The Atapuerca human fossils

After 20 years of research, the Atapuerca sites have provided a large amount of archaeological and palaeontological remains. Human fossils have been found in three sites: Gran Dolina, galería and Sima de los Huesos. The Early Pleistocene human fossils from Gran Dolina have been ascribed to a new species,Homo antecessor, that represent the last common ancestor of Neandertals and modern humans. The Sima de los Huesos fossils and all the European Middle Pleistocene human fossils are the ancestors exclusively of the Neandertals, which evolved in Europe in conditions of geographic and genetic isolation.     

Intrapopulational body size variation and cranial capacity variation in middle pleistocene humans: The Sima de los Huesos sample (Sierra de Atapuerca,Spain)

A sexual dimorphism more marked than in living humans has been claimed for European Middle Pleistocene humans, Neandertals and prehistoric modern humans. In this paper, body size and cranial capacity variation are studied in the Sima de los Huesos Middle Pleistocene sample. This is the largest sample of non-modern humans found to date from one single site, and with all skeletal elements represented. Since the techniques available to estimate the degree of sexual dimorphism in small palaeontological samples are all unsatisfactory, we have used the bootstraping method to asses the magnitude of the variation in the Sima de los Huesos sample compared to modern human intrapopulational variation. We analyze size variation without attempting to sex the specimens a priori. Anatomical regions investigated are scapular glenoid fossa; acetabulum; humeral proximal and distal epiphyses; ulnar proximal epiphysis; radial neck; proximal femur; humeral, femoral, ulnar and tibial shaft; lumbosacral joint; patella; calcaneum; and talar trochlea. In the Sima de los Huesos sample only the humeral midshaft perimeter shows an unusual high variation (only when it is expressed by the maximum ratio, not by the coefficient of variation). In spite of that the cranial capacity range at Sima de los Huesos almost spans the rest of the European and African Middle Pleistocene range. The maximum ratio is in the central part of the distribution of modern human samples. Thus, the hypothesis of a greater sexual dimorphism in Middle Pleistocene populations than in modern populations is not supported by either cranial or postcranial evidence from Sima de los Huesos. Am J Phys Anthropol 106:19–33, 1998. © 1998 Wiley-Liss, Inc.     

Stature estimation from complete long bones in the Middle Pleistocene humans from the Sima de los Huesos, Sierra de Atapuerca (Spain)

Systematic excavations at the site of the Sima de los Huesos (SH) in the Sierra de Atapuerca (Burgos, Spain) have allowed us to reconstruct 27 complete long bones of the human species Homo heidelbergensis. The SH sample is used here, together with a sample of 39 complete Homo neanderthalensis long bones and 17 complete early Homo sapiens (Skhul/Qafzeh) long bones, to compare the stature of these three different human species. Stature is estimated for each bone using race- and sex-independent regression formulae, yielding an average stature for each bone within each taxon. The mean length of each long bone from SH is significantly greater (p < 0.05) than the corresponding mean values in the Neandertal sample. The stature has been calculated for male and female specimens separately, averaging both means to calculate a general mean. This general mean stature for the entire sample of long bones is 163.6 cm for the SH hominins, 160.6 cm for Neandertals and 177.4 cm for early modern humans. Despite some overlap in the ranges of variation, all mean values in the SH sample (whether considering isolated bones, the upper or lower limb, males or females or more complete individuals) are larger than those of Neandertals. Given the strong relationship between long bone length and stature, we conclude that SH hominins represent a slightly taller population or species than the Neandertals. However, compared with living European Mediterranean populations, neither the Sima de los Huesos hominins nor the Neandertals should be considered ‘short’ people. In fact, the average stature within the genus Homo seems to have changed little over the course of the last two million years, since the appearance of Homo ergaster in East Africa. It is only with the emergence of H. sapiens, whose earliest representatives were ‘very tall’, that a significant increase in stature can be documented.     

New foot remains from the Gran Dolina-TD6 Early Pleistocene site (Sierra de Atapuerca, Burgos, Spain)

This paper presents and describes new foot fossils from the species Homo antecessor, found in level TD6 of the site of Gran Dolina (Sierra de Atapuerca, Burgos, Spain). These new fossils consist of an almost complete left talus (ATD6-95) and the proximal three-quarters of a right fourth metatarsal (ATD6-124). The talus ATD6-95 is tentatively assigned to Hominin 10 of the TD6 sample, an adult male specimen with which the second metatarsal ATD6-70+107 (already published) is also tentatively associated. Analysis of these fossils and other postcranial remains has made possible to estimate a stature similar to those of the specimens from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca, Burgos, Spain). The morphology of the TD6 metatarsals does not differ significantly from that of modern humans, Neanderthals and the specimens from Sima de los Huesos. Talus ATD6-95, however, differs from the rest of the comparative samples in being long and high, having a long and wide trochlea, and displaying a proportionally short neck.     

Human talus bones from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca,Burgos, Spain)

Here we present and describe comparatively 25 talus bones from the Middle Pleistocene site of the Sima de los Huesos (SH) (Sierra de Atapuerca, Burgos, Spain). These tali belong to 14 individuals (11 adult and three immature). Although variation among Middle and Late Pleistocene tali tends to be subtle, this study has identified unique morphological characteristics of the SH tali. They are vertically shorter than those of Late Pleistocene Homo sapiens, and show a shorter head and a broader lateral malleolar facet than all of the samples. Moreover, a few shared characters with Neanderthals are consistent with the hypothesis that the SH population and Neanderthals are sister groups. These shared characters are a broad lateral malleolar facet, a trochlear height intermediate between modern humans and Late Pleistocene H. sapiens, and a short middle calcaneal facet. It has been possible to propose sex assignment for the SH tali based on their size. Stature estimates based on these fossils give a mean stature of 174.4 cm for males and 161.9 cm for females, similar to that obtained based on the long bones from this same site.     

Early and Middle Pleistocene hominins from Atapuerca (Spain) show differences in dental developmental patterns

The Bayesian statistical approach considers teeth as forming a developmental module, as opposed to a tooth-by-tooth analysis. This approach has been employed to analyze Upper Pleistocene hominins, including Neandertals and some anatomically modern humans, but never earlier populations. Here, we show its application on five hominins from the TD6.2 level of the Gran Dolina site (Homo antecessor, Early Pleistocene) and the Sima de los Huesos site (Middle Pleistocene) of the Sierra de Atapuerca (Burgos, northern Spain). Our results show an advanced development of the third molars in both populations with respect to modern Homo sapiens. In addition, the Sima de los Huesos hominins differ from H. sapiens and H. antecessor in the relatively advanced development of their second molar. The relative mineralization of I1/M1 in H. antecessor appears to be similar to that of modern humans, as opposed to that of Neandertals, which appear to be unique. These observations, combined with reduced enamel formation times and the advanced development of the third molars, appear to indicate a shorter ontogenetic period in the hominins from Gran Dolina and Sima de los Huesos in comparison to modern human average.     

Human hyoid bones from the middle Pleistocene site of the Sima de los Huesos (Sierra de Atapuerca, Spain)

This study describes and compares two hyoid bones from the middle Pleistocene site of the Sima de los Huesos in the Sierra de Atapuerca (Spain). The Atapuerca SH hyoids are humanlike in both their morphology and dimensions, and they clearly differ from the hyoid bones of chimpanzees and Australopithecus afarensis. Their comparison with the Neandertal specimens Kebara 2 and SDR-034 makes it possible to begin to approach the question of temporal variation and sexual dimorphism in this bone in fossil humans. The results presented here show that the degree of metric and anatomical variation in the fossil sample was similar in magnitude and kind to living humans. Modern hyoid morphology was present by at least 530 kya and appears to represent a shared derived feature of the modern human and Neandertal evolutionary lineages inherited from their last common ancestor.     

Nonocclusal dental microwear analysis of 300,000-year-old Homo heilderbergensis teeth from Sima de los Huesos (Sierra de Atapuerca, Spain)

Casts of nonocclusal enamel surfaces of 190 teeth from the Middle Pleistocene site of Sima de los Huesos have been micrographed by scanning electron microscopy. Microscopic analyses of striation density and length by orientation show distinct patterns of intrapopulation variability. Significant differences in the number and length of the striations by orientation are found between maxillary and mandibular teeth. This probably reflects differences in the mechanical forces involved in the process of chewing food. Significant differences are present between isolated and in situ teeth that could be caused by postdepositional processes differentially affecting the isolated teeth. In addition, a distinct and very unusual striation pattern is observed in a sample of teeth that can be explained only by a strong nondietary, most probably postmortem abrasion of the enamel surfaces. These teeth have a very high density of scratches, shorter in length than those found on other teeth, that are not indicative of dietary habits. No known depositional process may account for the presence of such postmortem wear since heavy transportation of materials within the clayish sediments has been discarded for the site. Despite this, a characteristic dietary striation pattern can be observed in most of the teeth analyzed. Most likely the diet of the Homo heidelbergensis hominids from Sima de los Huesos was highly abrasive, probably with a large dependence on hard, poorly processed plant foods, such as roots, stems, and seeds. A highly significant sex-related difference in the striation pattern can also be observed in the teeth analyzed, suggesting a differential consistency in the foods eaten by females and males.     

Non-masticatory uses of anterior teeth of Sima de los Huesos individuals (Sierra de Atapuerca, Spain)

In this study we examine the labial and occlusal surfaces of incisors and canines of hominins recovered from the Sima de los Huesos (SH), middle Pleistocene site, in order to establish the possible extra-masticatory use of anterior teeth. We have compared the microwear of these fossils with microwear from the anterior teeth of Australian Aborigines, a population characterized by ethnographic evidence of the use of their teeth as a third hand. These two samples of teeth were microscopically analyzed using Scanning Electron Microscopy (SEM). Our results support the “cultural” origin of microwear observed on fossil teeth: we conclude that the SH hominins used their anterior teeth as a “third hand” for para- or extra-masticatory activities.     

The Atapuerca sites and their contribution to the knowledge of human evolution in Europe

Over the last two decades, the Pleistocene sites of the Sierra de Atapuerca (Spain) have provided two extraordinary assemblages of hominin fossils that have helped refine the evolutionary story of the genus Homo in Europe. The TD6 level of the Gran Dolina site has yielded about one hundred remains belonging to a minimum of six individuals of the species Homo antecessor. These fossils, dated to the end of the Lower Pleistocene (800 kyr), provide the earliest evidence of hominin presence in Western Europe. The origin of these hominins is unknown, but they may represent a speciation event from Homo ergaster/Homo erectus. The TD6 fossils are characterized by a significant increase in cranial capacity as well as the appearance of a “sapiens” pattern of craniofacial architecture. At the Sima de los Huesos site, more than 4,000 human fossils belonging to a minimum of 28 individuals of a Middle Pleistocene population (ca. 500–400 kyr) have been recovered. These hominins document some of the oldest evidence of the European roots of Neanderthals deep in the Middle Pleistocene. Their origin would be the dispersal out of Africa of a hominin group carrying Mode 2 technologies to Europe. Comparative study of the TD6 and Sima de la Huesos hominins suggests a replacement model for the European Lower Pleistocene population of Europe or interbreeding between this population and the new African emigrants.     

Enamel hypoplasias and physiological stress in the Sima de los Huesos Middle Pleistocene hominins

This study presents an analysis of linear enamel hypoplasias (LEH) and plane-form defects (PFD) in the hominine dental sample from the Sima de los Huesos (SH) Middle Pleistocene site in Atapuerca (Spain). The SH sample comprises 475 teeth, 467 permanent and 8 deciduous, belonging to a minimum of 28 individuals. The method for recording PFD and LEH is discussed, as well as the definition of LEH. The prevalence of LEH and PFD in SH permanent dentition (unilateral total count) is 4.6% (13/280). Only one deciduous tooth (lower dc) showed an enamel disruption. Prevalence by individual ranges from 18.7-30%. The most likely explanation for the relatively low LEH and PFD prevalence in the SH sample suggests that the SH population exhibited a low level of developmental stress. The age at occurrence of LEH and PFD was determined by counting the number of perikymata between each lesion and the cervix of the tooth. Assuming a periodicity of nine days for the incremental lines, the majority of LEH in the SH sample occurred during the third year of life and may be related to the metabolic stress associated with weaning.     

Endocranial traits of the Sima de los Huesos (Atapuerca,Spain) and Petralona (Chalkidiki,Greece) Middle Pleistocene ursids. Phylogenetic and biochronological implications

A complete cranium of Ursus deningeri from Petralona (Chalkidiki, Greece) covered by a thick carbonate crust has been virtually liberated through CT scan and 3D image reconstruction, and compared with a specimen from the Sima de los Huesos, Sierra de Atapuerca (Spain) Middle Pleistocene site. X-ray computed tomography allowed for the identification of previously unrecognized and phylogenetically relevant traits. Analysis of these traits and an additional series of classically defined traits demonstrate the near identity of these specimens, thereby, confirming an early stage of the speloid “(cave bear)” condition. The replicate luminescence ages obtained for the SH deposit provide a combined minimum age estimate of 427 ± 12 ka for the underlying fossils. Based on a series of primitive and derived morphological features of these two crania, a similar age is here proposed for the Petralona and SH U. deningeri.     

Pattern of dental development in Hominid XVIII from the Middle Pleistocene Atapuerca-Sima de los Huesos site (Spain)

. We describe the pattern of dental development of Hominid XVIII from the Middle Pleistocene Sima de los Huesos (SH) site of the Sierra de Atapuerca (Burgos, Spain). As expected, this pattern is similar to that of modern humans. A delay of development of the lower and upper canines was observed. In contrast, the relative advanced development of the lower second molars and, especially, the upper and lower third molars is noteworthy. This latter feature seems to be common in Pleistocene hominids, and suggests that the pattern of dental development evolved in the genus Homo during the Pleistocene. In European Middle Pleistocene hominids, this pattern probably was facilitated by the extra space available in the mandible and maxilla for developing teeth.     

On the age of the hominid fossils at the Sima de los Huesos, Sierra de Atapuerca, Spain: paleomagnetic evidence

We report new paleomagnetic data for the Middle Pleistocene hominid-bearing strata in the Sima de los Huesos, North Spain. Sediments (brown muds with human and bear fossils and the underlying sterile clayey and sandy unit) preserve both normal and reversed magnetic components. The sterile unit has exclusively reversed magnetization, dating back to the Matuyama Chron, and thus is Lower Pleistocene in age. The overlying fossiliferous muds have a dominant normal magnetization that overprints a partially resolved reversed magnetization. These data are compatible with one of the reversal events that occurred during the Brunhes Chron. Combined with the existing U-series dates and evidence from the macro- and microfauna, these paleomagnetic results suggest an age of the hominid fossils between 325 to 205 ka, whereas the underlying sand and silts are older than 780 ka.     

Interproximal grooving in the Atapuerca-SH hominid dentitions

The dental sample recovered from the Sima de los Huesos (SH) Middle Pleistocene cave site of the Sierra de Atapuerca (Spain) includes 296 specimens. Interproximal wear grooves have been observed in 20 maxillary and mandibular posterior teeth belonging to at least five of the 32 individuals identified so far in the SH hypodigm. Interproximal grooving affected only the adults, and at an age between 25 and 40 years. The appearance, morphology, and location pattern of the SH wear grooves are similar to those reported in other fossil hominids and in more recent human populations. Two alternative proposals, the toothpicking and the fiber or sinew processing hypotheses, compete for explaining the formation of this anomalous wear. The characteristics observed in the wear grooves of the SH teeth are compatible only with the habitual probing of interdental spaces by means of hard and inflexible objects. Dietary grit may also have contributed to the abrasion of the root walls during the motion of the dental probes. Am. J. Phys. Anthropol. 102:369–376, 1997. © 1997 Wiley-Liss, Inc.     

Brain size and encephalization in early to Mid-Pleistocene Homo

Important changes in the brain have occurred during the course of human evolution. Both absolute and relative size increases can be documented for species of Homo, culminating in the appearance of modern humans. One species that is particularly well-represented by fossil crania is Homo erectus. The mean capacity for 30 individuals is 973 cm(3). Within this group there is substantial variation, but brain size increases slightly in specimens from later time periods. Other Middle Pleistocene crania differ from those of Homo erectus. Characters of the facial skeleton, vault, and cranial base suggest that fossils from sites such as Arago Cave in France, the Sima de los Huesos in Spain, Bodo in Ethiopia, Broken Hill in Zambia, and perhaps Dali in China belong to the taxon Homo heidelbergensis. Ten of these mid-Quaternary hominins have brains averaging 1,206 cm(3) in volume, and many fall beyond the limits of size predicted for Homo erectus of equivalent age. When orbit height is used to construct an index of relative brain size, it is apparent that the (significant) increase in volume documented for the Middle Pleistocene individuals is not simply a consequence of larger body mass. Encephalization quotient values confirm this finding. These changes in absolute and relative brain size can be taken as further corroborative evidence for a speciation event, in which Homo erectus produced a daughter lineage. It is probable that Homo heidelbergensis originated in Africa or western Eurasia and then ranged widely across the Old World. Archaeological traces indicate that these populations differed in their technology and behavior from earlier hominins.     

Dental size variation in the Atapuerca-SH Middle Pleistocene hominids

The Middle Pleistocene Atapuerca-Sima de los Huesos (SH) site in Spain has yielded the largest sample of fossil hominids so far found from a single site and belonging to the same biological population. The SH dental sample includes a total of 452 permanent and deciduous teeth, representing a minimum of 27 individuals. We present a study of the dental size variation in these hominids, based on the analysis of the mandibular permanent dentition: lateral incisors, n=29; canines, n=27; third premolars, n=30; fourth premolars, n=34; first molars, n=38; second molars, n=38. We have obtained the buccolingual diameter and the crown area (measured on occlusal photographs) of these teeth, and used the bootstrap method to assess the amount of variation in the SH sample compared with the variation of a modern human sample from the Museu Antropologico of the Universidade of Coimbra (Portugal). The SH hominids have, in general terms, a dental size variation higher than that of the modern human sample. The analysis is especially conclusive for the canines. Furthermore, we have estimated the degree of sexual dimorphism of the SH sample by obtaining male and female dental subsamples by means of sexing the large sample of SH mandibular specimens. We obtained the index of sexual dimorphism (ISD=male mean/female mean) and the values were compared with those obtained from the sexed modern human sample from Coimbra, and with data found in the literature concerning several recent human populations. In all tooth classes the ISD of the SH hominids was higher than that of modern humans, but the differences were generally modest, except for the canines, thus suggesting that canine size sexual dimorphism in Homo heidelbergensis was probably greater than that of modern humans. Since the approach of sexing fossil specimens has some obvious limitations, these results should be assessed with caution. Additional data from SH and other European Middle Pleistocene sites would be necessary to test this hypothesis.     

Size variation in early human mandibles and molars from Klasies River,South Africa: Comparison with other middle and late Pleistocene assemblages and with modern humans

Previous studies of the Middle Stone Age human remains from Klasies River have concluded that they exhibited more sexual dimorphism than extant populations, but these claims have not been assessed statistically. We evaluate these claims by comparing size variation in the best‐represented elements at the site, namely the mandibular corpora and M₂s, to that in samples from three recent human populations using resampling methods. We also examine size variation in these same elements from seven additional middle and late Pleistocene sites: Skhūl, Dolní Věstonice, Sima de los Huesos, Arago, Krapina, Shanidar, and Vindija. Our results demonstrate that size variation in the Klasies assemblage was greater than in recent humans, consistent with arguments that the Klasies people were more dimorphic than living humans. Variation in the Skhūl, Dolní Věstonice, and Sima de los Huesos mandibular samples is also higher than in the recent human samples, indicating that the Klasies sample was not unusual among middle and late Pleistocene hominins. In contrast, the Neandertal samples (Krapina, Shanidar, and Vindija) do not evince relatively high mandibular and molar variation, which may indicate that the level of dimorphism in Neandertals was similar to that observed in extant humans. These results suggest that the reduced levels of dimorphism in Neandertals and living humans may have developed independently, though larger fossil samples are needed to test this hypothesis. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Reconstitution 3D par Computerized-tomography (CT) et endocrâne virtuel du crâne 5 du site de la Sima de Los Huesos (Atapuerca)

The 3d Ct reconstruction and virtual brain endocast of Cranium 5 from the site of “La Sima de los Huesos” (Atapuerca), allows us to get new information to increase the study and knowledge of Homo heidelbergensis population, and to compare this specimen with others in the fossil record, in order to understand the evolutionary process of the brain, focusing on the middle Pleistocene period. Furthermore, we can observe the changes this species (Homo heidelbergensis) has undergone, at least in Sima de los Huesos population making comparative studies with African and Asian middle Pleistocene specimens. We have used the new data to compare European Homo heidelbergensis represented by SH5 with Kabwe, a controversial specimen considered by some authors like the African Homo heidelbergensis representative, in order to establish the similarities and differences between both specimens.