Morphological description and comparison of the dental remains from Atapuerca-Sima de los Huesos site (Spain).

The systematic excavation of the Sima de los Huesos (SH) site in Sierra de Atapuerca (Burgos, Spain) has yielded the largest hominin collection worldwide for the Middle Pleistocene. The dental sample now consists of more than 500 teeth that provide exceptional opportunities to define the dental morphological pattern of a Middle Pleistocene population as well as develop hypotheses about the origins of the Neanderthals. The dental collection has now increased to over 533 specimens (525 permanent and 8 deciduous teeth), necessitating new morphological assessments. Thus, we present a detailed morphological description of the SH permanent dentition recovered up to 2007, accomplishing comparisons with European Middle Pleistocene hominins, Neanderthals, and early and contemporary Homo sapiens. We find that SH dentitions present all the morphological traits that, either in their degree of expression, frequency, or particular combination, are usually considered as typical of Homo neanderthalensis. This study ratifies the deep roots of the Neanderthal lineage in the Middle Pleistocene of Europe. In addition, SH teeth are morphologically "more Neanderthal" than other penecontemporaneous Middle Pleistocene samples such as Mauer or Arago, and even more derived than some classic Neanderthal samples. Thus, our study would not sustain the linearity of the accretion process hypothesized for the origins of the Neanderthals, and we suggest that other evolutionary models and scenarios should be explored for the Middle and Upper Pleistocene of Europe. We propose that more than one hominin lineage may have coexisted during the Middle Pleistocene in Europe.

Martinón-Torres M ，Bermúdez de Castro JM ，Gómez-Robles A ，Prado-Simón L ，Arsuaga JL ... -  《-》

Dental remains of the Middle Pleistocene hominins from the Sima de los Huesos site (Sierra de Atapuerca, Spain): Mandibular dentition.

The Middle Pleistocene site of the Sima de los Huesos (Sierra de Atapuerca, northern Spain) has yielded a considerable number of human fossils during the period 1984-2020. Among them, up to 314 mandibular teeth have been identified. In this second paper dedicated to the dentition we present the description of the eight dental classes of the mandible following the Arizona State University Dental Anthropology System (ASUDAS) classification. In addition, we show the mean mesiodistal and buccolingual diameters obtained in these teeth compared to those of Neanderthals and a modern human sample. The morphology of both the anterior and posterior teeth suggests a close relationship of the Sima de los Huesos hominins with the populations of the second half of the Middle Pleistocene of Europe and the Near East, as well as with the so-called classic Neanderthals of Europe. The combination of dental traits in these populations is characteristic and diagnostic and suggests grouping the Sima de los Huesos hominins with the other paleodemes in a Neanderthal clade. The dental evidence of the Sima de los Huesos hominins is key to propose a complex model for the settlement of Europe during the Middle Pleistocene. In this period, different migrations of human groups probably coming from Southwest Asia, replacements, prolonged isolations, as well as hybridization and introgression processes would have contributed to the diversity of hominins in Europe.

Bermúdez de Castro JM ，Martínez de Pinillos M ，Martín-Francés L ，Modesto-Mata M ，García-Campos C ，Arsuaga JL ，Martinón-Torres M ... -  《-》

Dental remains of the Middle Pleistocene hominins from the Sima de los Huesos site (Sierra de Atapuerca, Spain): Maxillary dentition.

The Middle Pleistocene site of the Sima de los Huesos (Sierra de Atapuerca, northern Spain) has yielded a considerable number of human fossils during the period 1984-2020. Among them, up to 253 maxillary teeth have been recovered. In this article, we present the description of the eight dental classes of the maxilla following the Arizona State University Dental Anthropology System classification. In addition, we present the mean mesiodistal and buccolingual diameters of these teeth compared to those of Neanderthals and a modern human sample. The morphology of both the anterior and posterior teeth suggests a close relationship of the Sima de los Huesos hominins with the populations of the second half of the Middle Pleistocene of Europe and the Near East, as well as with the so-called classic Neanderthals of Europe. Features with a recognizable taxonomic signal allow grouping the Sima de los Huesos hominins with different paleodemes into a Neanderthal clade. The dental evidence of the Sima de los Huesos hominins is key to suggest a complex model for the settlement of Europe during the Middle Pleistocene. During this period, different migrations of human groups probably coming from Southwest Asia, replacements, prolonged isolations, as well as hybridization and introgression processes would have contributed to the diversity of hominins in Europe.

Bermúdez de Castro JM ，Martínez de Pinillos M ，Martín-Francés L ，Modesto-Mata M ，García-Campos C ，Arsuaga JL ，Martinón-Torres M ... -  《-》

The Neandertal nature of the Atapuerca Sima de los Huesos mandibles.

The recovery of additional mandibular fossils from the Atapuerca Sima de los Huesos (SH) site provides new insights into the evolutionary significance of this sample. In particular, morphological descriptions of the new adult specimens are provided, along with standardized metric data and phylogenetically relevant morphological features for the expanded adult sample. The new and more complete specimens extend the known range of variation in the Atapuerca (SH) mandibles in some metric and morphological details. In other aspects, the addition of new specimens has made it possible to confirm previous observations based on more limited evidence. Pairwise comparisons of individual metric variables revealed the only significant difference between the Atapuerca (SH) hominins and Neandertals was a more vertical symphysis in the latter. Similarly, principal components analysis of size-adjusted variables showed a strong similarity between the Atapuerca (SH) hominins and Neandertals. Morphologically, the Atapuerca (SH) mandibles show nearly the full complement of Neandertal-derived features. Nevertheless, the Neandertals differ from the Atapuerca (SH) mandibles in showing a high frequency of the H/O mandibular foramen, a truncated, thinned and inverted gonial margin, a high placement of the mylohyoid line at the level of the M3, a more vertical symphysis and somewhat more pronounced expression of the chin structures. Size-related morphological variation in the SH hominins includes larger retromolar spaces, more posterior placement of the lateral corpus structures, and stronger markings associated with the muscles of mastication in larger specimens. However, phylogenetically relevant features in the SH sample are fairly stable and do not vary with the overall size of the mandible. Direct comparison of the enlarged mandibular sample from Atapuerca (SH) with the Mauer mandible, the type specimen of H. heidelbergensis, reveals important differences from the SH hominins, and there is no morphological counterpart of Mauer within the SH sample, suggesting the SH fossils should not be assigned to this taxon. The Atapuerca (SH) mandibles show a greater number of derived Neandertal features, particularly those related to midfacial prognathism and in the configuration of the superior ramus, than other European middle Pleistocene specimens. This suggests that more than one evolutionary lineage co-existed in the middle Pleistocene, and, broadly speaking, it appears possible to separate the European middle Pleistocene mandibular remains into two distinct groupings. One group shows a suite of derived Neandertal features and includes specimens from the sites of Atapuerca (SH), Payre, l'Aubesier and Ehringsdorf. The other group includes specimens that generally lack derived Neandertal features and includes the mandibles from the sites of Mauer, Mala Balanica, Montmaurin and (probably) Visogliano. The two published Arago mandibles differ strongly from one another, with Arago 2 probably belonging to this former group, and Neandertal affinities being more difficult to identify in Arago 13. Outside of the SH sample, derived Neandertal features in the mandible only become more common during the second half of the middle Pleistocene. Acceptance of a cladogenetic pattern of evolution during the European middle Pleistocene has the potential to reconcile the predictions of the accretion model and the two phases model for the appearance of Neandertal morphology. The precise taxonomic classification of the SH hominins must contemplate features from the dentition, cranium, mandible and postcranial skeleton, all of which are preserved at the SH site. Nevertheless, the origin of the Neandertal clade may be tied to a speciation event reflected in the appearance of a suite of derived Neandertal features in the face, dentition and mandible, all of which are present in the Atapuerca (SH) hominins. This same suite of features also provides a useful anatomical basis to include other European middle Pleistocene mandibles and crania within the Neandertal clade.

Quam R ，Martínez I ，Rak Y ，Hylander B ，Pantoja A ，Lorenzo C ，Conde-Valverde M ，Keeling B ，Ortega Martínez MC ，Arsuaga JL ... -  《-》

Dentine morphology of Atapuerca-Sima de los Huesos lower molars: Evolutionary implications through three-dimensional geometric morphometric analysis.

This study aims to explore the affinities of the Sima de los Huesos (SH) population in relation to Homo neanderthalensis, Arago, and early and contemporary Homo sapiens. By characterizing SH intra-population variation, we test current models to explain the Neanderthal origins. Three-dimensional reconstructions of dentine surfaces of lower first and second molars were produced by micro-computed tomography. Landmarks and sliding semilandmarks were subjected to generalized Procrustes analysis and principal components analysis. SH is often similar in shape to Neanderthals, and both groups are generally discernible from Homo sapiens. For example, the crown height of SH and Neanderthals is lower than for modern humans. Differences in the presence of a mid-trigonid crest are also observed, with contemporary Homo sapiens usually lacking this feature. Although SH and Neanderthals show strong affinities, they can be discriminated based on certain traits. SH individuals are characterized by a lower intra-population variability, and show a derived dental reduction in lower second molars compared to Neanderthals. SH also differs in morphological features from specimens that are often classified as Homo heidelbergensis, such as a lower crown height and less pronounced mid-trigonid crest in the Arago fossils. Our results are compatible with the idea that multiple evolutionary lineages or populations coexisted in Europe during the Middle Pleistocene, with the SH paradigm phylogenetically closer to Homo neanderthalensis. Further research could support the possibility of SH as a separate taxon. Alternatively, SH could be a subspecies of Neanderthals, with the variability of this clade being remarkably higher than previously thought.

Hanegraef H ，Martinón-Torres M ，Martínez de Pinillos M ，Martín-Francés L ，Vialet A ，Arsuaga JL ，Bermúdez de Castro JM ... -  《-》