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.     

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.     

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.     

Combined ESR/U-series chronology of Acheulian hominid-bearing layers at Trinchera Galería site,Atapuerca, Spain

The Sierra de Atapuerca, northern Spain, is known from many prehistoric and palaeontological sites documenting human prehistory in Europe. Three major sites, Gran Dolina, Galería and Sima del Elefante, range in age from the oldest hominin of Western Europe dated to 1.1 to 1.3 Ma (millions of years ago) at Sima del Elefante to c.a. 0.2 Ma on the top of the Galería archaeological sequence. Recently, a chronology based on luminescence methods (Thermoluminescence [TL] and Infrared Stimulated Luminescence [IRSL]) applied to cave sediments was published for the Gran Dolina and Galería sites. The authors proposed for Galería an age of 450 ka (thousands of years ago) for the units lower GIII and GII, suggesting that the human occupation there is younger than the hominid remains of Sima de los Huesos (>530 ka) around 1 km away.     

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.     

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.     

The human cranial remains from Gran Dolina Lower Pleistocene site (Sierra de Atapuerca, Spain).

In this article we study the cranial remains of the late Lower Pleistocene human fossils from Gran Dolina (Sierra de Atapuerca, Spain), assigned to the new species Homo antecessor. The cranial remains belong to at least five individuals, both juveniles and adults. The most outstanding feature is the totally modern human morphology of the very complete face ATD6-69, representing the earliest occurrence of the modern face in the fossil record. The Gran Dolina fossils show in the face a suite of modern human apomorphies not found in earlier hominids nor in contemporary or earlier Homo erectus fossils. There are also traits in the Gran Dolina fossils shared with both Neandertals and modern humans, which reinforce the hypothesis that Neandertals and modern humans form a clade, and that the Gran Dolina fossils are a common ancestor to both lineages.     

A geometric morphometric analysis of hominin upper premolars. Shape variation and morphological integration

This paper continues the series of articles initiated in 2006 that analyse hominin dental crown morphology by means of geometric morphometric techniques. The detailed study of both upper premolar occlusal morphologies in a comprehensive sample of hominin fossils, including those coming from the Gran Dolina-TD6 and Sima de los Huesos sites from Atapuerca, Spain, complement previous works on lower first and second premolars and upper first molars. A morphological gradient consisting of the change from asymmetric to symmetric upper premolars and a marked reduction of the lingual cusp in recent Homo species has been observed in both premolars. Although percentages of correct classification based on upper premolar morphologies are not very high, significant morphological differences between Neanderthals (and European middle Pleistocene fossils) and modern humans have been identified, especially in upper second premolars. The study of morphological integration between premolar morphologies reveals significant correlations that are weaker between upper premolars than between lower ones and significant correlations between antagonists. These results have important implications for understanding the genetic and functional factors underlying dental phenotypic variation and covariation.     

Updated Atapuerca biostratigraphy: Small-mammal distribution and its implications for the biochronology of the Quaternary in Spain

The Sierra de Atapuerca (Burgos, Spain) contains the most comprehensive archaeological and paleontological evidence of human evolution in Europe during the Quaternary. The time scale based on the microfossil content of the sedimentary infillings of the caves of Atapuerca has been used to attribute relative ages to the various paleontological and archaeological levels and correlate amongst the different sites. Microfossils are particularly significant as they are the dominant constituents of the caves from the Pleistocene to the Holocene of the Sierra de Atapuerca. The microfossils of the Atapuerca sites are mainly composed of isolated bones and teeth from small vertebrates, and the hard tissue of the vertebrate skeleton can be taxonomically classified. In revisiting the distribution and the classification of the small-mammal taxa along five of the main stratigraphic sequences from Atapuerca (Sima del Elefante, Gran Dolina, Galería-Zarpazos, Sima de los Huesos, and Portalón), we apply a new method, the “Unitary Associations” method, in order to refine the existing biozones, adding five new Faunal Units, and interpret their relative age. Finally, we correlate Atapuerca with other Pleistocene sites of Europe.     

Metric and morphological study of the upper cervical spine from the Sima de los Huesos site (Sierra de Atapuerca, Burgos, Spain)

In this article, the upper cervical spine remains recovered from the Sima de los Huesos (SH) middle Pleistocene site in the Sierra de Atapuerca (Burgos, Spain) are described and analyzed. To date, this site has yielded more than 5000 human fossils belonging to a minimum of 28 individuals of the species Homo heidelbergensis. At least eleven individuals are represented by the upper cervical (C1 and C2) specimens: six adults and five subadults, one of which could represent an adolescent individual. The most complete adult vertebrae (three atlases and three axes) are described, measured, and compared with other fossil hominins and modern humans. These six specimens are associated with one another and represent three individuals. In addition, one of these sets of cervical vertebrae is associated with Cranium 5 (Individual XXI) from the site. The metric analysis demonstrates that the Sima de los Huesos atlases and axes are metrically more similar to Neandertals than to our modern human comparative sample. The SH atlases share with Neandertals a sagittally elongated canal. The most remarkable feature of the SH (and Neandertal) axes is that they are craniocaudally low and mediolaterally wide compared to our modern male sample. Morphologically, the SH sample shares with Neandertals a higher frequency of caudally projected anterior atlas arch, which could reflect greater development of the longus colli muscle. In other features, such as the frequency of weakly developed tubercles for the attachment of the transverse ligament of the atlas, the Sima de los Huesos fossils show intermediate frequencies between our modern comparative samples and the Neandertals, which could represent the primitive condition. Our results are consistent with the previous phylogenetic interpretation of H. heidelbergensis as an exclusively European species, ancestral only to H. neanderthalensis.     

The medial pterygoid tubercle in the Atapuerca Early and Middle Pleistocene mandibles: Evolutionary implications

Numerous studies have attempted to identify the presence of uniquely derived (autoapomorphic) Neandertal features. Here, we deal with the medial pterygoid tubercle (MTP), which is usually present on the internal face of the ascending ramus of Neandertal specimens. Our study stems from the identification of a hypertrophied tubercle in ATD6‐96, an Early Pleistocene mandible recovered from the TD6 level of the Atapuerca‐Gran Dolina site and attributed to Homo antecessor. Our review of the literature and study of numerous original fossil specimens and high quality replicas confirm that the MTP occurs at a high frequency in Neandertals (ca. 89%) and is also present in over half (ca. 55%) of the Middle Pleistocene Sima de los Huesos (SH) hominins. In contrast, it is generally absent or minimally developed in other extinct hominins, but can be found in variable frequencies (<ca. 25%) in Pleistocene and recent H. sapiens samples. The presence of this feature in ATD6‐96 joins other traits shared by H. antecessor, the SH hominins and Neandertals. Since the TD6 hominins have been attributed either to MIS 21 or to MIS 25, it seems that a suite of assumed derived Neandertal features appeared in the Early Pleistocene, and they should be interpreted as synapomorphies shared among different taxa. We suggest that H. antecessor, the SH hominins and Neandertals shared a common ancestor in which these features appeared during the Early Pleistocene. The presence of the MTP in taxa other than H. neanderthalensis precludes this feature from being a Neandertal autapomorphy. Am J Phys Anthropol 156:102–109, 2015 © 2014 Wiley Periodicals, Inc.     

Twentieth anniversary of Homo antecessor (1997‐2017): a review

It has been twenty years since diagnosis and publication of the species Homo antecessor.¹ Since then, new human fossils recovered from the TD6 level of the Gran Dolina site (Sierra de Atapuerca, northern Spain) have helped to refine its taxonomic and phylogenetic position. In this paper, we present a synthesis of the most characteristic features of this species, as well as our interpretation derived from the latest investigations. We focus on the phylogenetic interpretation of Homo antecessor, taking into account the most recent paleogenetic analyses and a reassessment of the European Middle Pleistocene hominin record. We try to show that, twenty years after its publication, H. antecessor provides a good opportunity to address the morphology of the last common ancestor of Neandertals and modern humans.     

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.     

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.     

Right‐handed fossil humans

Fossil hominids often processed material held between their upper and lower teeth. Pulling with one hand and cutting with the other, they occasionally left impact cut marks on the lip (labial) surface of their incisors and canines. From these actions, it possible to determine the dominant hand used. The frequency of these oblique striations in an array of fossil hominins documents the typically modern pattern of 9 right‐ to 1 left‐hander. This ratio among living Homo sapiens differs from that among chimpanzees and bonobos and more distant primate relatives. Together, all studies of living people affirm that dominant right‐handedness is a uniquely modern human trait. The same pattern extends deep into our past. Thus far, the majority of inferred right‐handed fossils come from Europe, but a single maxilla from a Homo habilis, OH‐65, shows a predominance of right oblique scratches, thus extending right‐handedness into the early Pleistocene of Africa. Other studies show right‐handedness in more recent African, Chinese, and Levantine fossils, but the sample compiled for non‐European fossil specimens remains small. Fossil specimens from Sima del los Huesos and a variety of European Neandertal sites are predominately right‐handed. We argue the 9:1 handedness ratio in Neandertals and the earlier inhabitants of Europe constitutes evidence for a modern pattern of handedness well before the appearance of modern Homo sapiens.     

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.     

Restauration virtuelle d’Arago 21

Discovered in 1971 by Henry and Marie-Antoinette de Lumley, Arago 21 is the oldest complete human face from Europe. Three-dimensional virtual imaging methods were used to isolate the fossil fragments before articulating them according to their anatomical constraints. This new reconstruction of Arago 21, the first virtual one, was then compared by Procrustes superimposition to Pleistocene European, Asian and African fossils. These results, limited to the frontal bone, highlight the proximity between Arago 21 and fossils like Sima de los Huesos 5. However, anatomical and metric differences remain.     

再论南京直立人高鼻梁的成因

本文以周口店、南京、Atapuerca SH5、Petralona、Arago、Bodo、Kabwe的中更新世人类化石举例显示,在类似的环境中鼻梁高耸的程度可以不同,不同凉热可以有相似高耸的鼻梁,从而对南京直立人的高鼻梁不是由于对寒冷气候的适应的论点提出补充论证。在这样的情况下,自然应该考虑南京直立人鼻梁高耸的原因在于遗传的因素。本文试图探讨南京高耸鼻梁可能的基因来源,首先论证在中国化石人类中罕见高耸的鼻梁,更没有比南京更早的高耸鼻梁,而非洲和欧洲中更新世多见高耸鼻梁,这种状态在欧洲延续至今,而且非洲已经发现60万年前的比南京早的高耸鼻梁。最后讨论南京直立人的时代和与非洲、欧洲相距遥远的地理位置都不能否定本文的推论。     

Luminescence chronology of cave sediments at the Atapuerca paleoanthropological site, Spain

Ascertaining the timing of the peopling of Europe, after the first out-of-Africa demographic expansion at the end of the Pliocene, is of great interest to paleoanthropologists. One of the earliest direct evidences for fossil hominins in western Europe comes from an infilled karstic cave site called Gran Dolina at Atapuerca, in a stratum approximately 1.5m below the Brunhes-Matuyama (B-M) geomagnetic boundary (780ka) within lithostratigraphic unit TD6. However, most of the meters of fossil- and tool-bearing strata at Gran Dolina have been difficult to date. Therefore, we applied both thermoluminescence (TL) and infrared-stimulated-luminescence (IRSL) multi-aliquot dating methods to fine-silt fractions from sediment samples within Gran Dolina and the nearby Galería cave site. We also applied these methods to samples from the present-day surface soils on the surrounding limestone hill slopes to test the luminescence-clock-zeroing-by-daylight assumption. Within the uppermost 4m of the cave deposits at Gran Dolina, TL and paired TL and IRSL ages range stratigraphically from 198+/-19ka to 244+/-26ka. Throughout Gran Dolina, all luminescence results are stratigraphically self-consistent and, excepting results from two stratigraphic units, are consistent with prior ESR-U-series ages from progressively deeper strata. Thermoluminescence ages culminate at 960+/-120ka approximately 1m below the 780ka B-M boundary. At Galería, with one exception, TL and IRSL ages range stratigraphically downward from 185+/-26ka to 503+/-95ka at the base of the lowermost surface-inwash facies. These results indicate that TL and (sometimes) IRSL are useful dating tools for karstic inwash sediments older than ca. 100ka, and that a more accurate chronostratigraphic correlation is now possible among the main Atapuerca sites (Gran Dolina, Galería, Sima de los Huesos). Furthermore, the oldest TL age of ca. 960ka from Gran Dolina, consistent with biostratigraphic and paleomagnetic evidence, implies a probable numeric age of 900-950ka for the oldest hominin remains ( approximately 0.8m below the TL sample). This age window suggests a correspondence to Marine Isotope Stage (MIS) 25, a relatively warm and humid interglaciation.