Ontogenetic approach to variation in Middle Pleistocene hominids. Evidence from the Atapuerca-SH mandibles

The ontogenetic processes underlying the variation detected in the European Middle Pleistocene hominids are explored. Regulation of growth parameters of the ontogenetic trajectory of these hominid is discussed in the context of heterochrony schemes. The sample of mandibles coming from the Atauuerca-SH site is used as a study case. The variability shown by these mandibles can be arranged along a morphological gradient, and study of growth directions has shown that the remodelling patterns are in line with the existence of a single morphogenetic pattern controlling the process. In addition, the spectrum of morphology detected in the Atapuerca sample virtually encompasses the entire range of variability detected in European Middle Pleistocene samples. From a morphological viewpoint, a hypermorphic pattern seems to be the responsible for the individual variation detected in the sample. Yet, when this information is related to mandibular growth and craniofacial interactions, evidence of an interindividual gradient of somatic development for the Atapuerca hominids is provided. Several hypotheses concerning growth parameters, however, may account for this gradient. Time and rate hypermorphosis hypothesis are discussed. Coincidence of the gradient of variation detected in this sample and the general mandibular growth trajectory of living species, support the hypothesis that is “time of maturation” of the organism the key factor.     

The ATD6-5 mandibular specimen from Gran Dolina (Atapuerca, Spain). Morphological study and phylogenetic implications.

Metric and shape features of the Lower Pleistocene mandibular specimen ATD605 from the level 6 of Gran Dolina site (Atapuerca, Spain) are compared with a large sample of fossil hominid mandibles. The analysis shows that ATD6-5 displays a generalized morphology largely shared with both African and European Lower and Middle Pleistocene samples. However, distinctive African traits, such as corpus robustness and strong alveolar prominence, are absent in the Gran Dolina specimen. At the same time, none of the apomorphic features that characterize Middle and early Upper Pleistocene European hominids can be recognized in ATD6-5. Finally, the Gran Dolina specimen displays a remarkable position of the mylohyoid groove, only comparable to that found in immature specimens of Homo ergaster, and very rarely in adult H. sapiens. The morphology of ATD6-5 supports the hypothesis of an African origin for the first Europeans with subsequent phylogenetic continuity with Middle Pleistocene populations in Europe. These findings are consistent with H. antecessor being the last common ancestor of Neandertals and H. sapiens.     

东亚中更新世古人类下颔第二臼齿釉质-齿质连接面三维形状和釉质厚度分布

东亚中更新世古人类在头骨、下颌骨、牙齿等解剖部位表现出不同程度的形态多样性,中期成员代表为直立人,而晚期成员的演化地位具有较大争议。为进一步了解东亚中更新世古人类内部的形态变异特点和为东亚中更新世晚期古人类分类提供依据,本文使用微分同胚的表面匹配（Diffeomorphic Surface Matching, DSM）和形态测量图（Morphometric map）对下颌第二臼齿（M₂）釉质-齿质连接面的形状和齿冠侧面釉质厚度分布模式进行了量化分析。结果显示：1）东亚中更新世古人类与晚期人属成员（尼安德特人和现代人）存在较明显的形态差别;2）该时段晚期的东亚古人类相对中期直立人在侧面釉质厚度分布规律上具有独特性,并在釉质-齿质连接面的三维形状上与晚期人属成员更加接近。本文在以往对东亚中更新世古人类牙齿内外结构单个性状研究的基础上,使用三维形态测量方法进一步量化了M₂釉质-齿质连接面三维形状和侧面釉质厚度分布模式两项重要特征的变异特点,这对未来该时段同类型牙齿的形态鉴定以及解决东亚中更新世晚期古人类的分类地位具有一定意义。     

L’approvisionnement en matières premières lithiques au Pléistocène inférieur et moyen dans la Sierra de Atapuerca, Burgos (Espagne)

This paper summarizes the latest studies on lithic raw material raising that are currently undertaken within the Sierra de Atapuerca research project. During the past two years, several works have provided new petrographical and technological data, contributing to the knowledge of the kinds of materials exploited by the Atapuerca hominids, as well as the areas where those materials were raised. The sites yielding this information are Gran Dolina (Lower and Middle Pleistocene) and Galeria (Middle Pleistocene), both located in the Trinchera del Ferrocarril archeopaleontological complex.     

Cranial discrete traits in the middle pleistocene humans from Sima de los Huesos (Sierra de Atapuerca, Spain). Does hypostosis represent any increase in "ontogenetic stress" along the Neanderthal lineage?

Cranial discrete traits may be regarded as markers of dynamic responses to general and local perturbations of the morphogenetic pattern, particularly when they are viewed and examined in terms of hypostosis vs. hyperostosis. There are indications, in fact, that the variation between these two opposite conditions relates to mechanical stress suffered by the bony structures during early stages of growth and development. In a previous comparison between Neanderthals and modern humans, variable degrees and contrasting distribution patterns of hypostosis were found [Manzi et al. (1996), JHE30: 511-527]. In the present paper, the occurrence, expression and cranial distribution of 20 hypo-hyperostotic traits are examined in the Middle Pleistocene sample from Atapuerca - Sima de los Huesos (Spain), with the principal aim being to test whether or not the degree of cranial hypostosis increases during the evolution of the Neanderthals. Other Middle Pleistocene representatives of the genus Homo (Kabwe and Petralona), the Italian Neanderthals, and a large recent European sample are also considered. A general consistency between the gradual appearance and stabilization of the Neanderthal cranial features and the results of the present analysis is found and is interpreted as an indication that hypostosis does mark the occurrence of "ontogenetic stress". As suggested more than half a century ago by S. Sergi, an increase in "ontogenetic stress" in the Neanderthal lineage could result from the relationship between intracranial pressures and other (heterochronic) effects produced by the growth of a large brain (encephalization) and the ossification of an archaic (platycephalic) cranial vault.     

Middle Pleistocene hominids from Olduvai Gorge, northern Tanzania

Cranial, dental, and mandibular remains of eight Olduvai hominids are described in detail. Four individuals were recovered in situ in Beds II to IV, while three more are most probably derived from Bed IV, the Masek Beds and the Lower Ndutu Beds. One specimen is of uncertain provenance. Deposits from which the fossils were collected range from late Lower Pleistocene to Middle Pleistocene in age. Of particular interest are three fragmentary lower jaws, which can be compared to mandibles of Homo erectus known from localities in Northwest Africa and China. Olduvai hominid 22, a nearly complete half mandible with crowns of P3-M2 in place, shares many anatomical features with fossils from Ternifine and Choukoutien. This individual is also similar to a jaw from the Kapthurin Formation west of Lake Baringo, Kenya. How best to interpret these comparisons is not clear, but in view of marked similarities between specimens representing geographically diverse populations from different time periods, it may be unwise to rely on mandibular evidence alone to document the presence of regional lineages. Gradual change and continuity within a sequence of Northwest African Homo fossils has been endorsed by many workers, but such hypotheses cannot be tested adequately with the fragmentary jaws available.     

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.     

Human mandibular incisors from the late Middle Pleistocene locality of Hoedjiespunt 1, South Africa.

The Hoedjiespunt 1 locality is an archaeological and palaeontological site located on the Hoedjiespunt Peninsula at Saldanha Bay, South Africa. In 1996 two human teeth, a left central mandibular incisor and a left lateral mandibular incisor, were discovered during excavations in the late Middle Pleistocene palaeontological layers. These teeth are described and are found to belong to a single subadult individual. Despite their developmental stage, these incisors already display early signs of wear. Their crown diameters are larger than modern and archaeological African comparative material and are most closely comparable with crown diameters of an early Middle Pleistocene and late Middle Pleistocene dental sample from Africa, Europe and Asia. In the light of this metrical evidence, data on two previously excavated maxillary molars, most probably belonging to the same individual, were re-examined. It was found that the Hoedjiespunt 1 hominid possessed dental metrical features (large anterior teeth and small molars) comparable with other African and European hominids referred to the Middle Pleistocene.     

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.     

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.     

Hominid mandibular remains from Sangiran: 1952-1986 collection

Eight hominid mandibular and associated dental remains discovered between 1952-1986 from the Early Pleistocene deposits of Sangiran, Central Java, are described. Although the specimens are surface finds, their original stratigraphic positions can be reasonably inferred on the basis of coincidental sources of information. These specimens significantly increase the dento-gnathic sample available for intensive morphological investigation of the earliest Javanese hominids [Kaifu et al., 2005].     

Posterior dental size reduction in hominids: The Atapuerca evidence

In order to reassess previous hypotheses concerning dental size reduction of the posterior teeth during Pleistocene human evolution, current fossil dental evidence is examined. This evidence includes the large sample of hominid teeth found in recent excavations (1984–1993) in the Sima de los Huesos Middle Pleistocene cave site of the Sierra de Atapuerca (Burgos, Spain). The lower fourth premolars and molars of the Atapuerca hominids, probably older than 300 Kyr, have dimensions similar to those of modern humans. Further, these hominids share the derived state of other features of the posterior teeth with modern humans, such as a similar relative molar size and frequent absence of the hypoconulid, thus suggesting a possible case of parallelism. We believe that dietary changes allowed size reduction of the posterior teeth during the Middle Pleistocene, and the present evidence suggests that the selective pressures that operated on the size variability of these teeth were less restrictive than what is assumed by previous models of dental reduction. Thus, the causal relationship between tooth size decrease and changes in food-preparation techniques during the Pleistocene should be reconsidered. Moreover, the present evidence indicates that the differential reduction of the molars cannot be explained in terms of restriction of available growth space. The molar crown area measurements of a modern human sample were also investigated. The results of this study, as well as previous similar analyses, suggest that a decrease of the rate of cell proliferation, which affected the later-forming crown regions to a greater extent, may be the biological process responsible for the general and differential dental size reduction that occurred during human evolution. © 1995 Wiley-Liss, Inc.     

Enamel hypoplasia in the Middle Pleistocene hominids from Atapuerca (Spain)

The prevalence and chronology of enamel hypoplasias were studied in a hominid dental sample from the Sima de los Huesos (SH) Middle Pleistocene site at the Sierra de Atapuerca (Burgos, northern Spain). A total of 89 permanent maxillary teeth, 143 permanent mandibular teeth, and one deciduous lower canine, belonging to a minimum of 29 individuals, were examined. Excluding the antimeres (16 maxillary and 37 mandibular cases) from the sample, the prevalence of hypoplasias in the permanent dentition is 12.8% (23/179), whereas the deciduous tooth also showed an enamel defect. No statistically significant differences were found between both arcades and between the anterior and postcanine teeth for the prevalence of hypoplasias. In both the maxilla and the mandible the highest frequency of enamel hypoplasias was recorded in the canines. Only one tooth (a permanent upper canine) showed two different enamel defects, and most of the hypoplasias were expressed as faint linear horizontal defects. Taking into account the limitations that the incompleteness of virtually all permanent dentitions imposes, we have estimated that the frequency by individual in the SH hominid sample was not greater than 40%. Most of the hypoplasias occurred between birth and 7 years (N = 18, X = 3.5, SD = 1.3). Both the prevalence and severity of the hypoplasias of the SH hominid sample are significantly less than those of a large Neandertal sample. Furthermore, prehistoric hunter-gatherers and historic agricultural and industrial populations exhibit a prevalence of hypoplasias generally higher than that of the SH hominids. Implications for the survival strategies and life quality of the SH hominids are also discussed. © 1995 Wiley-Liss, Inc.     

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.     

Evolution of middle-late Pleistocene human cranio-facial form: A 3-D approach

The classification and phylogenetic relationships of the middle Pleistocene human fossil record remains one of the most intractable problems in paleoanthropology. Several authors have noted broad resemblances between European and African fossils from this period, suggesting a single taxon ancestral to both modern humans and Neanderthals. Others point out ‘incipient’ Neanderthal features in the morphology of the European sample and have argued for their inclusion in the Neanderthal lineage exclusively, following a model of accretionary evolution of Neanderthals. We approach these questions using geometric morphometric methods which allow the intuitive visualization and quantification of features previously described qualitatively. We apply these techniques to evaluate proposed cranio-facial ‘incipient’ facial, vault, and basicranial traits in a middle-late Pleistocene European hominin sample when compared to a sample of the same time depth from Africa. Some of the features examined followed the predictions of the accretion model and relate the middle Pleistocene European material to the later Neanderthals. However, although our analysis showed a clear separation between Neanderthals and early/recent modern humans and morphological proximity between European specimens from OIS 7 to 3, it also shows that the European hominins from the first half of the middle Pleistocene still shared most of their cranio-facial architecture with their African contemporaries.     

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.     

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.