuspal formation time was calculated as cuspal thickness divided by a mean secretion rate in the cuspal region. Given that mean secretion rates do not vary between Neandertals and modern humans (Dean et al., 2001; Macchiarelli et al., 2006; Smith et al., 2007a), we relied on secretion rates reported in modern humans for anterior and posterior teeth (Schwartz et al., 2001; Smith et al., 2007b). Second, a maximum cuspal formation time was derived relying on a regression equation relating cuspal thickness and formation time (Dean et al., 2001). In both cases, cuspal thickness was multiplied by a factor of 1.15 in order to take into account prism decussation (Risnes, 1986). Lateral enamel formation time can be calculated as the total number of perikymata multiplied by the periodicity. Perikymata were imaged with an Environmental Scanning Microscope (JEOL JSM-6460LV) in low vacuum mode, in secondary emissions mode, and an accelerating voltage of 15 kV. Teeth were placed with the buccal surface orthogonal to the electron beam inside the microscope chamber. Several micrographs were taken at 55 magnification from the earliest formed enamel at the cusp to the latest formed enamel at the cervix. To count the perikymata, a photomontage was made from these micrographs with Photoshop CS5™ software. The Gegant periodicity cannot be determined directly, since we do not have sectioned teeth from this individual. Neandertal periodicities range from 6 to 9 days, with a mean and modal value of 7 or 8 (Smith et al., 2010). This range is broader in modern humans (6e12 days) but the mean and modal value is the same (7e8 days; Dean and Reid, 2001; Reid and Dean, 2006). Moreover, these periodicities are inversely related with perikymata number (Reid and Ferrell, 2006). We addressed the question of periodicity in Gegant5 in two ways. First, assuming an equivalent crown formation time in both Neandertals and modern humans, the linear regression formula derived from Reid and Ferrell (2006) for canines was used to predict the periodicity in Gegant. Since the periodicity is the same in all teeth belonging to the same individual (FitzGerald, 1998), we use this predicted periodicity for the P3 as well. Second, periodicity in the Gegant individual was estimated relying on the mean, mode, and range of periodicities reported in Neandertals (Smith et al., 2010). Thus, crown formation times in the Gegant individual are calculated based on a range of periodicities (from 6 to 10 days). Assessment for the age at death of Gegant-5 was carried out based on incremental dental enamel characteristics. This is an accurate, species-specific method that is independent of the modern human dental pattern (Bromage and Dean, 1986; Beynon et al., 1998; Smith et al., 2006), but it requires estimating some parameters (e.g., periodicity and the age of onset of enamel formation), which may lead to a degree of uncertainty in the assessment of age at death. With the exception of the deciduous teeth and the M1, which start to form enamel matrix in utero (Schour, 1936; FitzGerald, 1998), estimating the (post-natal) enamel initiation time for the other teeth is necessary to assess the dental age at death. The initiation time can be established histologically using the earliest formed M1 cusp as a reference, and we have relied on published histological data for enamel initiation in the C1 and P3 in modern humans and Neandertals (Dean et al., 1993; Reid et al., 1998; Reid and Dean, 2000; Guatelli-Steinberg et al., 2005; Garlez et al., 2011). cía-Gonza


6


Humerus ontogeny To facilitate comparative analysis, the age at death of the Gegant-4 humerus was estimated relying on a variety of approaches. While the maximum length and distal width of the humerus are routinely used to estimate age at death in modern human fetal and juvenile individuals (Maresh, 1970; Fazekas and Kosa, 1978; Scheuer and Black, 2000), the incomplete preservation of the Gegant-4 specimen means neither of these measures can be taken directly. However, it is possible to estimate maximum humeral length based on anatomical criteria, taking into account features such as the location of the nutrient foramen relative to the olecranon fossa, as well as other diaphyseal dimensions and morphological features, including the absence of the distal epiphysis, the morphology of the lateral border, and the gracility of the deltoid insertion and radial groove. To further contribute to the assessment of the age at death and morphology of the Gegant-4 specimen, cross-sectional properties at the 35% level were compared with a small modern human ontogenetic series generated for this study. Eight well-preserved modern human humeri aged between 2 and 10 years were selected for mCT scanning from the medieval skeletal collection of the Priory of St. Peter and St. Paul, Taunton, UK (Dawson and Robson Brown, 2012). These sub-adult skeletons were aged by dental formation and eruption, and epiphyseal fusion. The tooth formation stages of Moorrees et al. (1963), as modified by Smith (1991b), were used along with the dental eruption chart of Schour and Massler (1944). Epiphyseal fusion and ossification age stages were obtained from Scheuer and Black (2000). A comparative data set of bone parameters was generated following the same protocol as employed for the fossil specimen. The Cova del Gegant-5 mandible Age at death and sex estimation The M1 shows only very slight wear resulting in a flattening of the protoconid cusp tip but no dentine exposure. This indicates the tooth had been in functional occlusion for a short period of time. The dm2 is missing most of the enamel cap, and wear cannot be assessed on this tooth. The canine and premolars are still unerupted and housed within the body of the mandible (Fig. 4). The formation stages of the permanent teeth (Table 2) suggest an age at death for the Gegant individual between 5.5 and 6.8 years, based on modern human standards (Anderson et al., 1976; Liversidge et al., 2006). However, the Demirjian developmental sequence displayed by the Gegant permanent teeth (DeEeDeF) is not represented by any individual (0 out of 100) within our modern reference sample (p ¼ 0.00). The greatest discrepancy in the Gegant developmental sequence appears to be a relatively advanced stage of mineralization in the P3. Tompkins (1996b) has noted that Neandertals show an advance in the mineralization of

the posterior dentition but a delay in the P3, relative to the incisors. This relative advance in the formation of the molars was subsequently documented in other immature Neandertals, ^teauneuf 2 (Colombo et al., 2013). Although no inincluding Cha cisors are preserved in the Gegant-5 individual, the posterior dentition (P4 and M1) is slightly advanced relative to the C1, and the dental sequence is matched in the La Quina H18 Neandertal (Smith et al., 2010). Long-period line count of perikymata in the Gegant-5 P3 (98) (Table 3) is closest to the modern South African mean but does also fall within the range of Neandertal variation. In contrast, the perikymata count in the C1 (141; Fig. 5) is closest to the Neandertal mean (159), a sample that generally shows fewer perikymata than in H. sapiens (Table 3). The perikymata count in the Gegant-5 C1 is outside the lower limits of the range of variation in both Inuits and Europeans but does fall within the range of variation seen in modern South Africans. Neandertal canines are generally characterized by a more uniform spacing of the perikymata over the entire buccal surface of the tooth crown. In contrast, and despite some variation, H. sapiens canines tend to show a “packing” of the perikymata closer to the cervicoenamel junction (CEJ) (GuatelliSteinberg et al., 2007; Guatelli-Steinberg and Reid, 2008). The distribution of perikymata counts per decile in the Gegant lower canine (beginning at the incisal edge for the first decile and ending at the cervical edge for the last decile) is: 11e11e9e8e10e16e20e21e20e15. Based on this distribution, 65.2% of perikymata are located in the cervical half of the tooth. This value falls well within the range of variation of modern human samples and is only slightly higher than that shown by Neandertals. Therefore, although the total number of perikymata of the Gegant5 canine is close to the Neandertal mean, their distribution on the tooth surface more closely matches that in modern human samples. Taking into account cuspal enamel formation time and a range of values (6e10 days) for the periodicity (Table 4), crown formation times for the Gegant teeth range from 3.0 to 4.6 years (C1) to 2.5e3.5 years (P3). The maximum estimate in Gegant is very close to the mean in the Medieval Danish sample for the C1 and falls between the South African and European samples for the P3 (Table 5), while the minimum estimate falls below the range of variation in all the comparative samples. Nevertheless, a 6-day periodicity has been reported in a few Neandertals (Smith et al., 2010) and also represents the lower end of the modern human range of variation (Reid and Dean, 2006). Relying on the mean and modal periodicity (8 days) in modern humans yields crown formation times of 3.8 and 3.0 years for the C1 and P3, respectively. When the mean periodicity (7 days) of Neandertals is used, the estimated crown formation times are 3.4 and 2.7 years for the C1 and P3, respectively. In the latter case, the closest fit to both of the Gegant teeth is shown by Neandertals.

Figure 4. Virtual reconstruction of Gegant-5 (a) showing the placement of the P3 and P4 within the mandibular corpus (b) and the internal morphology of the dentition (c). Scale bar ¼ 2 cm.



7

Table 2 Formation stages and metric dimensions of the Gegant-5 teeth.a Formation stage Tooth

Moorrees

C1 P3 P4 M1 dm2

Crc-Ri Ri Crc R1/2-R3/4

a b

Liversidge/Molleson

Demirjian

H2

D E D F e

MD (mm)

BL (mm)

CI

MCA (mm2)

Crown height (mm)

Total preserved crown/root height (mm)

8.0 7.9 7.8 11.4 10.0 est.

9.1 8.4 8.6 10.4

113.8 106.3 110.3 91.2

51.7 54.5 57.3 97.0

11.4 8.5

12.0 10.1

Specimen/sample

Gegant-5 Neandertals Inuit Newcastle South African

b

18.2b

Crown Index (CI) ¼ (BL 100)/MD. Measured Crown Area (MCA) following Wood and Abbott (1983). Corrected for slight wear.

Table 3 Perikymata counts in the Gegant-5 teeth compared with Neandertals and recent H. sapiens.a

a

7.3b

C1 mean ± s.d. range (n) 141 159 ± 20 135e198 198 ± 16 172e215 199 ± 22 164e249 163 ± 21 125e203

(10)

P3b mean ± s.d. range (n) 98 109 ± 16 88e130 (5)

dimorphic tooth in the dental arcade (Garn et al., 1977; Bermúdez de Castro et al., 2001). The overall size of the Gegant-5 canine is modest and does not provide a clear indication as to sex. The presence of a distal accessory ridge would be more consistent with a male classification. This is one of the most sexually dimorphic features of the dentition, appearing more often in males than females across ten modern human samples (Scott, 1977). Nevertheless, this provides, at most, tentative support for a male classification of Gegant-5.

(10) (13) (24)

137 ± 17 109e182 (19) 101 ± 12 83e125 (16)

Comparative data from Guatelli-Steinberg and Reid (2008). Measured on the buccal cusp.

Table 6 shows the age at death estimates in the Gegant-5 individual based on the C1 and P3. Age at death is estimated using modern human values for the enamel initiation time, since no data are available for Neandertal lower dentitions. Relying on a 7 or 8 day periodicity, the age at death in the Gegant individual ranges from 3.8 to 5.4 years (C1) and from 4.4 to 4.8 years (P3). Thus, a final age at death estimate of approximately 4.5e5.0 years seems reasonable. Sex determination in Gegant-5 is complicated by its fragmentary state of preservation and juvenile status. Sex-related features are largely restricted to the canine, since this is the most sexually

Mandibular morphology (Fig. 2) A single mental foramen is present at the level of the dm1/dm2 and is located in the lower half of the corpus. Corpus height (22.6 mm) and thickness (12.8 mm) can be measured at the mental foramen (Table 7). Comparison with fossil and recent juvenile mandibles shows Neandertals to be generally characterized by taller and thicker mandibles for their developmental age (Fig. 6), and the Gegant-5 specimen generally falls above the fossil and recent H. sapiens specimens of similar developmental age. Nevertheless, the resulting robusticity index (56.6) is modest. There is a tendency for the robusticity index to decline with developmental age (Table 7), and in this respect Gegant-5 surpasses only Combe Grenal 1 (49.6), which is slightly older. It is also only slightly higher than the late adolescent/adult Gegant-1 mandible (49.4 est.). In Gegant-5, the mental foramen is located below the dm1/dm2 interdental septum. Recent humans of a similar developmental age as Gegant-5 mainly show the mental foramen placed under the dm1 (64.3%), although more than a quarter of individuals (26.8%) show a similar placement under the dm1/dm2 as in Gegant-5 (Coquegniot and Minugh-Purvis, 2003). In contrast, 37.5% of Neandertals show a mental foramen placed under the dm1/dm2, while an additional 12.5% show a placement under the dm2. Thus, although there is some overlap between samples, Neandertals do generally show a more posteriorly placed mental foramen with respect to the tooth row, even at the young age of Gegant-5. In Gegant-5, the mental foramen is located 8.4 mm above the basal margin. The vertical placement of the mental foramen within the mandibular corpus can be assessed by comparing the distance from the basal margin with the corpus height at the level of the mental foramen. Neandertals are generally characterized by a mental foramen that is placed closer to the basal margin, within the lower half of the mandibular corpus (Daura et al., 2005). The resulting index in Gegant-5 (37.2) falls between that calculated for the Cova Negra CN7755 mandible (41.5) and the late adolescent/ adult Gegant-1 mandible (35.8), indicating a low placement for the mental foramen. Second deciduous molar (Fig. 2)

Figure 5. SEM montage of the Gegant-5 C1 (a) and P3 (b) showing the perikymata. The two teeth were imaged separately at a magnification of 25 (C1) and 19 (P3) in lower vacuum mode and with an accelerating voltage of 20 KV. Scale bars ¼ 1 mm.

The Gegant-5 dm2 is in situ in the mandible but is missing nearly the entire tooth crown, with only a small portion of enamel


8


Table 4 Crown formation time estimation in the Gegant-5 teeth.a Tooth

Cuspal thickness (mm)

Minimum cuspal formation time (days)b

Maximum cuspal formation time (days)c

Number of perikymata

CFT (6 days)

CFT (7 days)

CFT (8 days)

CFT (9 days)

CFT (10 days)

750 950

227 265.8

290.6 353.2

141 98

1104.8 897.5

1245.8 995.5

1386.8 1093.5

1527.8 1191.5

1668.8 1289.5

C1 P3

a CFT (Crown Formation Time) ¼ [(Maximum formation time þ minimum formation time)/2] þ (No. of perikymata periodicity). CFT estimates assume a periodicity ranging from 6 to 10 days. b Following Smith et al. (2007c). c Following Dean et al. (2001).

tentatively estimated at c. 10 mm based on the preserved enamel portion and the complete dentine surface. This is nearly identical to the MD dimension in the Cova Negra CN7755 individual (10.1 mm; Arsuaga et al., 1989), and falls within one standard deviation below the mean in Neandertals (10.5 ± 0.6; n ¼ 30; Mallegni and Trinkaus, 1997). It is also close to the mean values in recent human males (9.9 ± 0.5; n ¼ 69) and females (9.7 ± 0.5; n ¼ 64; Mallegni and Trinkaus, 1997).

Table 5 Crown formation time (days) in Neandertals and recent H. sapiens. Tooth

Neandertals Mean ± s.d. (n)

South African Mean ± s.d. (n)

Newcastle Mean ± s.d. (n)

Medieval Danish Mean ± s.d. (n)

C1 P3

1315 ± 15 (2)a 989 ± 7 (2)a

1494 ± 56 (25)b 1122 ± 42 (16)c

1866 ± 73 (13)b 1437 ± 68 (19)c

1670 ± 60 (67)b

a b c

Calculated from Smith et al. (2007c, 2010). Guatelli-Steinberg et al. (2005). Reid et al. (1998).

Canine (Fig. 7)

preserved along the distal face of the tooth. Thus, nothing can be said about its morphological details. The pulp chamber does not appear expanded in CT imaging and the specimen does not show taurodontism. The MD dimension of the crown (Table 2) is

The right canine crown is unworn and well preserved. The buccal face shows a pronounced hypoplastic line located 9.6 mm from the cusp tip. This would correspond to 2.3e4.3 years of age

Table 6 Age at death estimatea for the Cova del Gegant-5 mandible based on C1 and P3 formation times. Tooth

C1

P3 a

Initiation time (days)

123 126 138 146 201 570 609 675

Age at death

Source

6 day periodicity (years)





3.4 3.4 3.4 3.4 3.6 4.6 4.1 4.3

3.8 3.8 3.8 3.8 4.0 5.0 4.4 4.6

4.1 4.1 4.2 4.2 4.4 5.4 4.7 4.8

4.5 4.5 4.6 4.6 4.7 5.7 4.9 5.1

4.9 4.9 5.0 5.0 5.1 6.1 5.2 5.4

Antoine (2001) lez et al. (2011) García-Gonza Dean et al. (1993) Antoine (2001) Reid et al. (1998) Antoine (2001) Dean et al. (1993) Reid et al. (1998)

Based on a periodicity ranging from 6 to 10 days and taking into account different ages for enamel initiation.

Table 7 Main metric dimensions of the Gegant-5 mandible. Specimen/Sample

Age at death (yrs.)

Corpus height at mental foramen (mm)

Corpus thickness at mental foramen (mm)

Robusticity Index at mental foramena

Source

Gegant-5

4.5e5.0

22.6

12.8

56.6

Present study

Neandertals Palomas 49 Barakai Archi 1 Roc de Marsal Il Molare 1 Palomas 7 La Chaise 13 Devil's Tower Cova Negra (CN 7755) Combe Grenal 1

c. c. c. c. c. c. c. c. c. c.

19.2 20.1 20.0 17.0 20.9 21.3 20.5 22.8 20.0 27.4

11.4 14.2 12.0 12.7 12.2 12.7 12.5 13.6 13.3 13.6

59.4 70.6 60.0 74.7 58.4 59.6 61.0 59.6 66.5 49.6

Walker et al. (2010) Mallegni and Trinkaus (1997) Mallegni and Trinkaus (1997) Madre-Dupouy (1992) Mallegni and Trinkaus (1997) Walker et al. (2010) Mallegni and Trinkaus (1997) Mallegni and Trinkaus (1997) Arsuaga et al. (1989) Garralda and Vandermeersch (2000)

Modern Humans Le Figuier La Madeleine 4 Lagar Velho Skhul 1 Qafzeh 4 Qafzeh 10 Recent children (n ¼ 20)

c. 3.0 c. 3.0 c. 4.5 c. 4.5 c. 6.0 c. 6.0 2.0e5.0

18.0 19.0 20.5 16.4 26.3 24.2 17.2 ± 1.8

10.7 9.4 11.5 11.0 14.2 13.3 10.3 ± 1.0

59.4 49.5 56.1 67.1 54.0 55.0 60.4 ± 6.9

Billy (1979) Heim (1991) Trinkaus (2002) Mallegni and Trinkaus (1997) Original specimen Original specimen Madre-Dupouy (1992)

a

2.0 3.0 3.0 3.0 3.5 4.0 4.0 4.0 5.0 7.0

Calculated as (corpus thickness/corpus height) 100.



Figure 6. Scatterplots of developmental age versus corpus height (top) and thickness (bottom) at the level of the mental foramen. Neandertals, and the Gegant-5 specimen, generally show a taller and thicker mandibular corpus for their developmental age than do H. sapiens.

9

and is perhaps related to the age at weaning. The crown shows a high, pointed, centrally placed cusp tip, but the crown is slightly asymmetrical, with the mesial shoulder being higher than the distal. The mesial and distal marginal ridges are well developed, and a clear distal accessory ridge (ASUDAS Grade 4) is present on the lingual face of the crown. The lingual face shows a marked expression of several morphological features. Although the mesial marginal ridge is more pronounced along its length, the distal marginal ridge shows a very prominent bulge approximately midway down from the tip. This feature is continuous with the distal marginal ridge but in occlusal view is separated from the lingual face of the tooth by a clear furrow. Just mesial to this feature, at the base of the crown, there is a very small lingual tubercle with a free apex. The pattern of crown asymmetry and development of the mesial and distal marginal ridges in the Gegant-5 canine is similar to that nreported to characterize both the Atapuerca SH teeth (Martino Torres et al., 2012) and the Neandertals (Bailey, 2006). In contrast, the distal accessory ridge is found in only 25% of the Atapuerca SH n-Torres et al., 2012) but is much more lower canines (Martino common (approximately 85%) in Neandertals (Bailey, 2006). The expression of a bulge in the distal marginal ridge is considerably weaker in the Atapuerca SH sample and Neandertals compared with the Gegant-5 canine, which shows an exaggerated expression of this feature. Several of the Atapuerca SH specimens show a slight bulge along the lower portion of the distal marginal ridge, but it never reaches the expression seen in the Gegant-5 canine n-Torres et al., 2012). Similarly, a weak bulge is present in (Martino the Neandertal lower canine from Arcy-sur-Cure (Bailey and Hublin, 2006). Metrically, the MD (8.0 mm) and BL (9.1 mm) dimensions of the Gegant-5 canine fall within one standard deviation above the Atapuerca SH and Neandertal means, while a greater difference is noted compared with recent H. sapiens (Table 8). The measured crown area (MCA) in the Gegant-5 canine (51.7 mm2) is also modest, falling only slightly above the mean in the Atapuerca SH sample (mean ± s.d. ¼ 49.7 ± 7.4 mm2; range ¼ 37.1e65.7 mm2; n ¼ 14) (Bermúdez de Castro et al., 2001). Data for Neandertals are scarce, but the Gegant-5 canine is smaller than that of Amud 1 (58.4 mm2) and Petit-Puymoyen 3 (52.9 mm2). It is, however, outside the range of variation in a pooled-sex contemporary H. sapiens sample (mean ± s.d. ¼ 37.3 ± 4.8 mm2; range ¼ 25.9e49.3 mm2; n ¼ 216; Bermúdez de Castro et al., 2001). Third premolar (Fig. 8)

Figure 7. The Gegant-5 lower canine. Note the well-developed distal marginal ridge and the clear distal accessory ridge. Scale bar ¼ 1 cm.

The unworn P3 crown is well preserved, and the marked hypoplasias present on the canine are not visible on the buccal face of the P3. In occlusal view, this tooth is only slightly asymmetrical (Grade 1; Bailey, 2006), with the distal portion of the lingual contour being convex and the mesial portion being weakly concave. The dominant buccal cusp is joined to a much smaller lingual cusp by a continuous transverse crest. The buccal cusp tip is displaced lingually and is located in the center of the tooth crown, and the buccal face of this cusp makes up a large portion of the tooth in occlusal view. Neither mesial nor distal buccal grooves are present on the buccal face. However, a pronounced distal accessory crest (Grade 2; Bailey, 2006) is present just distal to the tip of the protoconid, running vertically from the occlusal edge into the talonid basin distal to the transverse crest. There is a single small lingual cusp located in a medial position, opposite the buccal cusp. No accessory lingual cusps are present, but a mesial lingual groove is observed. The slight asymmetry and central placement of the dominant buccal cusp tip seen in the Gegant-5 P3 also generally characterizes



10.4 10.5 ± 0.5 (38) 10.8 ± 0.6 (34) 10.7 ± 0.5 (402)

MD (mm) Mean ± s.d. (n)

11.4 11.3 ± 0.5 (39) 11.5 ± 0.7 (33) 11.1 ± 0.7 (402) 8.6 8.6 ± 0.6 (35) 8.9 ± 0.8 (32) 8.3 ± 0.5 (213)

Figure 8. The Gegant-5 P3. Note the well-developed distal accessory crest. Scale bar ¼ 1 cm.

7.8 7.2 ± 0.4 (25) 7.5 ± 0.5 (29) 7.0 ± 0.5 (213) 8.4 9.0 ± 0.5 (32) 8.8 ± 0.7 (29) 7.8 ± 0.5 (264)


7.9 7.9 ± 0.4 (33) 7.7 ± 0.5 (28) 6.8 ± 0.5 (264)

BL (mm) Mean ± s.d. (n)

9.1 8.7 ± 0.7 (29) 8.8 ± 0.8 (20) 7.6 ± 0.6 (87) 8.0 7.6 ± 0.4 (29) 7.8 ± 0.5 (20) 6.6 ± 0.4 (87) Gegant-5 Atapuerca (SH) Neandertals Recent H. sapiens


C1 Specimen/Sample

Table 8 Dimensions of the Gegant-5 teeth compared with Pleistocene and recent humans.

P3



P4


M1


Source

Present Study n-Torres et al. (2012) Martino Bermúdez de Castro (1993) Bermúdez de Castro (1993)

10

mez-Robles the Atapuerca SH sample as well as Neandertals (Go n-Torres et al., 2012). A distal accessory et al., 2008; Martino crest is found in approximately 50% of the Atapuerca SH specimens and is nearly ubiquitous (90%) in Neandertals but is also found in high frequencies in fossil H. sapiens (Bailey, 2006; n-Torres et al., 2012). The lingual cusp in the Gegant-5 Martino P3 is generally smaller than in the Atapuerca SH sample but the absence of accessory lingual cusps is a point of similarity. Nearly half of the Atapuerca SH sample (52.9%) shows a single lingual cusp, although accessory cusps do occur at a higher frequency n-Torres et al., 2012). Similarly, a among Neandertals (Martino mesial lingual groove is present in nearly two-thirds of Neandertal P3s (Bailey, 2006). The MD dimension (7.9 mm) in the Gegant-5 P3 is very similar to both the Atapuerca SH and Neandertal means (Table 8), while the BL dimension (8.4 mm) is somewhat smaller, perhaps a result of the relatively small lingual cusp. The MCA in Gegant-5 (54.5 mm2) is close to the Atapuerca SH and Neandertal means but outside the range of variation in recent H. sapiens (Table 9). Fourth premolar (Fig. 9) The unworn P4 crown is well preserved. In occlusal view, the crown is slightly asymmetrical (Grade 1; Bailey, 2006) due to the talonid development in the distal portion. The main buccal and lingual cusps are joined by a continuous transverse crest (Grade 2; Bailey, 2002) that delimits an anterior fovea mesially and a larger and deeper talonid basin distally. Along the buccal margin, just distal to the main buccal cusp tip, a slight raised crest extends into the central basin, corresponding to the distal accessory ridge (Grade 1; Bailey, 2006). Distal to this is a small cuspule without any crest-like extension. No mesial accessory ridge is present. The lingual margin shows a dominant metaconid located mesial to the protoconid tip. No mesial lingual groove is present, but an accessory cusp is present distal to the metaconid (ASUDAS Grade 2e3).



11

Table 9 Measured crown areas (mm2) in the Gegant-5 P3 and P4 and some comparative samples. Specimen Gegant-5 Atapuerca (SH) mean ± s.d. Atapuerca (SH) range (n) Neandertal mean ± s.d. Neandertal range (n) Recent humans (pooled sex) mean ± s.d. Recent humans (pooled sex) range (n) a

MCA P3 (mm2)

MCA P4 (mm2)

Ratio MCA P3/P4

Source

54.5 53.1 ± 6.6 40.5e64.6 (14) 53.2 ± 6.4 43.5e64.3 (11) 38.4 ± 4.3 27.9e50.4 (224)

57.3 50.6 ± 7.3 35.5-63.4 (14) 56.9 ± 10.3 43.2e67.7 (8) 44.0 ± 5.2 31.4e57.4 (204)

95.1 105.4 ± 5.5 97.3e114.7 (14) 104.0 ± 14.0 95.7e128.8 (5) 87.3a

Present study Bermudez de Castro et al. (2001) Hershkovitz et al. (2011) Bermudez de Castro et al. (2001)

Calculated based on mean values.

Although the phylogenetic polarity of some of these traits is a n-Torres et al., matter of debate (Bailey and Lynch, 2005; Martino 2006), the asymmetrical crown, continuous transverse crest, distal accessory crest, mesial placement of the metaconid tip, and accessory lingual cusps (all seen in the Gegant-5 P4) occur at high frequencies as individual features and in combination in both the nAtapuerca SH sample and in Neandertals (Bailey, 2006; Martino Torres et al., 2012). Thus, the morphology of the Gegant-5 P4 clearly aligns it with the Neandertal evolutionary lineage. The MD dimension of the Gegant-5 tooth falls slightly above the mean values for both the Atapuerca SH and Neandertal samples, while the BL dimension is at or below the mean values in these same samples (Table 8). In contrast, both dimensions fall above the recent human means. The MCA in the Gegant-5 P4 is also modest, falling within one standard deviation above the Atapuerca SH mean and close to the mean value in Neandertals (Table 9). Comparison of the size of the P3 versus the P4 reveals that the Gegant-5 specimen does not show the derived relative expansion of the P3 that characterizes the Atapuerca SH and Neandertal samples. First molar (Fig. 10) The crown of the first molar is well preserved and shows only the slightest trace of wear on the protoconid cusp tip. Posteriorly,

Figure 9. The Gegant-5 P4. Note the slight crown asymmetry, continuous transverse crest, mesially placed metaconid tip, slight distal accessory crest, and lingual accessory tubercle. Scale bar ¼ 1 cm.

the distal root, which was still in the process of formation, is exposed. The occlusal surface shows five main cusps and neither a C6 nor C7 are present. The metaconid and hypoconid clearly make contact in the central basin, and the Gegant-5 M1 thus shows a Y5 pattern of cusp contact. Anteriorly, the specimen shows a deep, wide anterior fovea delimited posteriorly by a continuous middle trigonid crest (Grade 2; Bailey, 2002) separating this feature from the central basin. Neither a distal trigonid crest nor a deflecting wrinkle is present. The mesial marginal ridge does not show any accessory tubercles, and there is no expression of a protostylid. The pulp chamber is clearly expanded in the Gegant-5 M1 (Fig. 4c), and this tooth would be classified as mesotaurodont (Index ¼ 1.35) according to Shaw (1928). Many of the morphological features expressed in the Gegant-5 M1 either occur in similar frequencies in Neandertals and modern humans or do not vary along taxonomic lines. Nevertheless, the presence of a continuous midtrigonid crest, like in the Gegant-5 M1, is nearly ubiquitous in Neandertals (Bailey, 2002, 2006) and is also nfound at a high frequency in the Atapuerca SH sample (Martino Torres et al., 2012). In contrast, this feature is rare or absent in fossil and recent H. sapiens (Bailey, 2006). Taurodontism of the pulp chamber has been reported to occur at high frequencies in Neandertal dentitions (Kallay, 1963), and this feature is variably present in recent human populations (Shaw, 1928). The MD and BL dimensions in the Gegant-5 tooth are very close to the mean values for the Atapuerca SH and Neandertal samples, and not far removed from recent H. sapiens (Table 8). Comparative data for the MCA and individual cusp areas are scarce, but the MCA in Gegant (97.0 mm2) is similar to the Atapuerca SH mean value (98.7 ± 8.9 mm2; n ¼ 22; Bermúdez de Castro et al., 2001) as well as Bolomor HCB-02 (Table 10). However, the Gegant-5 M1 is small

Figure 10. The Gegant-5 M1 in occlusal (left) and distal (right) views. Note the welldefined anterior fovea bounded posteriorly by a continuous midtrigonid crest and the incomplete formation of the root. Scale bar ¼ 1 cm.


12


Table 10 Measured crown area and relative cusp areas in the Gegant-5 M1 and some comparative specimens and samples. Specimen

MCA

Relative protoconid

Relative metaconid

Relative hypoconid

Relative entoconid

21.7 23.8 24.2

21.4 18.0 20.1

18.8 18.1 19.6

Gegant-5 Valdegoba 1 Bolomor HCB-02

97.0 108.2 97.5

23.3 26.2 26.0

Middle Pleistocene mean ± s.d. (n ¼ 6) Krapina mean ± s.d. (n ¼ 6) Neandertals mean ± s.d. (n ¼ 6) Living humans (pooled sex) mean ± s.d. (n ¼ 33)

117.6 ± 15.9 114.1 ± 15.5 108.8 ± 8.4 94.4 ± 7.5

26.4 26.2 26.8 26.1

± ± ± ±

2.9 1.0 2.0 1.5

relative to other (non-SH) middle Pleistocene humans as well as Neandertals, including the specimen from Valdegoba. The sizes of the individual cusps, from largest to smallest, conform to the following sequence: protoconid > metaconid ¼ hypoconid > entoconid > hypoconulid. Comparing the relative sizes of the individual cusps in Gegant-5 with other fossil samples (Table 10) reveals a smaller protoconid and larger hypoconulid in the Gegant-5 tooth. Gegant-5 also differs from two other Neandertal specimens from the Iberian Peninsula (Valdegoba 1 and Bolomor HCB-02) in showing a smaller protoconid and metaconid. The Cova del Gegant-4 humerus Age at death Based on the preserved portion of the shaft as well as the presence of some anatomical structures (e.g., nutrient foramen, superior margin of the olecranon fossa, etc.), a humeral diaphyseal length of 175e180 mm is estimated. This corresponds to an age at death of 5e5.5 years according to modern human standards (Scheuer and Black, 2000). However, the absence of the distal epiphysis, morphology of the lateral border, and gracility of the deltoid insertion and radial groove suggest an age at death of around 7 years using standards for modern humans (Scheuer and Black, 2000). Taken together, an age at death of approximately 5e7 years is suggested. However, the robust diaphysis, triangular cross-section, and thick cortical bone seen in the Gegant-4 humerus (Figs. 3 and 11) are not features which would normally be associated with a similarly aged modern human child. Comparative morphology Gegant-4 has a percent cortical area of 69.3% at 35% of shaft length, a higher value than any of the modern human specimens in our ontogenetic series (Table 11). This value is also higher than that reported for the Upper Paleolithic modern human specimen from

Figure 11. Cortical thickness in three recent H. sapiens juvenile humeri (a) compared with the Gegant-4 specimen (b). All specimens are to the same scale.

21.8 21.0 21.4 21.3

± ± ± ±

2.0 1.7 1.2 1.5

20.0 20.3 19.6 20.0

± ± ± ±

1.7 1.2 1.7 1.1

19.2 20.8 19.7 21.4

Relative hypoconulid 14.8 14.0 10.0

± ± ± ±

2.5 1.0 2.3 1.1

12.6 11.6 12.5 11.1

Source Present study Original specimen Arsuaga et al. (2012)

± ± ± ±

1.3 1.3 1.2 1.9

Trefný Trefný Trefný Trefný

(2005) (2005) (2005) (2005)

Lagar Velho (53%) but more similar to Skhul I (67%; Trinkaus et al., 2002) and lower than the Lower Pleistocene juvenile individual from the Gran Dolina ATD6-121 (82.7%; Bermúdez de Castro et al., 2012). The value in Gegant-4 is lower than in adult Lower and Middle Pleistocene fossils and Neandertals but more similar to adult Upper Pleistocene H. sapiens individuals (Table 12). Adult Neandertal long bones are characterized by a pronounced hypertrophy of the cortical bone (Trinkaus, 1983), and this feature is known to appear relatively early in ontogeny (Ruff et al., 1994; Cowgill, 2010). For example, in the Dederiyeh 1 Neandertal infant, whose age at death has been estimated at around 2 years based on dental formation, the cortical bone thickness is similar to the mean of modern human children aged 5e6 years (Sawada et al., 2004). It is not surprising, then, that the cortical thickness in the Gegant-4 humerus appears elevated for its age, compared with recent humans. Discussion The combination of morphological and metric features in the Gegant-5 individual clearly indicates Neandertal affinities for the specimen. Although little can be said about the bony morphology of the mandible, the mental foramen is placed posteriorly with respect to the tooth row and is located low in the mandibular corpus. In both of these features, it is similar to the late adolescent/ adult Neandertal mandible from the same site and to adult Neandertal mandibles more generally. The dentition shows a suite of morphological features that are most consistent with a Neandertal classification. Among these is the presence of a distal accessory crest in the C1, P3, and P4. In addition, the asymmetry, continuous transverse crest, mesial placement of the lingual cusp, and presence of an accessory lingual cusp in the P4 are nearly ubiquitous features in Neandertals as well as their middle Pleistocene precursors from Atapuerca (SH). Finally, the presence of a midtrigonid crest and taurodont pulp chamber in the M1 are also most consistent with a Neandertal classification. Indeed, in most morphological details the Atapuerca (SH) population closely resembles Neandertals n-Torres et al., 2012), and the dental similarity with the (Martino Gegant-5 teeth indicates this individual is a member of the Neandertal evolutionary lineage. Metrically, all of the Gegant-5 teeth are of modest size, falling near the Atapuerca (SH) and Neandertal means in most dimensions. The Atapuerca SH sample and Neandertals have been argued to show an increase in the size of the P3 relative to that of the P4. This relative increase in the size of the P3 in the Neandertal evolutionary lineage has been linked to the expansion of the anterior dentition more generally (Bermúdez de Castro, 1993; s, 1996), and Neandertal lineage Bermudez de Castro and Nicola specimens tend to show a P3:P4 size ratio >100. The Gegant-5 individual does not show this derived Neandertal feature, with a predominance of the P4. Interestingly, a similar pattern is seen in the Valdegoba 1 Neandertal, also from the Iberian Peninsula.



13

Table 11 Cross sectional parameters of the Gegant-4 humerus at 35% of total bone length compared with an ontogenetic series of modern humans.a Specimen

Age at death (years)

AeP diameter (mm)

MeL diameter (mm)

Mean cortical thickness (mm)

Periosteal perimeter (mm)

Total area (mm2)

Cortical area (mm2)

% Cortical area (%)

Gegant-4 SK303 SK1806 SK3050 SK2020 SK1205 SK1206 SK2080 SK2023

5e7 2 3 4 6 7 8 9 10

13.0 9.5 9.8 10.4 11.3 12.3 11.7 11.9 13.7

15.3 10.1 10.4 11.8 11.9 12.8 13.3 13.4 16.2

3.3 1.1 1.5 1.9 2.1 2.2 2.3 2.2 2.3

48.6 39.4 38.9 40.2 42.3 43.4 44.1 44.3 52.2

142.3 101.2 101.8 107.3 115.6 124.5 127.6 128.4 173.2

98.7 40.6 41.2 54.0 64.2 69.0 66.1 62.2 85.2

69.3 40.2 40.4 50.3 55.5 55.4 51.8 48.3 49.2

a Modern human specimens from the medieval archaeological collection of the Priory of St Peter and St Paul, Taunton, UK. Mean cortical thickness is the average of cortical thickness on the medial, lateral, anterior, and posterior margins.

Table 12 Cortical thickness in the Gegant-4 humerus at 35% of total bone length compared with Pleistocene and recent humans.a Specimen/sample Gegant-4 ATD6-148 Atapuerca-Sima de los Huesos (n ¼ 5) Neandertals (n ¼ 10) Early Upper Paleolithic H. sapiens Late Upper Paleolithic H. sapiens a

Age at death (years)

Total area (mm2)

Cortical area (mm2)

5e7 Adult Adult Adult Adult Adult

142.3 232.7 318.82 ± 35.98 300.16 ± 52.72 269.5 ± 36.1 261.8 ± 36.9

98.7 203.4 254.96 ± 45.43 240.70 ± 45.43 200.9 ± 33.5 189.6 ± 28.6

% Cortical area (%) 69.3 90.0 79.5 80.0 74.3 72.6

± ± ± ±

8.0 5.0 4.8 8.2

Comparative data from Bermúdez de Castro et al. (2012).

Changes in the relative sizes of the individual tooth cusps have recently been shown to be a useful taxonomic tool in the M1 for Pleistocene Homo (Quam et al., 2009), and Neandertals have been characterized as derived in their M1 cusp proportions (Bailey, 2004). In contrast, few if any differences are apparent between Neandertals and modern humans in the M1 cusp proportions (Trefný, 2005). Two Neandertal specimens from the Iberian Peninsula do differ from other Neandertals in showing a somewhat larger metaconid, but the metaconid in the Gegant-5 specimen does not seem to follow this same pattern. Whether the variation in M1 cusp proportions in Neandertals consistently follows any temporal or geographic patterns can only be assessed within a larger sample of Pleistocene Homo teeth. The age at death estimate of 4.5e5.0 years in the Gegant-5 individual is younger than that derived based on modern human standards (5.5e6.8 years), but is consistent with the suggestion that dental development in Neandertals was more rapid than in modern humans (Ramirez-Rozzi and Bermúdez de Castro, 2004; Smith et al., 2007c). Smith et al. (2007c) suggest than one crucial developmental difference between Neandertals and modern humans may be an earlier onset of enamel mineralization in the former. However, further study is required to confirm this suggestion, and modern humans do show some variation in this parameter as well (Dean et al., 1993; Tompkins, 1996a; Reid et al., 1998; Liversidge, 2008). At 4.5e5.0 years of age, the M1 in the Gegant individual was already erupted, although only very slight wear is visible on the mesiobuccal cusp. This result is consistent with other studies that have claimed an advanced molar development in Neandertals (Wolpoff, 1979; Smith et al., 2010), and an early M1 eruption has important implications since many life history traits correlate strongly across primates with the emergence of the M1 (Smith, 1991a; Macho, 2001). However, hypotheses about developmental patterns in Neandertals should ideally integrate both dental and skeletal data. Although Neandertal humeri from children of similar age as the Gegant-4 specimen are rare, the present results agree with previous

studies suggesting that the thick cortical bone characteristic of adult Neandertal humeri is also present at an early ontogenetic age (Ruff et al., 1994; Sawada et al., 2004; Arsuaga et al., 2007; Cowgill, 2010). Whether this is caused by mechanical loading, genetic control, or metabolic differences between populations is currently unclear. Some authors have suggested that increased cortical robusticity in adult Neandertals and archaic H. sapiens, relative to recent modern humans, could reflect higher levels of habitual activity (Ben-Itzhak et al., 1988; Trinkaus and Churchill, 1999; Rhodes and Knüsel, 2005). Similarly, in a study of humeral growth in an archaeological modern human population, cortical area growth was found to lag behind growth in length (Sumner and Andriacchi, 1996). These authors found that by age 10 the bone had reached about 70% of adult length, but only about 45% of adult cortical area. In addition, increase in length ceased between 15 and 20 years of age, but increases in cortical area did not plateau until the early 20s. This might imply that increased mechanical loading after growth in height had ceased underpins cortical thickening, a suggestion echoed by some studies of living human cohorts (Clark et al., 2007). Nevertheless, the appearance of thickened cortices in Neandertal specimens at relatively young ages suggests some degree of genetic control is also present (Ruff et al., 1994). Minimum number of individuals (MNI) The presence of five hominin specimens in the Cova del Gegant sample suggests that some of the remains could be associated. The approximately similar ages at death for both the Gegant-4 and Gegant-5 specimens raises the possibility that these two bones represent the same individual, and indeed they were found in close spatial proximity (~170 cm apart and at the same depth), in the same geological level (layer Vf) and area (GP2) of the site. Based on age at death incompatibilities, chronological differences, and spatial separation at the site, the remaining specimens seem to represent isolated individuals. Thus, the MNI for the Gegant sample would be four if Gegant-4 and Gegant-5 are associated or five if they are not.


14


Conclusion The Cova del Gegant remains show clear Neandertal affinities and currently are the only known fossil assemblage from NE Iberia where this diagnostic morphology has been identified in a secure, well-dated stratigraphic context. The two new specimens reported here, a juvenile mandible (Gegant-5) and humerus (Gegant-4), provide evidence for rapid dental development and early postcranial cortical thickening in Neandertals. The similar age at death estimations suggest that the remains may derive from a single individual. The specimens provide new information on the anatomical variation and ontogenetic processes which characterized Neandertals and join a growing sample of Pleistocene hominin fossils from the Iberian Peninsula documenting the course of human evolution during the European Upper Pleistocene (Quam et al., 2001; Zilhao and Trinkaus, 2002; Arsuaga et al., 2002, 2007, 2012; Daura et al., 2005; Garralda, 2005; Barroso Ruiz and de Lumley, 2006; Rosas et al., 2006; Trinkaus et al., 2007; Walker et al., 2008; Willman et al., 2012). Acknowledgments This paper is an output of the research project Humans, carní al massís del Garraf-Ordal i vors i medi natural durant el Plistoce curs baix del riu Llobregat, part of the Research Project El Plistoce a Catalunya, supported by the 2014SGR-108 Superior i l'Holoce (Generalitat de Catalunya) and HAR2011-26193 (MICINN) projects. Fieldwork was sponsored by Servei d'Arqueologia i Paleontologia (2014/100639) (Generalitat de Catalunya) and Ajuntament de Sitges. A portion of this research was financed by the Ministerio de n of the Government of Spain (Grant number: Ciencia e Innovacio CGL2009-12703-C03-03). The authors thank the various curators and institutions that have kindly provided access to original fossil specimens housed under their care. CT scanning of the Gegant-5 mandible was carried out in collaboration with Jose Miguel Carre n Humana at the Universidad tero at the Laboratorio de la Evolucio de Burgos (Spain) and financed by a grant from the Junta de Castilla n (Project No. BU005A09). J. Daura was supported by a posty Leo doctoral grant (Juan de la Cierva Subprogram JCI-2011-09543). L. n AtaRodríguez has enjoyed financial support from the Fundacio n puerca and the European Social Fund of the Junta de Castilla y Leo (CPIN Project No. 03-461AA-692.01). References n Arqueolo gica en el Antiguo Ad an-Alvarez, G., 2003. Memoria de la Actuacio n, Valladolid. Monasterio de San Pablo, Burgos. Junta de Castilla y Leo zar de Vel n de la Alca azco, A., Arsuaga, J., Martínez, I., Bonmatí, A., 2011. Revisio ~ olas, Gerona, Espan ~ a. Bol. R. Soc. Esp. Hist. Nat. Sec. mandibula humana de Ban Geol. 105, 99e108. Anderson, D., Thompson, G., Popovich, F., 1976. Age of attainment of mineralization stages of the permanent dentition. J. Forensic Sci. 21, 191e200. Antoine, D., 2001. Evaluating the periodicity of incremental structures in dental enamel as a means of studying growth in children from past populations. Ph.D. dissertation, University College London, London. Arsuaga, J.L., Gracia, A., Martínez, I., Bermúdez de Castro, J.M., Rosas, A., Villaverde, V., Fumanal, M.P., 1989. The human remains from Cova Negra (Valencia, Spain) and their place in European Pleistocene human evolution. J. Hum. Evol. 18, 55e92. Arsuaga, J.L., Martìnez, I., Villaverde, V., Lorenzo, C., Quam, R., Carretero, J.M., siles humanos del Paìs Valenciano. In: Villaverde, V. (Ed.), De Gracia, A., 2001. Fo ~ ones. El Inicio del Poblamiento Humano en las Tierras Neandertales a Croman Valenicanas. Universitat de Valencia, Valencia, pp. 265e322. Arsuaga, J.L., Villaverde, V., Quam, R., Gracia, A., Lorenzo, C., Martínez, I., Carretero, J.M., 2002. The Gravettian occipital bone from the site of Malladetes (Barx, Valencia, Spain). J. Hum. Evol. 43, 381e393. Arsuaga, J.L., Villaverde, V., Quam, R., Martínez, I., Carretero, J.M., Lorenzo, C., Gracia, A., 2007. New Neandertal remains from Cova Negra (Valencia, Spain). J. Hum. Evol. 52, 31e58. , M., Dale n, L., Go € therstro €m, A., 2011. Arsuaga, J., Quam, R., Daura, J., Sanz, M., Subira Neandertal mtDNA from a Late Pleistocene human mandible from the Cova del

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[Barcelona from the Swiss viewpoint].

[New Year - Everything remains the same?].

The chronology of the earliest Upper Palaeolithic in northern Iberia: New insights from L'Arbreda, Labeko Koba and La Viña.

Europatitan eastwoodi, a new sauropod from the lower Cretaceous of Iberia in the initial radiation of somphospondylans in Laurasia.

Neandertals revised.

A new Frenguelliidae (Insecta: Odonata) from the early Eocene of Laguna del Hunco, Patagonia, Argentina.

Archaeological remains accounting for the presence and exploitation of the North Atlantic right whale Eubalaena glacialis on the Portuguese Coast (Peniche, West Iberia), 16th to 17th Century.

Four new species of hangingflies (Insecta, Mecoptera, Bittacidae) from the Middle Jurassic of northeastern China.

New studies of post-Pleistocene human skeletal remains from the Rift Valley, Kenya.

A new species of Chironius Fitzinger, 1826 from the state of Bahia, Northeastern Brazil (Serpentes: Colubridae).

The 100th: An appealing new species of Dendropsophus (Amphibia: Anura: Hylidae) from northeastern Brazil.

On the Chronological Structure of the Solutrean in Southern Iberia.

How Far into Europe Did Pikas (Lagomorpha: Ochotonidae) Go during the Pleistocene? New Evidence from Central Iberia.

Clinical highlights from the 2013 ERS Congress in Barcelona.

Reidentification of avian embryonic remains from the cretaceous of mongolia.

From Arabia to Iberia: A Y chromosome perspective.

Thermoluminescence dating of the late Neanderthal remains from Saint-Césaire.

Three new species of the genus Paraleucilla Dendy, 1892 (Porifera, Calcarea) from the coast of Bahia State, Northeastern Brazil.

Neandertals mated early with modern humans.

The clinical presentation of celiac disease: experiences from northeastern iran.

Letter from Barcelona: 14th International AIDS Conference.

Otolith patterns of rockfishes from the northeastern Pacific.

Brief communication: Investigation of the semicircular canal variation in the Krapina Neandertals.

A New Treatment-integrated Prognostic Nomogram of the Barcelona Clinic Liver Cancer System for Hepatocellular Carcinoma.